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Aphids are serious pests of many crops in agroecosystems and their biological control is focused on enhancing the performance of specialized natural enemies of aphids such as parasitoid wasps and predators like ladybirds. However, ladybirds are often attacked by their own parasitoids in the fourth trophic level that can negatively affect ladybird performance and, hence, their effectiveness as control agents. The biology and ecology of these parasitoids has been less well explored. This study compared various life-history traits in two closely related parasitoids of the seven-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae): Oomyzus scaposus and O. spiraculus (Hymenoptera: Eulophidae), which naturally co-occur in eastern China and are facultatively gregarious koinobiont larval-pupal endoparasitoids of ladybird beetles. They can oviposit and develop in all four larval instars of their hosts but kill and emerge from the pupae. Both parasitoids did not have a clear oviposition preference for any host instar, but oviposition duration tended to increase in first to third instar hosts. Moreover, oviposition time was significantly longer for O. spiraculus than for O. scaposus. Adult eclosion from parasitized hosts (ranging between 35 and 45%) and sex ratios (85–90% female) were similar in both species and did not differ among host instars. Brood sizes were similar in both species but tended to increase in first to third instar hosts. Egg-to-adult development time was shorter and the eclosing adults of O. scaposus were heavier than those of O. spiraculus. In both species, development time decreased with host instar at parasitism, but instar-specific effects on biomass differed between the two species: heavier O. scaposus adults developed from second and third instar hosts, whereas biomass of for O. spiraculus tended to decrease with instar at parasitism. In both species, females were significantly larger than males. Our results show that expression of some of the life-history traits vary depending on which instar is parasitized, but do not point at a specific instar optimal for each of the parasitoids. Moreover, despite being closely related, there is some variability in the expression of life-history traits in both parasitoids.

Endophytic bacteria are known for their ability in promoting plant growth and defense against biotic and abiotic stress. However, very little is known about the microbial endophytes living in the spermosphere. Here, we isolated bacteria from the seeds of five different populations of wild cabbage (Brassica oleracea L) that grow within 15 km of each other along the Dorset coast in the UK. The seeds of each plant population contained a unique microbiome. Sequencing of the 16S rRNA genes revealed that these bacteria belong to three different phyla (Actinobacteria, Firmicutes, and Proteobacteria). Isolated endophytic bacteria were grown in monocultures or mixtures and the effects of bacterial volatile organic compounds (VOCs) on the growth and development on B. oleracea and on resistance against a insect herbivore was evaluated. Our results reveal that the VOCs emitted by the endophytic bacteria had a profound effect on plant development but only a minor effect on resistance against an herbivore of B. oleracea. Plants exposed to bacterial VOCs showed faster seed germination and seedling development. Furthermore, seed endophytic bacteria exhibited activity via volatiles against the plant pathogen F. culmorum. Hence, our results illustrate the ecological importance of the bacterial seed microbiome for host plant health and development., Here, we isolated bacteria from the seeds of five different populations of wild cabbage (Brassica oleracea L.) that grow within 15 km of each other along the Dorset coast in the UK. The seeds of each plant population contained a unique set of bacteria. We tested the effect of these bacterial endophytes on the growth and development on wild cabbage and on resistance against an insect herbivore (Mamestra brassicae) and a plant pathogenic fungus (Fusarium culmorum). Our results reveal the endophytic bacteria had a profound effect on plant development and health but only a minor effect on resistance against an herbivore insect.

Changes in the frequency, duration, and intensity of rainfall events are among the abiotic effects predicted under anthropogenic global warming. Heavy downpours may profoundly affect the development and survival of small organisms such as insects. Here, we examined direct (physically on the insects) and indirect (plant‐mediated) effects of simulated downpours on the performance of caterpillars of two lepidopteran herbivores (Plutella xylostella and Pieris brassicae) feeding on black mustard (Brassica nigra) plants. Host plants were exposed to different rainfall regimes both before and while caterpillars were feeding on the plants in an attempt to separate direct and indirect (plant‐mediated) effects of rainfall on insect survival and development. In two independent experiments, downpours were simulated as a single long (20 min) or as three short (5 min) daily events. Downpours had a strong negative direct effect on the survival of P. xylostella, but not on that of P. brassicae. Direct effects of downpours consistently increased development time of both herbivore species, whereas effects on body mass depended on herbivore species and downpour frequency. Caterpillar disturbance by rain and recorded microclimatic cooling by 5°C may explain extended immature development. Indirect, plant‐mediated effects of downpours on the herbivores were generally small, despite the fact that sugar concentrations were reduced and herbivore induction of secondary metabolites (glucosinolates) was enhanced in plants exposed to rain. Changes in the frequency of precipitation events due to climate change may impact the survival and development of insect herbivores differentially. Broader effects of downpours on insects and other arthropods up the food chain could seriously impair and disrupt trophic interactions, ultimately destabilizing communities.

Summary Evolutionary arms‐races between plants and insect herbivores have long been proposed to generate key innovations such as plant toxins and detoxification mechanisms that can drive diversification of the interacting species. A novel front‐line of plant defence is the killing of herbivorous insect eggs.We test whether an egg‐killing plant trait has an evolutionary basis in such a plant–insect arms‐race. Within the crucifer family (Brassicaceae), some species express a hypersensitive response (HR)‐like necrosis underneath butterfly eggs (Pieridae) that leads to eggs desiccating or falling off the plant. We studied the phylogenetic distribution of this trait, its egg‐killing effect on and elicitation by butterflies, by screening 31 Brassicales species, and nine Pieridae species.We show a clade‐specific induction of strong, egg‐killing HR‐like necrosis mainly in species of the Brassiceae tribe including Brassica crops and close relatives. The necrosis is strongly elicited by pierid butterflies that are specialists of crucifers. Furthermore, HR‐like necrosis is linked to PR1 defence gene expression, accumulation of reactive oxygen species and cell death, eventually leading to egg‐killing.Our findings suggest that the plants’ egg‐killing trait is a new front on the evolutionary arms‐race between Brassicaceae and pierid butterflies beyond the well‐studied plant toxins that have evolved against their caterpillars.

Plant chemical defences impact not only herbivores, but also organisms in higher trophic levels that prey on or parasitize herbivores. While herbivorous insects can often detoxify plant chemicals ingested from suitable host plants, how such detoxification affects endoparasitoids that use these herbivores as hosts is largely unknown. Here, we used transformed plants to experimentally manipulate the major detoxification reaction used by Plutella xylostella (diamondback moth) to deactivate the glucosinolate defences of its Brassicaceae host plants. We then assessed the developmental, metabolic, immune, and reproductive consequences of this genetic manipulation on the herbivore as well as its hymenopteran endoparasitoid Diadegma semiclausum. Inhibition of P. xylostella glucosinolate metabolism by plant-mediated RNA interference increased the accumulation of the principal glucosinolate activation products, the toxic isothiocyanates, in the herbivore, with negative effects on its growth. Although the endoparasitoid manipulated the excretion of toxins by its insect host to its own advantage, the inhibition of herbivore glucosinolate detoxification slowed endoparasitoid development, impaired its reproduction, and suppressed the expression of genes of a parasitoid-symbiotic polydnavirus that aids parasitism. Therefore, the detoxification of plant glucosinolates by an herbivore lowers its toxicity as a host and benefits the parasitoid D. semiclausum at multiple levels.

1. Parasitoid females foraging for hosts rely on cues derived from the insect host, the host plant and/or their interaction, and all of these can be learned during the immature and adult stages. 2. The present study investigated the importance of rearing history on foraging behaviour of Diaeretiella rapae, an endoparasitoid often associated with aphids feeding on brassicaceous plant species. 3. Parasitoids were reared on one of the four possible combinations, comprising two brassicaceous host plant species, Brassica nigra or Raphanus sativus, and two aphid species Brevicoryne brassicae or Myzus persicae. These parasitoids were tested in a Y‐tube olfactometer and given the choice between volatiles emitted by an aphid‐infested plant (25 or 100 aphids per plant) and an uninfested control plant. The parasitoid's responses were compared when offered: (i) the same plant–aphid combination as the one on which it had been reared; (ii) the same host plant infested with the alternative aphid species; or (iii) an alternative plant with the alternative aphid species. 4. Aphid density did affect the behavioural responses to the various odour sources, but rearing history did not. Diaeretiella rapae only preferred aphid‐induced to non‐induced plant volatiles at low aphid infestation level, whereas they did not discriminate between volatiles at high aphid infestation level. 5. It is concluded that aphid‐induced volatiles of brassicaceous plants play an important role during host habitat location, but seem less important for parasitoids to locate the aphid host itself. The data are discussed in the light of manipulation of host plant defences by aphids.

Levels of plant secondary metabolites are not static and often change in relation to plant ontogeny. They also respond to abiotic and biotic changes in the environment, e.g., they often increase in response to biotic stress, such as herbivory. In contrast with short-lived annual plant species, especially those with growing periods of less than 2–3 months, investment in defensive compounds of vegetative tissues in biennial and perennial species may also vary over the course of an entire growing season. In garden experiments, we investigated the dynamics of secondary metabolites, i.e. glucosinolates (GSLs) in the perennial wild cabbage (Brassica oleracea), which was grown from seeds originating from three populations that differ in GSL chemistry. We compared temporal long-term dynamics of GSLs over the course of two growing seasons and short-term dynamics in response to herbivory by Pieris rapae caterpillars in a more controlled greenhouse experiment. Long-term dynamics differed for aliphatic GSLs (gradual increase from May to December) and indole GSLs (rapid increase until mid-summer after which concentrations decreased or stabilized). In spring, GSL levels in new shoots were similar to those found in the previous year. Short-term dynamics in response to herbivory primarily affected indole GSLs, which increased during the 2-week feeding period by P. rapae. Herbivore-induced changes in the concentrations of aliphatic GSLs were population-specific and their concentrations were found to increase in primarily one population only. We discuss our results considering the biology and ecology of wild cabbage.

Several studies have shown that pre-infestation with aphids can improve plant quality for herbivorous caterpillars. This effect is often explained by the negative crosstalk between specific plant defence, signal-transduction pathways induced by aphids and caterpillars, respectively. However, in these studies caterpillars are introduced on the plants by the researcher, whereas in nature, the adult mother often chooses the food plants for her offspring. According to the preference–performance hypothesis adult females should choose oviposition sites that result in optimal performance and survival of their offspring. In this study, we investigated whether three lepidopteran species–Pieris brassicae (L.) (Pieridae), Plutella xylostella L. (Plutellidae) and Mamestra brassicae L. (Noctuidae)–prefer aphid-infested over clean plants. Adult females of the three species was given the choice between wild cabbage (Brassica oleracea L., Brassicaceae) plants infested with aphids, Brevicoryne brassicae (L.) (Hemiptera: Aphididae) for 3, 7, or 14 days vs. non-infested clean plants. Pieris brassicae females was also given the choice between plants dually infested with B. brassicae aphids and P. xylostella caterpillars when the order of infestation was varied. For oviposition, adult females of all three species did not discriminate between aphid-infested and clean plants, irrespective of the duration of aphid infestation. Also, P. brassicae females did not discriminate between sets of dually infested plants, irrespective of the order of infestation. Several mechanisms are discussed that could explain this lack of preference.

Global climatic changes may lead to the arrival of multiple range-expanding species from different trophic levels into new habitats, either simultaneously or in quick succession, potentially causing the introduction of manifold novel interactions into native food webs. Unraveling the complex biotic interactions between native and range-expanding species is critical to understand the impact of climate change on community ecology, but experimental evidence is lacking. In a series of laboratory experiments that simulated direct and indirect species interactions, we investigated the effects of the concurrent arrival of a range-expanding insect herbivore in Europe, Spodoptera littoralis, and its associated parasitoid Microplitis rufiventris, on the native herbivore Mamestra brassicae, and its associated parasitoid Microplitis mediator, when co-occurring on a native plant, Brassica rapa. Overall, direct interactions between the herbivores were beneficial for the exotic herbivore (higher pupal weight than the native herbivore), and negative for the native herbivore (higher mortality than the exotic herbivore). At the third trophic level, both parasitoids were unable to parasitize the herbivore they did not coexist with, but the presence of the exotic parasitoid still negatively affected the native herbivore (increased mortality) and the native parasitoid (decreased parasitism rate), through failed parasitism attempts and interference effects. Our results suggest different interaction scenarios depending on whether S. littoralis and its parasitoid arrive to the native tritrophic system separately or concurrently, as the negative effects associated with the presence of the parasitoid were dependent on the presence of the exotic herbivore. These findings illustrate the complexity and interconnectedness of multitrophic changes resulting from concurrent species arrival to new environments, and the need for integrating the ecological effects of such arrivals into the general theoretical framework of global invasion patterns driven by climatic change.

The effects of temporal variation in the quality of short-lived annual plants on oviposition preference and larval performance of insect herbivores has thus far received little attention. This study examines the effects of plant age on female oviposition preference and offspring performance in the large cabbage white butterfly Pieris brassicae. Adult female butterflies lay variable clusters of eggs on the underside of short-lived annual species in the family Brassicaceae, including the short-lived annuals Brassica nigra and Sinapis arvensis, which are important food plants for P. brassicae in The Netherlands. Here, we compared oviposition preference and larval performance of P. brassicae on three age classes (young, mature, and pre-senescing) of B. nigra and S. arvensis plants. Oviposition preference of P. brassicae declined with plant age in both plant species. Whereas larvae performed similarly on all three age classes in B. nigra, preference and performance were weakly correlated in S. arvensis. Analysis of primary (sugars and amino acids) and secondary (glucosinolates) chemistry in the plant shoots revealed that differences in their quality and quantity were more pronounced with respect to tissue type (leaves vs. flowers) than among different developmental stages of both plant species. Butterflies of P. brassicae may prefer younger and smaller plants for oviposition anticipating that future plant growth and size is optimally synchronized with the final larval instar, which contributes >80% of larval growth before pupation. Electronic supplementary material The online version of this article (doi:10.1007/s10886-017-0853-9) contains supplementary material, which is available to authorized users.

Adult dietary regimes in insects may affect egg production, fecundity and ultimately fitness. This is especially relevant in parasitoid wasps where many species serve as important biological control agents of agricultural pests. Here, we tested the effect of honey and sugar diets on daily fecundity schedules, lifetime reproductive success and longevity in four species of parasitoid wasps when reared on their respective hosts. The parasitoid species were selected based on dichotomies in host usage strategies and reproductive traits. Gelis agilis and G. areator are idiobiont ecto-parasitoids that develop in non-growing hosts, feed on protein-rich host fluids to maximize reproduction as adults and produce small numbers of large eggs. Meteorus pulchricornis and Microplitis mediator are koinobiont endoparasitoids that develop inside the bodies of growing hosts, do not host-feed, and produce greater numbers of small eggs. Parasitoids were reared on diets of either pure honey (containing trace amounts of proteins), heated honey (with denatured proteins) and a honey-mimic containing sugars only. We hypothesized that the benefits of proteins in honey would enhance reproduction in the ectoparasitoids due to their high metabolic investment per egg, but not in the koinobionts. Pure honey diet resulted in higher lifetime fecundity in G. agilis compared with the honey-mimic, whereas in both koinobionts, reproductive success did not vary significantly with diet. Longevity was less affected by diet in all of the parasitoids, although there were variable trade-offs between host access and longevity in the four species. We argue that there are both trait-based and association-specific effects of supplementary nutrients in honey on reproductive investment and success in parasitoid wasps.

Plant responses to dual herbivore attack are increasingly studied, but effects on the metabolome have largely been restricted to volatile metabolites and defence-related non-volatile metabolites. However, plants subjected to stress, such as herbivory, undergo major changes in both primary and secondary metabolism. Using a naturally occurring system, we investigated metabolome-wide effects of single or dual herbivory on Brassica nigra plants by Brevicoryne brassicae aphids and Pieris brassicae caterpillars, while also considering the effect of aphid density. Metabolomic analysis of leaf material showed that single and dual herbivory had strong effects on the plant metabolome, with caterpillar feeding having the strongest influence. Additionally, aphid-density-dependent effects were found in both the single and dual infestation scenarios. Multivariate analysis revealed treatment-specific metabolomic profiles, and effects were largely driven by alterations in the glucosinolate and sugar pools. Our work shows that analysing the plant metabolome as a single entity rather than as individual metabolites provides new insights into the subcellular processes underlying plant defence against multiple herbivore attackers. These processes appear to be importantly influenced by insect density.

In addition to controlling pest organisms, the systemic neurotoxic pesticide fipronil can also have adverse effects on beneficial insects and other non-target organisms. Here, we report on the sublethal effects of fipronil on the farmland butterfly Pieris brassicae . Caterpillars were reared on plants that had been grown from seeds coated with fipronil or on leaf discs topically treated with a range of fipronil dosages (1–32 µg kg −1 on dry mass basis). Females that had developed on fipronil plants laid ca half the number of eggs than females that had developed on control plants. In the bioassay with leaf discs, longevity and lifetime egg production declined with increasing fipronil dosage. Remarkably, exposure to fipronil during larval development primarily affected the adult stage. Chemical analyses of leaf tissues collected from seed-treated plants revealed concentrations of fipronil and its degradation products close to the analytical limit of detection (less than or equal to 1 µg kg −1 ). The effective dosage was fivefold higher in the leaf-disc than in the whole-plant experiment. In the whole plant, degradation of fipronil to products that are more toxic than fipronil may explain this discrepancy. Neurotoxicity of insecticides at the level of detection decreases the probability of pinpointing insecticides as the causal agent of harmful effects on non-target organisms.

In three Dutch populations of the native small hogweed (Heracleum sphondylium L. [Apiales: Apiaceae]), and one of the invasive giant hogweed (H. mantegazzianum Sommeier & Levier [Apiales: Apiaceae]), interactions between a specialist herbivore, the parsnip webworm (Depressaria radiella), and its associated parasitoids were compared during a single growing season. We found host plant species-related differences in the abundance of moth pupae, the specialist polyembryonic endoparasitoid, Copidosoma sosares, the specialist pupal parasitoid, Barichneumon heracliana, and a potential hyperparasitoid of C. sosares, Tyndaricus scaurus Walker (Hymenoptera: Encyrtidae). Adult D. radiella body mass was similar across the three small hogweed populations, but moths and their pupal parasitoid B. heracliana were smaller when developing on giant than on small hogweeds where the two plants grew in the same locality (Heteren). Mixed-sex and all-male broods of C. sosares were generally bigger than all-female broods. Furthermore, adult female C. sosares were larger than males and adult female mass differed among the three small hogweed populations. The frequency of pupal parasitism and hyperparasitism also varied in the different H. sphondylium populations. These results show that short-term (intra-seasonal) effects of plant population on multitrophic insects are variable among different species in a tightly linked food chain.

In natural populations of insect herbivores, genetic differentiation is likely to occur due to variation in host plant utilization and selection by the local community of organisms with which they interact. In parasitoids, engaging in intimate associations with their host during immature development, local variation may exist in host quality for parasitoid development. We compared the development of a gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae), collected in The Netherlands, in three strains and three caterpillar instars (L1?L3) of its main host, Pieris brassicae L. (Lepidoptera: Pieridae). Hosts had been collected in The Netherlands and France, and were reared in the laboratory for one generation. We also used an established Dutch laboratory strain that had not been exposed to parasitoids for at least 24 generations. Parasitoid survival to adulthood was inversely correlated with host instar at parasitism. Adult parasitoid body mass was largest when hosts were parasitized as L1 and smallest when hosts were parasitized as L3, whereas egg-to-adult development time was quickest on L3 hosts and slowest on L1 hosts. Higher survival and faster development of C. glomerata on French L2 hosts also showed that there is variation in host-instar-related suitability. Many L2 and most L3 caterpillars that were parasitized exhibited signs of pathogen infection and perished within a few days of parasitism, whereas this never happened when hosts were parasitized as L1 or in non-parasitized control caterpillars. Our results reveal that, irrespective of the host strain, L1 hosts are optimally synchronized with C. glomerata development. By contrast, the high precocious mortality of L3 larvae may be due to stress-induced regulation by the parasitoid in order to ?force? its developmental program into synchrony with the developing parasitoid larvae. Our results underscore a potentially important role played by pathogens in mediating herbivore?parasitoid interactions that are host-instar-dependent in their expression.

Plants are commonly attacked by a variety of insect herbivores and have developed specific defenses against different types of attackers. At the molecular level, herbivore-specific signalling pathways are activated by plants in response to attackers with different feeding strategies. Feeding by leaf-chewing herbivores predominantly activates jasmonic acid (JA)-regulated defenses, whereas feeding by phloem-sucking herbivores generally activates salicylic acid (SA)-regulated defenses. When challenged sequentially by both phloem-sucking and leaf-chewing herbivores, SA-JA antagonism may constrain the plant’s ability to timely and adequately divert defense to the second herbivore that requires activation of a different defensive pathway. We investigated the effect of the temporal sequence of infestation by the aphid Brevicoryne brassicae and three caterpillar species, Plutella xylostella, Pieris brassicae, and Mamestra brassicae, on the interaction between JA and SA signal-transduction pathways in three wild cabbage populations. We found no support for SA-JA antagonism, irrespective of the temporal sequence of herbivore introduction or the identity of the caterpillar species based on the transcript levels of the JA- and SA-regulated marker genes LOX and PR-1, respectively, at the examined time points, 6, 24, and 48 h. In general, infestation with aphids alone had little effect on the transcript levels of the two marker genes, whereas the three caterpillar species upregulated not only LOX but also PR-1. Transcriptional changes were different for plants from the three different natural cabbage populations.

The effects of multiple insect attacks on herbivore-induced plant volatiles and carnivorous arthropods are increasingly studied. Phytopathogens also represent an important threat to plants, and plant defence strategies against pathogens and insects are strongly interconnected, yet the potential impact of pathogens on insect-induced volatiles has been largely overlooked, and degree of pathogenicity is rarely considered. We investigated how pathogen challenge, with virulent and avirulent strains of Xanthomonas campestris either alone or with simultaneous Pieris brassicae caterpillar herbivory, affected the volatile emissions of Brassica nigra plants. The impact of these volatiles on the foraging behaviour of Cotesia glomerata parasitoids wasps was then assessed. Pathogens themselves induced volatiles that were highly attractive to parasitoids, and enhanced the attractiveness of host-infested plant volatiles. Chemical analyses revealed that virulent and avirulent strains differentially induced plant volatiles, with primarily sesquiterpene, homoterpene and green leaf volatile compounds contributing to the differences. Strong similarities were found in the blends induced by the virulent strain and caterpillar herbivory. Challenge by either virulent or avirulent pathogens has a significant impact on plant chemistry and its interactions with other community members, demonstrating the importance of integrating pathogen- and insect-based research to broaden our knowledge of plant defences under conditions of increasing complexity.

Changes in the arthropod community structure can be attributed to differences in constitutively expressed plant traits or those that change depending on environmental conditions such as herbivory. Early-season herbivory may have community-wide effects on successive insect colonisation of host plants and the identity of the initially inducing insect may determine the direction and strength of the effects on the dynamics and composition of the associated insect community. 2. Previous studies have addressed the effect of early infestation with a chewing herbivore. In the present study, the effect of early infestation was investigated with a phloem-feeding aphid [Brevicoryne brassicae L. (Hemiptera, Aphididae)] on the insect community associated with three wild cabbage (Brassica oleracea L.) populations, which are known to differ in defence chemistry, throughout the season in field experiments. 3. Aphid infestation had asymmetric effects on the associated insect community and only influenced the abundance of the natural enemies of aphids, but not that of chewing herbivores and their natural enemies. The effect size of aphid infestation further depended on the cabbage population. 4. Aphid feeding has been previously reported to promote host-plant quality for chewing herbivores, which has been attributed to antagonism between the two major defence signalling pathways controlled by the hormones salicylic acid (SA) and jasmonic acid (JA), respectively. Our results show no effects of early infestation by aphids on chewing herbivores, suggesting the absence of long-term JA–SA antagonism. 5. Investigating the effects of the identity of an early-season coloniser and genotypic variation among plant populations on insect community dynamics are important in understanding insect–plant community ecology.

Closely related species in nature usually exhibit very similar phylogenetically conserved traits, such as reproduction, behavior and development. Here, we compared fecundity schedules, lifetime reproductive success and offspring sex ratios in three congeneric facultative hyperparasitoid wasps that exhibit several overlapping traits and which co-occur in the same small-scale habitats. Gelis agilis, G. proximus and G. hortensis are abundant in meadows and forest edge habitats in the Netherlands. Gelis agilis is asexual (all female), whereas the other two species reproduce sexually. Here they developed on cocoons of the primary parasitoid Cotesia glomerata. When provided with unlimited hosts, lifetime reproductive success was three times higher in G. proximus than in G. agilis with G. hortensis producing intermediate numbers of offspring. All three species depleted their teneral reserves during their lives. Females of G. proximus and G. hortensis lived significantly longer than females of G. agilis. Offspring sex ratios in young G. proximus mothers were female-biased and marginally male-biased in G. hortensis. As mothers aged, however, the ratio of male:female progeny produced rapidly increased until no daughters emerged later in life. Our results reveal significant differences in reproductive traits among the three species despite them co-occurring in the same microhabitats, being very closely related and morphologically similar. The increase in the production of male progeny by Gelis mothers over time suggests a depletion in sperm number or viability with age. This is especially interesting, given that Gelis species are among the least fecund parasitoids thus far studied. It is likely that in the field most Gelis mothers are probably only able to parasitize a few hosts and to maintain the production of female offspring.

Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource?consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels). Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons). We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens. Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature-dependent. In turn, the observed effects of AGW on the functional responses of the hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article.

Insect parasitoids can play ecologically important roles in virtually all terrestrial plant-insect herbivore interactions, yet whether parasitoids alter the defensive traits that underlie interactions between plants and their herbivores remains a largely unexplored question. Here, we examined the reciprocal trophic interactions among populations of the wild cabbage Brassica oleracea that vary greatly in their production of defensive secondary compounds - glucosinolates (GSs), a generalist herbivore, Trichoplusia ni, and its polyembryonic parasitoid Copidosoma floridanum. In a greenhouse environment, plants were exposed to either healthy (unparasitized), parasitized, or no herbivores. Feeding damage by herbivores induced higher levels of the indole GSs, glucobrassicin and neoglucobrassicin, but not any of the other measured GSs. Herbivores parasitized by C. floridanum induced cabbage plants to produce 1.5 times more indole GSs than levels induced by healthy T. ni and five times more than uninduced plants. As a gregarious endoparasitoid, C. floridanum causes its host T. ni to feed more than unparasitized herbivores resulting in increased induction of indole GSs. In turn, herbivore fitness parameters (including differential effects on male and female contributions to lifetime fecundity in the herbivore) were negatively correlated with the aliphatic GSs, sinigrin and gluconapin, whereas parasitoid fitness parameters were negatively correlated with the indole GSs, glucobrassicin and neoglucobrassicin. That herbivores and their parasitoids appear to be affected by different sets of GSs was unexpected given the intimate developmental associations between host and parasitoid. This study is the first to demonstrate that parasitoids, through increasing feeding by their herbivorous hosts, can induce higher levels of non-volatile plant chemical defenses. While parasitoids are widely recognized to be ubiquitous in most terrestrial insect herbivore communities, their role in influencing plant-insect herbivore relationships is still vastly underappreciated.

Insects feeding on aboveground and belowground tissues can influence each other through their shared plant and this is often mediated by changes in plant chemistry. We examined the effects of belowground root fly (Delia radicum) herbivory on the performance of an aboveground herbivore (Plutella xylostella) and its endoparasitoid wasp (Cotesia vestalis). Insects were reared on three populations of wild cabbage (Brassica oleracea) plants, exhibiting qualitative and quantitative differences in root and shoot defense chemistry, that had or had not been exposed to root herbivory. In addition, we measured primary (amino acids and sugars) and secondary [glucosinolate (GS)] chemistry in plants exposed to the various plant population-treatment combinations to determine to what extent plant chemistry could explain variation in insect performance variables using multivariate statistics. In general, insect performance was more strongly affected by plant population than by herbivory in the opposite compartment, suggesting that population-related differences in plant quality are larger than those induced by herbivory. Sugar profiles were similar in the three populations and concentrations only changed in damaged tissues. In addition to population-related differences, amino acid concentrations primarily changed locally in response to herbivory. Whether GS concentrations changed in response to herbivory (indole GS) or whether there were only population-related differences (aliphatic GS) depended on GS class. Poor correlations between performance and chemical attributes made biological interpretation of these results difficult. Moreover, trade-offs between life history traits suggest that factors other than food nutritional quality contribute to the expression of life history traits.

1. Herbivory can change plant quality, which may have consequences for interactions between the inducing herbivore and other insect community members. 2. Studies investigating the effects of plant quality on herbivore performance often have neglected the egg stage, and instead introduced larvae onto the plant. Recently, we reported that herbivore oviposition by Pieris brassicae (Linnaeus) (Large Cabbage White Butterfly) reduced the plant quality of Brassica nigra L. (black mustard) for subsequent herbivores. 3. It remains unclear how persistent and common these plant-mediated effects of oviposition are. Here, five species of wild Brassicaceae were used (B. nigra L., Brassica oleracea L., Sinapis arvensis L., Moricandia arvensis L., and Moricandia moricandioides Boiss). The response to oviposition by the specialist P. brassicae was determined by following the natural sequence of events: oviposition, egg, larval, and pupal development. All tested plant species are known to interact with P. brassicae in nature. Caterpillar, pupal mass, and development time on plants exposed to butterfly eggs were assessed compared with egg-free plants. 4. It was shown that the plant-mediated effects of oviposition are not specific for B. nigra but occur in most of the tested plant species except for M. arvensis. However, the strength of the plant-mediated effect on caterpillar growth depended on plant species. Thus, across different members of the Brassicaceae family, oviposition can influence plant quality and has negative consequences on P. brassicae growth. Further studies are needed to assess to what extent this trait might be phylogenetically conserved.

A recent study showed that a wingless parasitoid, Gelis agilis, exhibits a suite of ant-like traits that repels attack from wolf spiders. When agitated, G. agilis secreted 6-methyl-5-hepten-2-one (sulcatone), which a small number of ant species produce as an alarm/panic pheromone. Here, we tested four Gelis parasitoid species, occurring in the same food chain and microhabitats, for the presence of sulcatone and conducted two-species choice bioassays with wolf spiders to determine their degree of susceptibility to attack. All four Gelis species, including both winged and wingless species, produced sulcatone, whereas a closely related species, Acrolyta nens, and the more distantly related Cotesia glomerata, did not. In two-choice bioassays, spiders overwhelmingly rejected the wingless Gelis species, preferring A. nens and C. glomerata. However, spiders exhibited no preference for either A. nens or G. areator, both of which are winged. Wingless gelines exhibited several ant-like traits, perhaps accounting for the reluctance of spiders to attack them. On the other hand, despite producing sulcatone, the winged G. areator more closely resembles other winged cryptines like A. nens, making it harder for spiders to distinguish between these two species. C. glomerata was also preferred by spiders over A. nens, suggesting that other non-sulcatone producing cryptines nevertheless possess traits that make them less attractive as prey. Phylogenetic reconstruction of the Cryptinae reveals that G. hortensis and G. proximus are ‘sister’species, with G. agilis, and G.areator in particular evolving along more distant trajectories. We discuss the possibility that wingless Gelis species have evolved a suite of ant-like traits as a form, of mimicry to repel predators on the ground.

11 páginas, 5 figuras y 3 tablas., Studies reporting domestication efects on plant defences have focused on constitutive, but not on induced defences. However, theory predicts a trade-of between constitutive (CD) and induced defences (ID), which intrinsically links both defensive strategies and argues for their joint consideration in plant domestications studies. We measured constitutive and induced glucosinolates in wild cabbage (Brassica oleracea ssp. oleracea) and two domesticated varieties (B. oleracea var. acephala and B. oleracea var. capitata) in which the leaves have been selected to grow larger. We also estimated leaf area (proxy of leaf size) to assess size-defence trade-ofs and whether domestication efects on defences are indirect via selection for larger leaves. Both CD and ID were lower in domesticated than in wild cabbage and they were negatively correlated (i.e. traded of) in all of the cabbage lines studied. Reductions in CD were similar in magnitude for leaves and stems, and CD and leaf size were uncorrelated. We conclude that domestication of cabbage has reduced levels not only constitutive defences but also their inducibility, and that reductions in CD may span organs not targeted by breeding. This reduction in defences in domesticated cabbage is presumably the result of direct selection rather than indirect efects via trade-ofs between size and defences., This research was fnancially supported by a Regional Government of Galicia Grant (IN607D 2016/001), a Spanish National Research Grant (AGL2015–70748-R) and the Ramón y Cajal Research Programme (RYC-2013-13230) to XM. MF was supported by the Juan de la Cierva Programme (IJCI-2014-19653).

Wind is an important abiotic factor that influences an array of biological processes, but it is rarely considered in studies on plant-herbivore interactions. Here, we tested whether wind exposure could directly or indirectly affect the performance of two insect herbivores, Plutella xylostella and Pieris brassicae, feeding on Brassica nigra plants. In a greenhouse study using a factorial design, B. nigra plants were exposed to different wind regimes generated by fans before and after caterpillars were introduced on plants in an attempt to separate the effects of direct and indirect wind exposure on herbivores. Wind exposure delayed flowering, decreased plant height and increased leaf concentrations of amino acids and glucosinolates. Plant-mediated effects of wind on herbivores, that is effects of exposure of plants to wind prior to herbivore feeding, were generally small. However, development time of both herbivores was extended and adult body mass of P. xylostella was reduced when they were directly exposed to wind. By contrast, wind-exposed adult P. brassicae butterflies were significantly larger, revealing a trade-off between development time and adult size. Based on these results, we conducted a behavioural experiment to study preference by an avian predator, the great tit (Parus major) for last instar P. brassicae caterpillars on plants that were exposed to either control (no wind) or wind (fan-exposed) treatments. Tits captured significantly more caterpillars on still than on wind-exposed plants. Our results suggest that P. brassicae caterpillars are able to perceive the abiotic environment and to trade off the costs of extended development time against the benefits of increased size depending on the perceived risk of predation mediated by wind exposure. Such adaptive phenotypic plasticity in insects has not yet been described in response to wind exposure.

Among parasitoids that develop inside the bodies of feeding, growing hosts (so-called ‘koinobiont’ endoparasitoids), two strategies have evolved to dispose of host resources. The larvae of one group consumes most host tissues before pupation, whereas in the other the parasitoid larvae consume only host hemolymph and fat body and at maturity emerge through the host cuticle to pupate externally. Here we compared development and survival (to adult emergence) of two related larval endoparasitoids (Braconidae: Microgastrinae) of the diamondback moth, Plutella xylostella. Larvae of Dolichogenidea sicaria are tissue feeders whereas larvae of Cotesia vestalis are hemolymph feeders. Here, development of P. xylostella and the two parasitoids was compared on three populations (one cultivar [Cyrus], two wild, [Winspit and Kimmeridge]) of cabbage that have been shown to vary in direct defense and hence quality. Survival of P. xylostella and C. vestalis (to adult eclosion) did not vary with cabbage population, but did so in D. sicaria, where survival was lower when reared on the wild populations than on the cultivar. Furthermore, adult herbivore mass was significantly higher and development was significantly shorter in moths reared on the cultivar. The tissue-feeing D. sicaria was larger but took longer to develop than the hemolymph-feeder C. vestalis. The performance of both parasitoids was better on the cabbage cultivar than on the wild populations, although the effects were less apparent than in the host. Our results show that (1) differences in plant quality are diffused up the food chain, and (2) the effects of host quality are reflected on the development of both parasitoids.

Crop domestication is the process of artificially selecting plants to increase their suitability to human requirements: taste, yield, storage, and cultivation practices. There is increasing evidence that crop domestication can profoundly alter interactions among plants, herbivores, and their natural enemies. Overall, little is known about how these interactions are affected by domestication in the geographical ranges where these crops originate, where they are sympatric with the ancestral plant and share the associated arthropod community. In general, domestication consistently has reduced chemical resistance against herbivorous insects, improving herbivore and natural enemy performance on crop plants. More studies are needed to understand how changes in morphology and resistance-related traits arising from domestication may interact with environmental variation to affect species interactions across multiple scales in agroecosystems and natural ecosystems.

1. Plant traits that enhance the attraction of the natural enemies of their herbivores have been postulated to function as an ‘indirect defence’. An important underlying assumption is that this enhanced attraction results in increased plant fitness due to reduced herbivory. This assumption has been rarely tested. 2. We investigated whether there are fitness consequences for the charlock mustard Sinapis arvensis, a short-lived outcrossing annual weedy plant, when exposed to groups of large cabbage white (Pieris brassicae) caterpillars parasitized by either one of two wasp species, Hyposoter ebeninus and Cotesia glomerata, that allow the host to grow during parasitism. Hyposoter ebeninus is solitary and greatly reduces host growth compared with healthy caterpillars, whereas C. glomerata is gregarious and allows the host to grow approximately as large as unparasitized caterpillars. Both healthy and parasitized P. brassicae caterpillars initially feed on the foliage, but later stages preferentially consume the flowers. 3. In a garden experiment, plants damaged by parasitized caterpillars produced more seeds than conspecific plants damaged by unparasitized caterpillars. Reproductive potential (germination success multiplied by total seed number) was similar for plants that were not exposed to herbivory and those that were damaged by parasitized caterpillars and lower for plants that were damaged by healthy unparasitized caterpillars. However, these quantitative seed traits negatively correlated with the qualitative seed traits, individual seed size and germination success, suggesting a trade-off between these two types of traits. 4. We show that parasitism of insect herbivores that feed on reproductive plant tissues may have positive fitness consequences for S. arvensis. The extent to which plant fitness may benefit depends on parasitoid lifestyle (solitary or gregarious), which is correlated with the amount of damage inflicted on these tissues by the parasitized host.

1. In nature, several parasitoid species often exploit the same stages of a common herbivore host species and are able to coexist despite competitive interactions amongst them. Less is known about the direct effects of resource quality on intrinsic interactions between immature parasitoid stages. The present study is based on the hypothesis that variation in the quality or type of plant resources on which the parasitoids indirectly develop may be complementary and thus facilitate niche segregation favouring different parasitoids in intrinsic competition under different dietary regimes. 2. The present study investigated whether two herbivore species, the cabbage butterflies Pieris brassicae and Pieris rapae (Pieridae), and the quality of two important food plants, Brassica oleracea and Brassica nigra (Brassicaceae), affect the outcome of intrinsic competition between their primary larval endoparasitoids, the gregarious Cotesia glomerata (Braconidae) and the solitary Hyposoter ebeninus (Ichneumonidae). 3. Hyposoter ebeninus is generally an intrinsically superior competitor over C.glomerata. However, C.glomerata survived more antagonistic encounters with H.ebeninus when both developed in P.brassicae rather than in P.rapae caterpillars, and while its host was feeding on B.nigra rather than B.oleracea. Moreover, H.ebeninus benefitted from competition by its higher survival in multiparasitised hosts. 4. These results show that both plant and herbivore species mediate the battleground on which competitive interactions between parasitoids are played out and may affect the outcomes of these interactions in ways that enable parasitoids to segregate their niches. This in turn may promote coexistence among parasitoid species that are associated with the same herbivore host.

Summary Low-dose crosstalk between jasmonic acid and salicylic acid signalling pathways results in a dynamic plant phenotype in terms of plant volatile emission and behavioural responses of an herbivorous spider mite., The jasmonic acid (JA) and salicylic acid (SA) signalling pathways, which mediate induced plant defence responses, can express negative crosstalk. Limited knowledge is available on the effects of this crosstalk on host-plant selection behaviour of herbivores. We report on temporal and dosage effects of such crosstalk on host preference and oviposition-site selection behaviour of the herbivorous spider mite Tetranychus urticae towards Lima bean (Phaseolus lunatus) plants, including underlying mechanisms. Behavioural observations reveal a dynamic temporal response of mites to single or combined applications of JA and SA to the plant, including attraction and repellence, and an antagonistic interaction between SA- and JA-mediated plant responses. Dose-response experiments show that concentrations of 0.001mM and higher of one phytohormone can neutralize the repellent effect of a 1mM application of the other phytohormone on herbivore behaviour. Moreover, antagonism between the two signal-transduction pathways affects phytohormone-induced volatile emission. Our multidisciplinary study reveals the dynamic plant phenotype that is modulated by subtle changes in relative phytohormonal titres and consequences for the dynamic host-plant selection by an herbivore. The longer-term effects on plant–herbivore interactions deserve further investigation.

Plants respond to herbivory with the emission of plant volatiles, which can be used by the herbivores' natural enemies to locate their hosts or prey. In nature, plants are often simultaneously confronted with insect herbivores and phytopathogens, potentially interfering with the attraction of the herbivores' enemies as a result of modifications of the induced volatile blend. Here, we investigated parasitoid (Cotesia glomerata) attraction to volatiles of plants challenged by different attackers, either alone or in combination with Pieris brassicae caterpillars, hosts of C. glomerata. We used a natural system consisting of Brassica nigra plants, eggs and larvae of P. brassicae, Brevicoryne brassicae aphids and the bacterial phytopathogen Xanthomonas campestris pv. campestris. In all cases, parasitoids successfully located host-infested plants, and wasp foraging behaviour was unaffected by the simultaneous presence of a non-host attacker or host eggs. Analysis of the volatile emissions show that the volatile blends of caterpillar-infested treatments were different from those without caterpillars. Furthermore, dually attacked plants could not be separated from those with only caterpillars, regardless of non-host identity, supporting the behavioural data. Our results suggest that, in this system, indirect plant defences may be more resistant to interference than is generally assumed, with volatiles induced during dual attack remaining reliable indicators of host presence for parasitoids.

Attack by multiple herbivores often leads to modification of induced plant defenses compared to single herbivory, yet little is known about the effects on induced indirect plant defense. Here, we investigated the effect of sequential induction of plant defense by Mamestra brassicae caterpillar oral secretion and an infestation by Tetranychus urticae spider mites on the expression of indirect plant defense in Lima bean plants. The effect on indirect defense was assessed using behavior assays with the specialist predatory mite Phytoseiulus persimilis in an olfactometer, headspace analysis of 11 major herbivore-induced plant volatiles (HIPVs) including (E)-β-ocimene, and transcript levels of the corresponding gene Phaseolus lunatus (E)-β-ocimene synthase (PlOS). Predatory mites were found to distinguish between plants induced by spider mites and caterpillar oral secretion but not between plants with single spider mite infestation and plants induced by caterpillar oral secretion prior to spider mite infestation. Indeed, the volatile blends emitted by plants induced by spider mites only and the sequential induction treatment of caterpillar oral secretion followed by spider mite infestation, were similar. Our results suggest that plant indirect defense is not affected by previous treatment with oral secretion of M. brassicae caterpillars.

Attraction of parasitoids to plant volatiles induced by multiple herbivory depends on the specific combinations of attacking herbivore species, especially when their feeding modes activate different defense signalling pathways as has been reported for phloem feeding aphids and tissue feeding caterpillars. We studied the effects of pre-infestation with non-host aphids (Brevicoryne brassicae) for two different time periods on the ability of two parasitoid species to discriminate between volatiles emitted by plants infested by host caterpillars alone and those emitted by plants infested with host caterpillars plus aphids. Using plants originating from three chemically distinct wild cabbage (Brassica oleracea) populations, Diadegma semiclausum switched preference for dually infested plants to preference for plants infested with Plutella xylostella hosts alone when the duration of pre-aphid infestation doubled from 7 to 14 days. Microplitis mediator, a parasitoid of Mamestra brassicae caterpillars, preferred dually-infested plants irrespective of aphid-infestation duration. Separation of the volatile blends emitted by plants infested with hosts plus aphids or with hosts only was poor, based on multivariate statistics. However, emission rates of individual compounds were often reduced in plants infested with aphids plus hosts compared to those emitted by plants infested with hosts alone. This effect depended on host caterpillar species and plant population and was little affected by aphid infestation duration. Thus, the interactive effect of aphids and hosts on plant volatile production and parasitoid attraction can be dynamic and parasitoid specific. The characteristics of the multi-component volatile blends that determine parasitoid attraction are too complex to be deduced from simple correlative statistical analyses. Electronic supplementary material The online version of this article (doi:10.1007/s10886-017-0842-z) contains supplementary material, which is available to authorized users.

In some parasitic Hymenoptera the dying caterpillars remain attached or close to the parasitoid cocoons. It has been suggested that the caterpillars act as ‘bodyguards’ for the vulnerable cocoons and therefore protect them against predators and/or hyperparasitoids (the ‘usurpation hypothesis’). This hypothesis has been demonstrated in associations where the caterpillars remain active and/or aggressive after parasitism. However, in other associations the caterpillars are so physiologically depleted after parasitism that they are unable to physically defend the cocoons and instead sit atop them in a moribund state. In this study a generalist predator, the spined soldier bug, Podisus maculiventris Say (Hemiptera: Pentatomidae), was provided with cocoons of the gregarious endoparasitoid Cotesia glomerata L. and the solitary endoparasitoid Microplitis mediator Haliday (both Hymenoptera: Braconidae), in turn attended by their hosts, Pieris brassicae L. (Lepidoptera: Pieridae) and Mamestra brassicae L. (Lepidoptera: Noctuidae), respectively. Cotesia glomerata produces broods of up to 40 cocoons and the dying caterpillars sit atop the cocoons where they exhibit little response to physical stimuli. Previous studies reported that dying P. brassicae caterpillars were ineffective bodyguards against two species of hyperparasitoids. In both associations, the dying host caterpillars were significantly preferred as food by P. maculiventris over the parasitoid cocoons. However, in absence of caterpillars, the bugs readily attacked the C. glomerata cocoons. Alternatively, the survival of M. mediator was very low, irrespective of whether a caterpillar was present or not. Caterpillars attacked by M. mediator are several times smaller than those attacked by C. glomerata. Consequently, the predators ran out of food much more quickly in the former and switched from one prey to the other. We show that in some host–parasitoid associations the dying caterpillars provide more visually apparent or nutritionally superior prey, rather than acting as bodyguards.

1.Plants respond to insect herbivores with changes in physical and chemical traits, both locally and systemically, in leaves and flowers. Such phenotypic changes may influence the behaviour of every community member that interacts with the plant. Here, we address effects of plant responses to eggs and subsequent herbivory by caterpillars on plant-mediated interactions with pollinators and consequences for plant fitness. 2.Using a common garden set-up, we have investigated responses of Brassica nigra plants to herbivore exposure from egg deposition onwards throughout larval development. We quantified effects of infestation by the specialist Pieris brassicae on: 1. behaviour of pollinators; 2. volatile emission and 3. timing and number of seeds produced. 3.Egg deposition and folivory did not influence visitation by pollinators to plots of infested or control plants. Effects of herbivore infestation on both pollinator visitation and volatile emission were observed only at a later stage, when caterpillars were feeding on the flowers. 4.Remarkably, before eggs had hatched, infested plants accelerated seed production. The caterpillars that developed from the eggs fed on flowers but not on seeds and thus seed production prior to herbivory on flowers safeguarded reproductive output. 5.The results of this study show that early plant investments in reproduction can successfully prevent consumption of expensive reproductive tissues. By accelerating seed production, plants prevented consumption of flowers and effectively defended themselves against the herbivores

Co-evolutionary theory underpins our understanding of interactions in nature involving plant–herbivore and host–parasite interactions. However, many studies that are published in the empirical literature that have explored life history and development strategies between endoparasitoid wasps and their hosts are based on species that have no evolutionary history with one another. Here, we investigated novel associations involving two closely related solitary endoparasitoids that originate from Europe and North America and several of their natural and factitious hosts from both continents. The natural hosts of both species are also closely related, all being members of the same family. We compared development and survival of both parasitoids on the four host species and predicted that parasitoid performance is better on their own natural hosts. In contrast with this expectation, survival, adult size and development time of both parasitoids were similar on all (with one exception) hosts, irrespective as to their geographic origin. Our results show that phylogenetic affinity among the natural and factitious hosts plays an important role in their nutritional suitability for related parasitoids. Evolved traits in parasitoids, such as immune suppression and development, thus enable them to successfully develop in novel host species with which they have no evolutionary history. Our results show that host suitability for specialized organisms like endoparasitoids is closely linked with phylogenetic history and macro-evolution as well as local adaptation and micro-evolution. We argue that the importance of novel interactions and ‘ecological fitting’ based on phylogeny is a greatly underappreciated concept in many resource–consumer studies.

1. Intrinsic competition was compared in three species of braconid wasps, the solitary Meteorus pulchricornis Wesmael, and the gregarious Cotesia kariyai (Watanabe) and Cotesia ruficrus Haliday in caterpillars of their common host, the armyworm Mythimna separata Walker. Competition was determined in pair-wise contests consisting of simultaneous and subsequent parasitisms at various time intervals between the first and second attacks (

The performance of natural enemies, such as parasitoid wasps, is affected by differences in the quality of the host’s diet, frequently mediated by species or population-related differences in plant allelochemistry. Here, we compared survival, development time, and body mass in a generalist herbivore, the cabbage moth, Mamestra brassicae, and its solitary endoparasitoid, Microplitis mediator, when reared on two cultivated (CYR and STH) and three wild (KIM, OH, and WIN) populations of cabbage, Brassica oleracea. Plants either were undamaged or induced by feeding of larvae of the cabbage butterfly, Pieris rapae. Development and biomass of M. brassicae and Mi. mediator were similar on both cultivated and one wild cabbage population (KIM), intermediate on the OH population, and significantly lower on the WIN population. Moreover, development was prolonged and biomass was reduced on herbivore-induced plants. However, only the survival of parasitized hosts (and not that of healthy larvae) was affected by induction. Analysis of glucosinolates in leaves of the cabbages revealed higher levels in the wild populations than cultivars, with the highest concentrations in WIN plants. Multivariate statistics revealed a negative correlation between insect performance and total levels of glucosinolates (GS) and levels of 3-butenyl GS. However, GS chemistry could not explain the reduced performance on induced plants since only indole GS concentrations increased in response to herbivory, which did not affect insect performance based on multivariate statistics. This result suggests that, in addition to aliphatic GS, other non- GS chemicals are responsible for the decline in insect performance, and that these chemicals affect the parasitoid more strongly than the host. Remarkably, when developing on WIN plants, the survival of Mi. mediator to adult eclosion was much higher than in its host, M. brassicae. This may be due to the fact that hosts parasitized by Mi. mediator pass through fewer instars, and host growth is arrested when they are only a fraction of the size of healthy caterpillars. Certain aspects of the biology and life-history of the host and parasitoid may determine their response to chemical challenges imposed by the food plant.

Communities are riddled with indirect species interactions and these interactions can be modified by organisms that are parasitic or symbiotic with one of the indirectly interacting species. By inducing plant responses, herbivores are well known to alter the plant quality for subsequent feeders. The reduced performance of herbivores on induced plants cascades into effects on the performance of higher trophic level organisms such as parasitoids that develop inside herbivores. Parasitoids themselves may also, indirectly, interact with the host plant by affecting the behaviour and physiology of their herbivorous host. Here, we show that, through their herbivorous host, larvae of two parasitoid species differentially affect plant phenotypes leading to asymmetric interactions among parasitoid larvae developing in different hosts that feed on the same plant. Our results show that temporally separated parasitoid larvae are involved in indirect plant-mediated interactions by a network of trophic and non-trophic relationships.

1. Two field experiments were carried out to examine the role of patch size, host density, and complexity of the surrounding habitat, on the foraging behaviour of the parasitoid wasp Cotesia glomerata in the field. 2. First, released parasitoids were recaptured on patches of one or four Brassica nigra plants, each containing 10 hosts that were placed in a mown grassland area. Recaptures of females were higher than males, and males and females aggregated at patches with four plants. 3. In experiment 2, plants containing 0, 5 or 10 hosts were placed in unmown grassland plots that differed in plant species composition, on bare soil, and on mown grassland. Very low numbers of parasitoids were recaptured in the vegetated plots, while high numbers of parasitoids were recaptured on plants placed on bare soil or in mown grassland. Recaptures were higher on plants on bare soil than on mown grassland, and highest on plants containing 10 hosts. The host density effect was significantly more apparent in mown grassland than on bare soil. 4. Cotesia glomerata responds in an aggregative way to host density in the field. However, host location success is determined mostly by habitat characteristics, and stronger host or host-plant cues are required when habitat complexity increases.

In many parts of the world, the larvae of the cabbage white butterflies, Pieris rapae and P. brassicae, are considered to be major pests in several economically important brassicaceous crops including various cultivars of cabbage and mustard. Thus far, biological control of these pests has focused on parasitoids including species in the genus Cotesia. We examined interactions between the solitary ichneumonid parasitoid, Hyposoter ebeninus, developing in 1st to 3rd (L1–L3) larval instars of both P. rapae and P. brassicae. H. ebeninus is common in central and southern Europe, but has thus far received little attention as a possible biological control agent of cabbage butterflies. Larvae of both pierids continued to grow after they were parasitized, and development was only arrested some 5–7 days later. Caterpillars parasitized in the third instar grew significantly larger than larvae parasitized as L1 or L2. Adult parasitoid body mass was inversely correlated with host instar parasitized, and female wasps were significantly larger than male wasps. Egg-to-adult development time in H. ebeninus did not vary between the two hosts, but the parasitoid exhibited protandry. Parasitoid survival was generally higher in larvae of P. rapae than in larvae of P. brassicae, but varied with instar in the two hosts. Our study shows that H. ebeninus has promise as a biological control agent, particularly against its more suitable host, P. rapae.

Plant–insect interactions occur in spatially heterogeneous habitats. Understanding how such interactions shape density distributions of herbivores requires knowledge on how variation in plant traits (e.g. nutritional quality) affects herbivore abundance through, for example, affecting movement rates and aggregation behaviour. We studied the effects of plant patch size and herbivore-induced differences in plant nutritional quality on local densities of insect herbivores for two Brassica oleracea cultivars, i.e. white cabbage and Brussels sprouts. Early season herbivory as a treatment resulted in measurable differences in glucosinolate concentrations in both cultivars throughout the season. Herbivore induction and patch size both influenced community composition of herbivores in both cultivars, but the effects differed between species. Flea beetles (Phyllotreta spp.) were more abundant in large than in small patches, and this patch response was more pronounced on white cabbage than on Brussels sprouts. Herbivore-induction increased densities in all patches. Thrips tabaci was also more abundant in large patches and densities of this species were higher on Brussels sprouts than on white cabbage. Thrips densities were lower on induced than on control plants of both cultivars and this negative effect of induction tended to be more pronounced in large than in small patches. Densities of the cabbage moth (Mamestra brassicae) were lower on Brussels sprouts than on white cabbage and lower on herbivore-induced than on uninduced plants, with no effect of patch size. No clear effects of patch size and induction were found for aphids. This study shows that constitutive and herbivore-induced differences in plant traits interact with patch responses of insect herbivores.

1. For their larval development, parasitoids depend on the quality and quantity of resources provided by a single host. Therefore, a close relationship is predicted between the size of the host at parasitism and the size of the emerging adult wasp. This relationship is less clear for koinobiont than for idiobiont parasitoids. 2. As size differentiation in host species exhibiting sexual size dimorphism (SSD) is likely to occur already during larval development, in koinobiont larval endoparasitoids the size of the emerging adult may also be constrained based on the sex of the host caterpillar. 3. Sex-specific growth trajectories were compared in unparasitised Plutella xylostella caterpillars and in second and fourth instar hosts that were parasitised by the solitary larval koinobiont endoparasitoid Diadegma semiclausum. Both species exhibit SSD, where females are significantly larger than males. 4. Healthy female P. xylostella caterpillars developed significantly faster than their male conspecifics. Host regulation induced by D. semiclausum parasitism depended on the instar attacked. Parasitism in second-instar caterpillars reduced growth compared to healthy unparasitised caterpillars, whereas parasitism in fourth-instar caterpillars arrested development. The reduction in growth was most pronounced in hosts producing male D. semiclausum. 5. Parasitism itself had the largest impact on host growth. SSD in the parasitoid is mainly the result of differences in growth rate of the parasitoid–host complex producing male and female wasps and differences in exploitation of the host resources. Female wasps converted host biomass more efficiently into adult biomass than males.

The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the field of ecology of multitrophic interactions. Scarcely studied aspects include the effects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the effects of constitutive and herbivore-induced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as first instars were low and did not differ among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed differences in encapsulation rates between plant populations could not be explained exclusively by differences in host growth on the different Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the first study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, affecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of fitness costs and benefits of herbivore diet on the third trophic level.

Adult female Phytoseiulus persimilis Athias-Henriot (Acari, Phytoseiidae) of a laboratory population show a set of characteristic symptoms, designated as non-responding (NR) syndrome. Mature predators shrink, cease oviposition and die. They show a lower degree of attraction to herbivore-induced plant volatiles and a greater tendency to leave prey patches carrying ample prey. Moreover, predators may carry excretory crystals in the legs, may cease prey consumption and have a low excretion rate. Here, we satisfy Koch’s postulates for a strain of Acaricomes phytoseiuli (DSM 14247) that was isolated from symptomatic female P. persimilis of the NR-population. Adult female P. persimilis were either exposed to a bacterial inoculum suspension (treatment) or to sterile distilled water (control) for a period of 3 days. Control and treated predators were examined for the occurrence of six symptoms characteristic for the NR-syndrome and the presence of A. phytoseiuli after inoculation. The latter was done by re-isolation of A. phytoseiuli from individual predators and predator feces placed on nutrient agar, by PCR-based identification and by histopathological studies of individual predators. The NR-syndrome was clearly induced in those predators that had been exposed to the bacterial inoculum (incubation time = 2–5 days, fraction shrunken females = 80%), whereas predators exposed to water did not show the NR-syndrome. A. phytoseiuli was never isolated from control predators whereas it could be re-isolated from 60% of the treated predators (N = 37) and from feces of 41% of treated predators (N = 17). Only one day after exposure A. phytoseiuli could not be re-isolated from treated predators and their feces. Light and electron microscope studies of predators exposed to A. phytoseiuli revealed striking bacterial accumulations in the lumen of the alimentary tract together with extreme degeneration of its epithelium. In addition, bacterial foci also occurred in the fat body. These phenomena were not observed in control predators that were exposed to sterile water. The present data prove that A. phytoseiuli can infect the predatory mite P. persimilis and induce the NR-syndrome and characteristic histopathological changes in adult female P. persimilis. This is the first record of a bacterial pathogen in a phytoseiid mite and the first description of pathogenic effects of a bacterial species in the genus Acaricomes.

Most studies on plant defenses against insect herbivores investigate direct and indirect plant defenses independently. However, these defenses are not necessarily mutually exclusive. Plant metabolites can be transmitted through the food chain and can also affect the herbivore’s natural enemies. A conflict may arise when a natural enemy is attracted to a plant that is suboptimal in terms of its own fitness. In addition, plant defenses are often studied in cultivated plant species in which artificial selection may have resulted in reduced resistance against insect herbivores. In this study, we investigated both direct and indirect plant defenses in two closely related wild brassicaceous plant species, Brassica nigra L. and Sinapis arvensis L. The herbivore Pieris brassicae L. (Lepidoptera: Pieridae), which is specialized on brassicaceous plant species, developed faster and attained higher pupal mass when reared on B. nigra than on S. arvensis . In contrast, Cotesia glomerata L. (Hymenoptera: Braconidae), which is a gregarious endoparasitoid of P. brassicae caterpillars, developed equally well on P. brassicae irrespective of the food plant on which its host had been reared. The feeding strategy of the parasitoid larvae, that is, selectively feeding on hemolymph and fat body, is likely to allow for a much wider host-size range without affecting the size or development time of the emerging parasitoids. In flight chamber experiments, C. glomerata , which had an oviposition experience in a host that fed on Brussels sprout, exhibited significant preference for host-damaged B. nigra over host-damaged S. arvensis plants. Headspace analysis revealed quantitative and qualitative differences in volatile emissions between the two plant species. This parasitoid species may use a range of cues associated with the host and the host’s food plant in order to recognize the different plant species on which the host can feed. These results show that there is no conflict between direct and indirect plant defenses for this plant‐host‐ parasitoid complex.

Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

Virtually all studies of plant-herbivore-natural enemy interactions focus on plant quality as the major constraint on development and survival. However, for many gregarious feeding insect herbivores that feed on small or ephemeral plants, the quantity of resources is much more limiting, yet this area has received virtually no attention. Here, in both lab and semi-field experiments using tents containing variably sized clusters of food plants, we studied the effects of periodic food deprivation in a tri-trophic system where quantitative constraints are profoundly important on insect performance. The large cabbage white Pieris brassicae, is a specialist herbivore of relatively small wild brassicaceous plants that grow in variable densities, with black mustard (Brassica nigra) being one of the most important. Larvae of P. brassicae are in turn attacked by a specialist endoparasitoid wasp, Cotesia glomerata. Increasing the length of food deprivation of newly molted final instar caterpillars significantly decreased herbivore and parasitoid survival and biomass, but shortened their development time. Moreover, the ability of caterpillars to recover when provided with food again was correlated with the length of the food deprivation period. In outdoor tents with natural vegetation, we created conditions similar to those faced by P. brassicae in nature by manipulating plant density. Low densities of B. nigra lead to potential starvation of P. brassicae broods and their parasitoids, replicating nutritional conditions of the lab experiments. The ability of both unparasitized and parasitized caterpillars to find corner plants was similar but decreased with central plant density. Survival of both the herbivore and parasitoid increased with plant density and was higher for unparasitized than for parasitized caterpillars. Our results, in comparison with previous studies, reveal that quantitative constraints are far more important that qualitative constraints on the performance of gregarious insect herbivores and their gregarious parasitoids in nature.

Infochemicals play an important role in structuring intra-and interspecific interactions. Many parasitoid wasp species rely on herbivory or oviposition-induced plant volatiles (HIPVs/OIPVs) to locate their herbivorous hosts, and must cope with variation in the volatile blends due to factors such as plant/host species, herbivore density or attack by several herbivores. However, little is known about how dual herbivory or changes in herbivore density affect multiple parasitoid species, each attacking a different herbivore, in the same system. In a natural system, we investigated the effect of dual attack on the ability of three parasitoid species to differentiate between volatiles induced by hosts and those induced by a combination of hosts and nonhosts. Black mustard, Brassica nigra, plants were infested with eggs or caterpillars of Pieris brassicae, alone or in combination with different densities of Brevicoryne brassicae aphids. We determined the ability of three different parasitoid species that parasitize either P. brassicae eggs (Trichogramma brassicae), caterpillars (Cotesia glomerata) or B. brassicae aphids (Diaeretiella rapae) to discriminate between the induced volatiles, and analysed the plant volatile blends. Dual infestation did not affect the parasitoid species equally and aphid infestation altered, in a density-dependent manner, the volatile-mediated foraging of all three parasitoid species. Chemical analyses of the volatile blends revealed nonlinear emission patterns in relation to aphid density in both plants attacked by aphids alone and in plants attacked by a combination of aphids and caterpillars. Simple correlations between behaviour and volatile emissions in pairwise comparisons suggest the importance of certain volatiles explaining attraction, whereas dose-response type analyses reveal that these simple correlation analyses provide an incomplete picture. (C) 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.