Influence of fungal isolates infecting tall fescue on multitrophic interactions

The epichloae are ascomycetous fungi in the genera Epichloë and Neotyphodium that live within grasses. Some of these fungi produce alkaloids that can help protect the host from herbivores. The alkaloids may also travel up the food web and affect members of the third trophic level. In this way they can produce trophic cascades which are rippling effects when a trophic level impacts those above or below it. We briefly summarize the general patterns of multitrophic effects of endophytes and highlight the most recent studies on this topic. Further, we report on our study in which we tested if different fungal strains in tall fescue (cultivar Jesup) affect multitrophic interactions involving aphids and their parasitoid natural enemies. Using both the common strain of N. coenophialum and a novel isolate (AR577), we allowed potted plants to be colonized by aphids and parasitoids in a semi-natural setting. We found that endophyte infection of tall fescue resulted in greater vegetative growth of the plant. We also found that N. coenophialum modified bottom-up cascades by depressing both aphid and parasitoid densities. Finally, we found that multitrophic effects were modified by fungal isolate: the common strain had stronger negative impacts on aphid and parasitoid densities than did the novel isolate.     

Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants?

Endophytic fungi, particularly in the genus Neotyphodium, are thought to interact mutualistically with host grasses primarily by deterring herbivores and pathogens via production of alkaloidal mycotoxins. Little is known, however, about how these endophytes interact with host plants and herbivores outside the realm of agronomic forage grasses, such as tall fescue, and their livestock grazers or invertebrate pest herbivores. We tested the effects of Neotyphodium inhabiting introduced tall fescue and native Arizona fescue on preference, survival, and performance of the leaf-cutting ant, Acromyrmex versicolor, an important generalist herbivore in the southwestern United States. In a choice experiment, we determined preferences of foraging queens and workers for infected and uninfected tall fescue and Arizona fescue. In a no-choice experiment, we determined queen survival, worker production, and size of fungal gardens for foundress queens reared on diets of infected and uninfected tall fescue and Arizona fescue. Foraging workers and queens did not significantly prefer either uninfected tall fescue or Arizona fescue relative to infected grasses, although ants tended to harvest more uninfected than infected tall fescue and more infected than uninfected Arizona fescue. Queen survivorship and length of survival was greater on uninfected tall fescue, uninfected Arizona fescue, and infected Arizona fescue than on infected tall fescue or the standard diet of palo verde and mesquite leaves. No queens survived beyond 6 weeks of the study when fed the infected tall fescue diet, in contrast to the effects of the other diets. Likewise, worker production was much lower and fungal garden size much smaller on infected tall fescue than in all other treatments, including the standard diet. In general, ant colonies survived and performed better on uninfected tall fescue and infected and uninfected Arizona fescue than standard diets of palo verde and mesquite leaves. The interaction of Neotyphodium with its host grasses is highly variable and these endophytes may increase, not alter, or even decrease resistance to herbivores. The direction of the interaction depends on host and fungal genotype, herbivore species, and environmental factors. The presence of endophytes in most, if not all, host plants suggests that endophytes may alter foraging patterns, performance, and survival of herbivores, such as leaf-cutting ants, but not always in ways that increase host plant fitness. Received: 27 October 1998 / Accepted: 19 October 1998     

Plant‐mediated indirect effects and the persistence of parasitoid–herbivore communities

We have examined the effects of herbivore diversity on parasitoid community persistence and stability, mediated by nonspecific information from herbivore‐infested plants. First, we investigated host location and patch time allocation in the parasitoid Cotesia glomerata in environments where host and/or nonhost herbivores were present on Brassica oleracea leaves. Parasitoids were attracted by infochemicals from leaves containing nonhost herbivores. They spent considerable amounts of time on such leaves. Thus, when information from the plant is indistinct, herbivore diversity is likely to weaken interaction strengths between parasitoids and hosts. In four B. oleracea fields, all plants contained herbivores, often two or more species. We modelled parasitoid–herbivore communities increasing in complexity, based on our experiments and field data. Increasing herbivore diversity promoted the persistence of parasitoid communities. However, at a higher threshold of herbivore diversity, parasitoids became extinct due to insufficient parasitism rates. Thus, diversity can potentially drive both persistence and extinctions.     

Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

1. Induced plant responses can affect herbivores either directly, by reducing herbivore development, or indirectly, by affecting the performance of natural enemies. Both the direct and indirect impacts of induction on herbivore and parasitoid success were evaluated in a common experimental system, using clonal poplar trees Populus nigra (Salicales: Salicaceae), the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae), and the gregarious parasitoid Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae). 2. Female parasitoids were attracted to leaf odours from both damaged and undamaged trees, however herbivore‐damaged leaves were three times more attractive to wasps than undamaged leaves. Parasitoids were also attracted to herbivore larvae reared on foliage and to larval frass, but they were not attracted to larvae reared on artificial diet. 3. Prior gypsy moth feeding elicited a systemic plant response that retarded the growth rate, feeding, and survival of gypsy moth larvae, however induction also reduced the developmental success of the parasitoid. 4. The mean number of parasitoid progeny emerging from hosts fed foliage from induced trees was 40% less than from uninduced trees. In addition, the proportion of parasitised larvae that survived long enough to issue any parasitoids was lower on foliage from induced trees. 5. A conceptual and analytical model is provided to describe the net impacts of induced plant responses on parasitoids, and implications for tritrophic interactions and biological control of insect pests are discussed.     

The role of herbivore‐ and plant‐related experiences in intraspecific host preference of a relatively specialized parasitoid

Parasitoids use odor cues from infested plants and herbivore hosts to locate their hosts. Specialist parasitoids of generalist herbivores are predicted to rely more on herbivorederived cues than plant-derived cues. Microplitis croceipes (Cresson)(Hymenoptera: Braconidae) is a relatively specialized larval endoparasitoid of Heliothis virescens (F.)(Lepidoptera: Noctuidae), which is a generalist herbivore on several crops including cotton and soybean. Using M. croceipes/H. virescens as a model system, we tested the following predictions about specialist parasitoids of generalist herbivores:(i) naive parasitoids will show innate responses to herbivore-emitted kairomones, regardless of host plant identity and (ii) herbivore-related experience will have a greater influence on intraspecific oviposition preference than plant-related experience. Inexperienced (naive) female M. croceipes did not discriminate between cotton-fed and soybean-fed H. virescens in oviposition choice tests, supporting our first prediction. Oviposition experience alone with either host group influenced subsequent oviposition preference while experience with infested plants alone did not elicit preference in M. croceipes, supporting our second prediction. Furthermore, associative learning of oviposition with host-damaged plants facilitated host location. I terestingly, naive parasitoids attacked more soybeathan cotton-fed host larvae in two-choice tests when a background of host-infested cotton odor was supplied, and vice versa. This suggests that plant volatiles may have created an olfactory contrast effect. We discussed ecological significance of the results and concluded that both plant- and herbivore-related experiences play important role in parasitoid host foraging.     

Differential induction of plant chemical defenses by parasitized and unparasitized herbivores: consequences for reciprocal,multitrophic interactions

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.     

Fungal endophytes of grasses and their effects on an insect herbivore

Summary The effects of endophytic fungi (Tribe Balansiae, Clavicipitaceae, Ascomycetes) of grasses on an insect herbivore were studied by feeding paired groups of larvae of the fall armyworm (Spodoptera frugiperda, Noctuidae, Lepidoptera) leaves from either infected or uninfected individuals. Perennial ryegrass infected by the Lolium endophyte, tall fescue infected by Epichloe typhina, dallisgrass infected by Myriogenospora atramentosa, Texas wintergrass infected by Atkinsonella hypoxylon, and sandbur infected by Balansia obtecta were utilized. The endophytes of ryegrass and fescue previously have been shown to be toxic to mammalian herbivores and to deter feeding of some insect herbivores. In this study we extend the antiherbivore properties of those endophytes to the fall armyworm and demonstrate that fungal endophytes in three other genera have similar antiherbivore properties. For most grasses, survival and weights of fall armyworm larvae fed infected leaves were significantly lower and larval duration was significantly longer compared to larvae fed uninfected leaves. Resistance to herbivores may provide a selective advantage to endophyte-infected grasses in natural populations.     

Structure of a herbivore–parasitoid community: Are parasitoids shared by different herbivore guilds?

Plant–herbivore–parasitoid interactions are a common occurrence in terrestrial food webs. Few parasitoids are thought to be shared by host insects of different feeding guilds because different parasitism strategies are required to use hosts of different feeding types. However, this assumption has rarely been tested using data from nature. To clarify whether parasitoids are shared among host guilds, I examined the structure of parasitoid communities on herbivore guilds associated with two Rhododendron species (Ericaceae) in a temperate secondary forest in central Japan. Leaf- and flower-feeding insects were collected from Rhododendron reticulatum and Rhododendron macrosepalum shrubs and reared in the laboratory for 3 years from April 1999 to March 2002. In total, 79 species of holometabolous herbivores (Lepidoptera, Diptera, Coleoptera, and Hymenoptera) were recorded, with 62 species on R. reticulatum and 51 species on R. macrosepalum. A total of 81 parasitoid species (Hymenoptera and Diptera) was recorded from the sampled herbivores, with 48 species from those on R. reticulatum and 50 species from those on R. macrosepalum. In total, 36 herbivore species were parasitised by 1–18 parasitoid species per host species, although the number of parasitoid species was strongly affected by sample size. Parasitoids that had two or more host species frequently attacked herbivore species from different families or on different host plants, whereas they did not attack species from different herbivore guilds; no parasitoids were shared between external feeders and rollers. Therefore, my results support the hypothesis that few parasitoids are shared among herbivores of different feeding guilds.     

Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly

Variation of host quality affects population dynamics of parasitoids, even at the landscape scale. What causes host quality to vary and the subsequent mechanisms by which parasitoid population dynamics are affected can be complex. Here, we examine the indirect interaction of a plant pathogen with a parasitoid wasp. Under laboratory conditions, parasitoids from hosts fed fungus-infected plants weighed less than those from hosts fed uninfected plants, indicating that the fungus causes the hosts to be of poor quality. However, parasitoids reared from hosts fed fungal-infected diet also tended to be female, a characteristic associated with high host quality. The pathogen, herbivore and parasitoid persist regionally as metapopulations in a shared landscape in Aland, Finland. In an analysis of the metapopulation dynamics of the parasitoid over 6 years, the probability of colonization of a host population increased by more than twofold in patches occupied by the plant pathogen. While we cannot determine that the relationship is causal, a compelling explanation is that the plant pathogen facilitates the establishment by the parasitoid by increasing the fraction of female offspring. This is a novel mechanism of spatial multi-trophic level interactions.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Variation in Nitrogen Utilization in Acremonium coenophialum Isolates

Acremonium coenophialum, a fungal endosymbiont in tall fescue, is responsible for the production of alkaloid toxins. Animals grazing endophyte-infected tall fescue often show toxicosis. In marginal environments, the endophyte is important for long-term survival of tall fescue. Few differences in endophyte isolates from individual tall fescue plants have been reported. To aid development of a toxicosis-free tall fescue, it is important to identify differences in endophyte isolates. This report describes variation in nitrogen utilization in a defined culture medium by endophyte isolates from Kentucky-31 tall fescue. Overall, the best nitrogen sources for dry weight production of mycelium were proline and potassium nitrate. Thirty-four isolates grown on agar-solidified defined media with single nitrogen sources showed variation in nitrogen utilization. Fifty percent of the isolates were unable to utilize two or more amino acids. Manipulation of endophyte variation could lead to development of a toxicosis-free tall fescue cultivar.     

Isolate-dependent impacts of fungal endophytes in a multitrophic interaction

Neotyphodium lolii , an endophytic fungus of perennial ryegrass, deters Argentine stem weevil, Listronotus bonariensis , an important insect pest of pastures in New Zealand. Deterrence is apparently due to several alkaloids the fungus produces. We asked if the fungus also affects the third trophic level. Specifically, we tested if several different isolates of the fungus altered the growth and survival of the parasitoid, Microctonus hyperodae . Adult weevils were collected from paddocks near Lincoln, New Zealand and maintained in an environmental chamber. Weevils were assorted into treatment groups and fed perennial ryegrass (cv. Nui) lacking endophyte infection (nil) or containing one of the following endophyte strains: ARW, AR1, AR6, AR37. All endophyte strains differed from one another with respect to the profile of alkaloids they produce. Following two weeks of acclimation, weevils were placed with M. hyperodae to allow for parasitization. Weevils were then placed into Petri dishes (10 per dish) and fed grass clippings from the appropriate treatment group. We collected weevils as they died and dissected them to assess the development of parasitoids. Emergence of prepupae from hosts and survival to adulthood were also recorded. Fungal isolates did not differ in their influence on weevil feeding or survival. In contrast, the effect of the endophyte on the parasitoid varied among isolates of the fungus. Isolates ARW and AR6 reduced parasitoid adult emergence relative to nil endophyte. In contrast, AR37 had no negative effect on survival of the parasitoid. Furthermore, an index of developmental rate showed that parasitoids developed more slowly when reared from hosts fed grass containing any of the strains of N. lolii , except AR37, compared to endophyte-free grass. Negative effects of the endophyte on parasitoid survival were associated with the presence of ergovaline while effects on parasitoid development rate were associated with the presence of any alkaloid.     

Expression of the bacteriophage T4 lysozyme gene in tall fescue confers resistance to gray leaf spot and brown patch diseases

Tall fescue (Festuca arundinacea Schreb.) is an important turf and forage grass species worldwide. Fungal diseases present a major limitation in the maintenance of tall fescue lawns, landscapes, and forage fields. Two severe fungal diseases of tall fescue are brown patch, caused by Rhizoctonia solani, and gray leaf spot, caused by Magnaporthe grisea. These diseases are often major problems of other turfgrass species as well. In efforts to obtain tall fescue plants resistant to these diseases, we introduced the bacteriophage T4 lysozyme gene into tall fescue through Agrobacterium-mediated genetic transformation. In replicated experiments under controlled environments conducive to disease development, 6 of 13 transgenic events showed high resistance to inoculation of a mixture of two M. grisea isolates from tall fescue. Three of these six resistant plants also displayed significant resistance to an R. solani isolate from tall fescue. Thus, we have demonstrated that the bacteriophage T4 lysozyme gene confers resistance to both gray leaf spot and brown patch diseases in transgenic tall fescue plants. The gene may have wide applications in engineered fungal disease resistance in various crops.     

The interaction between host and host plant influences the oviposition and performance of a generalist ectoparasitoid

The successful development of parasitoids of herbivores depends on the quality of their host, which is often affected by the host plant. Therefore, a parasitoid’s oviposition decisions will directly depend on the host, but also on plant quality. Here, we investigated the direct effects of host species and the indirect effects of the host’s food plant on the oviposition decisions and performance of the gregarious ectoparasitoid Euplectrus platyhypenae Howard (Hymenoptera: Eulophidae). With a series of no‐choice experiments, we determined the oviposition and performance of the parasitoid on: (1) two caterpillar species, fall armyworm, Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae), and velvet armyworm, Spodoptera latifascia Walker, reared on maize (Zea mays L., Poaceae), (2) the same caterpillars reared on maize, bean (Phaseolus vulgaris L., Fabaceae), or squash (Cucurbita pepo L., Cucurbitaceae) leaves, and (3) S. latifascia caterpillars reared on leaves of wild and cultivated lima bean, Phaseolus lunatus L. All these insects and plants originate from Mesoamerica where they have coexisted for thousands of years in the traditional agricultural system known as Milpa in which maize, beans, and squash are planted together. We found that the preferred and best combination of host and host plant for parasitoid performance was S. frugiperda on maize. Parasitoids laid larger clutches, had higher survival, and more females and larger adults emerged from S. frugiperda reared on maize. However, when both caterpillar species were reared on squash, S. latifascia was the better host. Contrary to the literature, S. frugiperda was not able to develop on bean plants. Results from the lima bean experiment showed that parasitoid performance was best when S. latifascia was reared on leaves of cultivated compared to wild lima bean. These findings are discussed in the context of mixed cropping in which the ability of generalist parasitoids to switch among hosts and host plant species could be advantageous for pest management.     

Increasing floral diversity for selective enhancement of biological control agents: A double-edged sward?

Floral resource subsidies can have differential effects on insect herbivores compared with the herbivores’ natural enemies. While the nectar of many plant species enhances parasitoid fitness, it may also increase damage by herbivores. This may occur as a result of enhanced herbivore fitness or by enhancing fourth-trophic-level processes, possibly disrupting a trophic cascade as a result. The responses of different arthropod guilds to different floral resource subsidies were compared using Plutella xylostella (Hyponomeutidae), its parasitoid Diadegma semiclausum (Ichneumonidae) and data from two other published herbivore–parasitoid systems. These were Dolichogenidea tasmanica (Braconidae) and its host Epiphyas postvittana, and Copidosoma koehleri (Encyrtidae) and its host Phthorimaea operculella. The parasitoids and hosts in the three systems exhibited differential responses to the nectar sources. The differential response was not explained by morphology, demonstrating that physical access to nectaries alone does not determine the potential of flowers as a food source. For some flowering plants, enhancement of herbivore and parasitoid fitness occurred. Other flowering plants, such as buckwheat and phacelia, conferred a selective enhancement on parasitoids by increasing only their fitness. More effective conservation biocontrol may be achieved by the provision of selective floral resources. Attempts to ‘engineer’ agroecosystems to enhance biological control require an extensive knowledge of the ecology of the herbivore, its enemies and their interactions with potential resource subsidies.     

Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes

Aims

Novel fungal endophyte (Neotyphodium coenophialum; Latch, Christensen and Samuels; Glenn, Bacon, and Hanlin) genotypes in symbiosis with tall fescue (Lolium arundinaceum; Schreb. Darbysh.) have been recently introduced to agricultural seed markets. These novel endophytes do not produce the full suite of toxins that the ‘common toxic’ form does, and therefore, may not have the same consequences on plant and soil processes. Here, we evaluated the effects of endophyte presence and genotype on ecosystem processes of tall fescue stands.

Methods

We quantified the effects of the presence of the common toxic endophyte (CT), two novel endophyte genotypes (AR-542, AR-584), no endophyte (endophyte free, E-), and a mixture of all endophyte statuses (mix) within a single genotype of tall fescue (PDF) on various soil and plant parameters.

Results

Endophyte presence and genotype affected tall fescue cover and plant species diversity: cover—CT, AR-542, AR -584, mix > E- and species diversity—E- > AR-542, AR -584 > CT, mix. Most measured soil parameters had significant endophyte effects. For example, higher fluxes of soil CO₂ and N₂O were measured from stands of AR-542 than from the other endophyte treatments.

Conclusions

These results indicate that endophyte presence and genetic identity are important in understanding the ecosystem-scale effects of this agronomically important grass-fungal symbiosis.     

Interaction between fungal endophytes and environmental stressors influences plant resistance to insects

Neotyphodium coenophialum, an endophytic fungus that infects shoots of tall fescue (Festuca arundinacea), may protect its host from herbivory through production of alkaloids. Yet, the fungus can also modify plant resource allocation, regrowth dynamics, and drought tolerance, and these changes may also influence herbivores. We tested if N. coenophialum infection interacted with stress (drought or simulated herbivory) to modify plant resistance to insects. We assigned greenhouse plants to one of four treatments: 1) clipping at 3 cm above the soil surface, 2) drought stress during insect bioassays, 3) drought stress prior to insect bioassays, or 4) daily watering. Treatments were crossed with presence or absence of endophyte to give eight treatment combinations, and we assessed the performance of bird cherry‐oat aphid (Rhopalosiphum padi) and fall armyworm (Spodoptera frugiperda) feeding on plants in two separate experiments from each of the eight treatments. Aphids were placed into clip bags on leaf blades and allowed to reproduce parthenogenetically. Plant tissue was fed to third instar fall armyworm caterpillars until they molted into the fifth instar. Developmental time was recorded and larval growth was obtained gravimetrically. We also assessed total protein nitrogen (N) and loline alkaloids in plants.
Total protein N was unaffected by endophyte infection. In contrast, stress influenced total protein N, but its effect varied with endophyte infection. Uninfected plants that were clipped had higher total protein N; this trend was absent in infected plants. Plants in drought stress had lower N, but only if they were infected. Lolines were nearly absent from uninfected plants. In infected plants they tended to be higher in clipped plants. The effect of endophyte infection differed between the two insects: aphid reproduction was reduced by the endophyte, but endophyte infection enhanced caterpillar performance. Both insects were affected by interactions between the endophyte and stress. Aphids were negatively affected by drought stress, but only when feeding on uninfected plants, while caterpillars showed the opposite response, displaying lower performance on drought stressed plants only if they were infected. Aphids reproduced faster on regrowth tissue (following damage by clipping) of uninfected plants, but endophyte infection cancelled this effect. In contrast, performance of caterpillars was not influenced by an interaction between damage and infection. We conclude that N. coenophialum does not provide universal resistance to insects. Endophyte‐mediated resistance varies with insect species and will be a complex function of environmental stress, including drought and prior damage.     

Associative learning of host presence in non‐host environments influences parasitoid foraging

1. Parasitoids are known to utilise learning of herbivore‐induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non‐suitable herbivores (non‐hosts). Simultaneous infestation of plants by hosts and non‐hosts has been found to result in induction of HIPVs that differ from host‐infested plants. Each non‐host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non‐host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non‐hosts in the laboratory and in semi‐field experiments. 3. In two‐choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant–host–non‐host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non‐host caterpillar Mamestra brassicae or the non‐host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non‐host caterpillars or aphids in a semi‐field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.     

Transgenic GNA Expressing Potato Plants Augment the Beneficial Biocontrol of Lacanobia Oleracea (Lepidoptera: Noctuidae) by the parasitoid Eulophus Pennicornis (Hymenoptera; Eulophidae)

The effect of expressing the gene encoding snowdrop lectin (Galanthus nivalis agglutinin, GNA) in transgenic potato plants, on parasitism of the phytophagous insect pest Lacanobia oleracea by the gregarious ectoparasitoid Eulophus pennicornis, was investigated in glasshouse trials. Expression of GNA (approx. 1.0% total soluble protein) by transgenic plants significantly reduced the level of pest damage, thus confirming previous studies. Furthermore, the presence of the parasitoid significantly reduced the levels of damage incurred either by the transgenic or control plants when compared to those plants grown in the absence of the parasitoid. For the GNA expressing plants the presence of the parasitoid resulted in further reductions (ca. 21%) in the level of damage caused by the pest species. The ability of the wasp to parasitise and subsequently develop on the pest larvae was not altered by the presence of GNA in the diet of the host. E. pennicornis progeny that developed on L. oleracea reared on GNA expressing plants showed no significant alteration in fecundity when compared with wasps that had developed on hosts fed on control potato plants, although mean size and longevity of female parasitoids was significantly reduced. The number of F ₂ progeny produced by parasitoids derived from hosts fed on GNA-expressing plants was not significantly different to those produced by parasitoids from hosts fed control plants. Results from the present study demonstrate that the use of transgenic plants expressing insecticidal proteins can be compatible with the deployment of beneficial insects and that the two factors may interact in a positive manner.     

Fitness-related traits in a parasitoid fly are mediated by effects of plants on its host

Plants can affect parasitoids directly, by reducing or enhancing their ability to locate hosts, or indirectly by affecting the fitness of herbivores and thus of parasitoids. Tritrophic interactions between three host plants (cucumber, tomato, sweet pepper), a polyphagous herbivore Trichoplusia ni and a generalist parasitoid Compsilura concinnata were assessed. Plants had a strong effect on T. ni larval survival, as well as on C. concinnata fitness-related traits: cucumber-fed hosts yielded parasitoids with shorter larval development time and females had heavier pupal weights than parasitoids from host larvae that were fed tomato. Furthermore, C. concinnata was more efficient at finding cucumber-fed than tomato-fed T. ni . These results suggest that C. concinnata has different efficiency and potential as a biocontrol agent on the different crops. This highlights the importance of assessing tritrophic interactions in systems where an inundative biological control agent may be released against generalist targets on more than one crop plant.