Influence of genetic variation in the fungal endophyte of a grass on an herbivore and its parasitoid

Neotyphodium coenophialum (Glenn, Bacon, Price & Hanlin) (Ascomycota: Clavicipitaceae) is an endophytic fungus that lives symbiotically within grasses and produces alkaloids that can help protect its hosts from some insect pests. We used laboratory‐based experiments to investigate whether fungal genotype influences an herbivore and its parasitoid. We tested whether variation in novel isolates, plus a control lacking fungal infection, affected preference by fall armyworm, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae: Amphipyrini), and growth and survival of Euplectrus comstockii Howard (Hymenoptera: Eulophidae: Euplectrini), a parasitoid of fall armyworm. Caterpillars preferred leaf blades in choice experiments from uninfected tall fescue [Lolium arundinaceum (Schreb.) Darbysh., cultivar Jesup (Poaceae)] and tended to avoid blades from plants containing fungal isolates AR502, AR542, or the most common strain from pastures in Georgia, USA, in tall fescue. However, caterpillars fed as much on leaf blades from plants containing isolate AR502 as from those lacking infection. Parasitoid pupal mass was not influenced by fungal isolate, yet fungal isolate did influence parasitoid survival. Survival was higher than expected for parasitoids reared from hosts fed plants lacking fungal infection, but was lower than expected for those reared from hosts fed plants infected with the common strain or AR542 isolates. In contrast, parasitoids reared from hosts fed plants infected with isolate AR502 did not experience higher mortality than expected by chance. Our results show that N. coenophialum can modify bottom‐up trophic cascades through direct effects on herbivores, as well as indirect effects on a natural enemy of the herbivores and that the fungus may influence the tritrophic interaction in ways that counterbalance herbivore protection provided by the symbiont. Our work also shows that these effects are influenced by fungal genotype. As attempts are made to produce forage cultivars with strains of fungal endophyte that lack negative influences on livestock, it will be prudent for investigators to assess the multi‐trophic effects of these novel associations within agroecosystems.     

Insect Feeding Deterrents in Endophyte-Infected Tall Fescue

The presence of an endophytic fungus, Acremonium coenophialum, in tall fescue (Festuca arundinacea) deterred aphid feeding by Rhopalosiphum padi and Schizaphis graminum. Both species of aphid were unable to survive when confined to endophyte-infected tall fescue plants. Feeding deterrents and toxic factors to R. padi and Oncopeltus fasciatus, large milkweed bug, were primarily associated with a methanol extract obtained when endophyte-infected tall fescue seed was serially extracted with hexane, ethyl acetate, and methanol. The concentrations of pyrrolizidine alkaloids were determined to be 30 to 100 times greater in the methanol extract than in the hexane and ethyl acetate extracts.     

Influence of endophyte infection, plant age and harvest interval on Rhopalosiphum padi survival and its relation to quantity of N-formyl and N-acetyl loline in tall fescue

Rhopalosiphum padi L. (Homoptera: Aphididae) is sensitive to loline alkaloids present in tall fescue, Festuca arundinacea Shreb., infected with the endophytic fungus, Acremonium coenophialum Morgan-Jones & Gams. Aphid survival was higher on endophyte-free plants regardless of plant age after germination or age of regrowth tissue after clipping. Survival of aphids on endophyte-infected grass was lower on young tissue but increased as plants aged, although it never reached the same level on endophyte-free plants. Both N-formyl and N-acetyl loline increased as uncut or regrowth tissue aged; however, this was influenced by the age of the plant at the initial cut and the clipping frequency. Although even small amounts of loline cause high aphid mortality, the aphids are able to survive on endophyte-infected plants if the tillers have senescing leaves which contain lower amounts of loline. Preference for senescing leaves may help R. padi avoid plant parts containing high amounts of toxic allelochemicals, thus contributing to higher numbers of aphids on older, endophyte-infected plants.     

Development and use of molecular diagnostic tools to determine trophic links and interspecific interactions in aphid-parasitoid communities in Hawaii

There has been much debate regarding the impact of parasitoid competition and hyperparasitism on the successful biological control of aphid pests. Difficulty in the evaluation of interspecific interactions and trophic links using conventional rearing and dissection methods has prevented a deeper understanding of such relationships. The analysis of trophic links in the parasitoid community associated with the melon aphid (Aphis gossypii) in Hawaii provides a unique opportunity to assess complex interactions that occur in a system where all of the aphids and parasitoids have been introduced. Here, we developed and applied multiplex PCR assays to investigate the occurrence of in-host competition between parasitoids and/or hyperparasitoids on melon aphids collected from fields of Colocasia esculenta. To fully document the parasitoid-hyperparasitoid community within A. gossypii, both live and mummified aphids were examined. A total of 818 live and 245 mummified aphids were analyzed using the multiplex assays, with congruent rearing of over 600 mummified aphids serving as a basis for qualitative comparisons in terms of species composition and trophic linkages. The rearing and the DNA methods showed similar trends, with sharp declines in one parasitoid species followed by sharp increases in another during the course of the season. Molecular analyses revealed that hyperparasitism and multiparasitism of live aphids is remarkably low, whereas hyperparasitism of mummified aphids was extraordinarily high in both rearing and molecular analyses. In comparison to reared samples, molecular analysis of the parasitoid community was more complete and permitted the identification of previously unknown or unconfirmed trophic linkages. The potential of this approach in future studies on the biological control of aphids in Hawaii, particularly in light of new parasitoid introductions, is discussed.     

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.     

Microsite conditions influence nutritive value characteristics of a tall fescue cultivar devoid of,or infected with a native,or a novel non-ergogenic endophyte

Tall fescue [Lolium arundinaceum, Schreb., S.J. Darbysh.] productivity and persistence often benefits from association with Neotyphodium coenophialum [Morgan-Jones and Gams], Glenn, Bacon, and Hanlin) endophyte. The influence of novel, non-ergogenic endophytes on nutritive value is unclear, especially when simultaneous stresses (e.g., defoliation and shading) are imposed on the association. We conducted a field experiment using Jesup tall fescue that had either a native or novel non-ergogenic fungal endophyte (AR542; referred to as MaxQ?), or that was endophyte free. Dry matter production and nutritive value including crude protein (CP), non-structural carbohydrates (TNC), ergo- and loline alkaloids, and phenolics were determined for plants stockpiled or clipped repeatedly in sites differing in the amount of light. Productivity varied less among sites when plants were infected with a native endophyte compared to novel or no endophyte. The trend suggests that native endophyte contributed to resilience of the host in this experiment. Leaf dry matter content was affected by host–endophyte association interacting with light availability suggesting differences in leaf composition could occur. Herbage CP increased, whereas TNC decreased with increasing shade. The concentration of loline alkaloids, irrespective of host–endophyte association, tended to increase in leaves with decreasing light availability and could be related to the relatively greater N concentrations in shade-grown leaves. Phenolics decreased in leaves, but increased in stembases as light availability decreased. The combination of increased loline alkaloids in leaves and phenolics in stembases, suggests that shade-grown tall fescue might have some competitive advantage based on the known anti-herbivory attributes of loline alkaloids and phenolic compounds.     

The Endosymbiont Arsenophonus Is Widespread in Soybean Aphid,Aphis glycines,but Does Not Provide Protection from Parasitoids or a Fungal Pathogen

Aphids commonly harbor bacterial facultative symbionts that have a variety of effects upon their aphid hosts, including defense against hymenopteran parasitoids and fungal pathogens. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is infected with the symbiont Arsenophonus sp., which has an unknown role in its aphid host. Our research goals were to document the infection frequency and diversity of the symbiont in field-collected soybean aphids, and to determine whether Arsenophonus is defending soybean aphid against natural enemies. We performed diagnostic PCR and sequenced four Arsenophonus genes in soybean aphids from their native and introduced range to estimate infection frequency and genetic diversity, and found that Arsenophonus infection is highly prevalent and genetically uniform. To evaluate the defensive role of Arsenophonus, we cured two aphid genotypes of their natural Arsenophonus infection through ampicillin microinjection, resulting in infected and uninfected isolines within the same genetic background. These isolines were subjected to parasitoid assays using a recently introduced biological control agent, Binodoxys communis [Braconidae], a naturally recruited parasitoid, Aphelinus certus [Aphelinidae], and a commercially available biological control agent, Aphidius colemani [Braconidae]. We also assayed the effect of the common aphid fungal pathogen, Pandora neoaphidis (Remaudiere & Hennebert) Humber (Entomophthorales: Entomophthoraceae), on the same aphid isolines. We did not find differences in successful parasitism for any of the parasitoid species, nor did we find differences in P. neoaphidis infection between our treatments. Our conclusion is that Arsenophonus does not defend its soybean aphid host against these major parasitoid and fungal natural enemies.     

Acute exposure to ergot alkaloids from endophyte-infected tall fescue does not alter absorptive or barrier function of the isolated bovine ruminal epithelium

Ergot alkaloids in endophyte-infected (Neotyphodium coenophialum) tall fescue (Lolium arundinaceum) have been shown to cause a reduction in blood flow to the rumen epithelium as well as a decrease in volatile fatty acids (VFA) absorption from the washed rumen of steers. Previous data also indicates that incubating an extract of endophyte-infected tall fescue seed causes an increase in the amount of VFA absorbed per unit of blood flow, which could result from an alteration in the absorptive or barrier function of the rumen epithelium. An experiment was conducted to determine the acute effects of an endophyte-infected tall fescue seed extract (EXT) on total, passive or facilitated acetate and butyrate flux across the isolated bovine rumen as well as the barrier function measured by inulin flux and tissue conductance (G_t). Flux of ergovaline across the rumen epithelium was also evaluated. Rumen tissue from the caudal dorsal sac of Holstein steers (n=6), fed a common diet, was collected and isolated shortly after slaughter and mounted between two halves of Ussing chambers. In vitro treatments included vehicle control (80% methanol, 0.5% of total volume), Low EXT (50 ng ergovaline/ml) and High EXT (250 ng ergovaline/ml). Results indicate that there is no effect of acute exposure to ergot alkaloids on total, passive or facilitated flux of acetate or butyrate across the isolate bovine rumen epithelium (P>0.51). Inulin flux (P=0.16) and G_t (P>0.17) were not affected by EXT treatment, indicating no alteration in barrier function due to acute ergot alkaloid exposure. Ergovaline was detected in the serosal buffer of the High EXT treatment indicating that the flux rate is ~0.25 to 0.44 ng/cm² per hour. Data indicate that specific pathways for VFA absorption and barrier function of the rumen epithelium are not affected by acute exposure to ergot alkaloids from tall fescue at the concentrations tested. Ergovaline has the potential to be absorbed from the rumen of cattle that could contribute to reduced blood flow and motility and lead to reduced growth rates of cattle.     

Impact of a parasitoid on the bacterial symbiosis of its aphid host

Embryo production in aphids is absolutely dependent on the function of symbiotic bacteria, mainly Buchnera, and the growth and development of koinobiont parasitoids in aphids requires the diversion of nutrients from aphid embryo production to the parasitoid. The implication that the bacterial symbiosis may be promoted in parasitized aphids to support the growing parasitoid was explored by analysis of the number and biomass of mycetocytes, and the aphid cells bearing Buchnera, in the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) parasitized by the wasp Aphidius ervi Haliday (Hymenoptera: Braconidae). Aphids hosting a young larval parasitoid bore more mycetocytes of greater total biomass, and embryos of lower biomass than unparasitized aphids. Furthermore, one of the three aphid clones tested, which limited teratocyte growth (giant cells of parasitoid origin having a trophic role), bore smaller mycetocytes and larger embryos, than one or both of the two aphid clones with greater susceptibility to the parasitoid. These data suggest that susceptibility of the aphid‐Buchnera symbiosis to parasitoid‐mediated manipulation may, directly or indirectly, contribute to aphid susceptibility to parasitoid exploitation.     

Does variation in host plant association and symbiont infection of pea aphid populations induce genetic and behaviour differentiation of its main parasitoid, Aphidius ervi?

The host-associated differentiation (HAD) hypothesis states that higher trophic levels in parasitic associations should exhibit similar divergence in case of host sympatric speciation. We tested HAD on populations of Aphidius ervi the main parasitoid of the pea aphid Acyrthosiphon pisum, emerging from host populations specialized on either alfalfa or red clover. Host and parasitoid populations were assessed for genetic variation and structure, while considering geography, host plant and host aphid protective symbionts Regiella insecticola and Hamiltonella defensa as potential covariables. Cluster and hierarchical analyses were used to assess the contribution of these variables to population structure, based on genotyping pea aphids and associated A. ervi with microsatellites, and host aphid facultative symbionts with 16S rDNA markers. Pea aphid genotypes were clearly distributed in two groups closely corresponding with their plant origins, confirming strong plant associated differentiation of this aphid in North America. Overall parasitism by A. ervi averaged 21.5 % across samples, and many parasitized aphids producing a wasp hosted defensive bacteria, indicating partial or ineffective protective efficacy of these symbionts in the field. The A. ervi population genetic data failed to support differentiation according to the host plant association of their pea aphid host. Potential for parasitoid specialization was also explored in experiments where wasps from alfalfa and clover aphids were reciprocally transplanted on alternate hosts, the hypothesis being that wasp behaviour and parasitic stages should be most adapted to their host of origin. Results revealed higher probability of oviposition on the alfalfa aphids, but higher adult emergence success on red clover aphids, with no interaction as expected under HAD. We conclude that our study provides no support for the HAD in this system. We discuss factors that might impair A. ervi specialization on its divergent aphid hosts on alfalfa and clover.     

Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks

Climate change leads to phenology shifts of many species. However, not all species shift in parallel, which can desynchronize interspecific interactions. Within trophic cascades, herbivores can be top–down controlled by predators or bottom–up controlled by host plant quality and host symbionts, such as plant-associated micro-organisms. Synchronization of trophic levels is required to prevent insect herbivore (pest) outbreaks. In a common garden experiment, we simulated an earlier arrival time (~2 weeks) of the aphid Rhopalosiphum padi on its host grass Lolium perenne by enhancing the aphid abundance during the colonization period. L. perenne was either uninfected or infected with the endophytic fungus Epichloë festucae var. lolii. The plant symbiotic fungus produces insect deterring alkaloids within the host grass. Throughout the season, we tested the effects of enhanced aphid abundance in spring on aphid predators (top–down) and grass–endophyte (bottom–up) responses. Higher aphid population sizes earlier in the season lead to overall higher aphid abundances, as predator occurrence was independent of aphid abundances on the pots. Nonetheless, after predator occurrence, aphids were controlled within 2 weeks on all pots. Possible bottom–up control of aphids by increased endophyte concentrations occurred time delayed after high herbivore abundances. Endophyte-derived alkaloid concentrations were not significantly affected by enhanced aphid abundance but increased throughout the season. We conclude that phenology shifts in an herbivorous species can desynchronize predator–prey and plant–microorganism interactions and might enhance the probability of pest outbreaks with climate change.     

Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems?

We have investigated community and ecosystem consequences of endophyte symbiosis with tall fescue over the past 13 y. Lolium arundinaceum is the most abundant plant in the eastern USA, and most is infected by the wild-type KY-31 endophyte Neotyphodium coenophialum. We established two large experimental grasslands (in 1994 and in 2000) with endophyte-infected or endophyte-free seed sown on recently plowed herbaceous vegetation. Other plant species established by seed or vegetative fragments. No other treatments were applied and plots were subject to natural biotic and abiotic variation. A third experiment examined ecological influences on endophyte infection dynamics starting from an intermediate infection frequency. Finally, we synthesized recent literature investigating the impacts of the tall fescue endophyte on the abundance of associated arthropod species. We found wide-ranging consequences of the endophyte from significant effects on soil feedback and decomposition rates, to plant-plant competition, diversity, productivity, invasibility and succession, to plant-herbivore interactions and energy flow through the food web. Further, we found that herbivore pressure caused rapid increases in infection frequency. Our results suggest that endophyte symbiosis in tall fescue can have a transforming effect on ecological systems.     

Influence of “protective” symbionts throughout the different steps of an aphid–parasitoid interaction

Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e., from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum, and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid–symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola, two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid–symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host–parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect–symbiont associations.     

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

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

Floral diversity, parasitoids and hyperparasitoids – A laboratory approach

Adding floral resources to agro-ecosystems to improve biological control can enhance the survival, egg load, and parasitism rate of insect parasitoids. However, this may not always be the case because the herbivore may benefit from the added resource as much as, or more than the third-trophic level. In addition, the natural enemies of those in the third-trophic level may also derive improved fitness from the added resources. Both these processes will dampen trophic cascades, leading to less-effective biological control. In this study, the effect of adding different flowering plants on the longevity, egg load, aphid parasitism rates and hyperparasitism of Aphidius ervi Haliday (Hymenoptera: Braconidae) by its hyperparasitoid Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) were investigated, using the pea aphid Acyrthosiphon pisum Harris (Homoptera: Aphididae) as the herbivore. Parasitoids exposed to buckwheat survived, on average, between four to five times as long as those in the control (water) and those in phacelia, alyssum and coriander treatments survived three to four times as long. Hyperparasitoids exposed to buckwheat survived five to six times as long as those in the control and three to five times longer with the other plants compared with the control. Almost all flower species significantly increased parasitoid and hyperparasitoid egg loads and the number of parasitised aphids and parasitised mummies compared with control. Understanding the factors influencing the dynamics of multitrophic interactions involving flowering plants, herbivores, parasitoids and hyperparasitoids is a fertile area for future research. One of the most challenging areas in contemporary ecology concerns the relative importance of different types of biodiversity mediating trophic interactions and thereby influencing the structure of communities and food webs. This paper begins to explore this using an experimental, laboratory-based approach.     

The effect of entomopathogenic Lecanicillium spp. (Hypocreales: Cordycipitaceae) on the aphid parasitoid Aphidius colemani (Hymenoptera: Aphidiinae)

The effects of entomopathogenic Lecanicillium spp. (Zare and Gams) on Aphidius colemani (Viereck) adult longevity and ovipositional behavior and on the emergence rate and longevity of the F₁ generation of this parasitoid insect were evaluated under laboratory conditions. Moreover, the ability of three strains of Lecanicillium spp. to penetrate the cuticle of aphids parasitized by A. colemani at different larval stages was investigated. Although fungal treatments at high concentrations (10⁷?conidia/ml) reduced adult longevity, no significant effects were observed at lower concentrations. The number of ovipositional probings, sting failure rate of the ovipositor, and time intervals between periods of ovipositional behavior were not significantly different between the experimental groups and controls at all concentrations for all fungal strains. Fungal inoculation showed no significant effects on the emergence rate and longevity of the adult A. colemani F₁ generation. Fungal penetration was detected in 60?% of aphids inoculated with fungi 7?days after parasitoid exposure. However, fungal detection was drastically reduced and undetectable when fungal inoculation occurred 8 and 9?days after parasitization, respectively. Our results suggest the coapplication of Lecanicillium spp. and A. colemani for aphid control is possible under certain conditions because of their high compatibility.     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

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

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

Encroachment of Endophyte-infected on Endophyte-free Tall Fescue

Persistence of endophyte-free (E-) tall fescue (Festuca arundinaceaSchreb.)is erratic. Little information exists as to how fast endophyte(Neotyphodium coenophialum)-infected (E+) tall fescue mightencroach on E- tall fescue and whether specific conditions mightinfluence the speed of encroachment. Plots of E+ and E- tallfescue genotypes 7 and 17 were established using a modifiedNelder's design to compare performance of the E+ forms of theplants in pure and mixed communities at different populationdensities. The plots were planted at the USDA Southern PiedmontConservation Research Laboratory in Watkinsville, Georgia, andthe University of Georgia Plant Sciences Farm in Bogart, Georgia.Plants were grown over a 5 year period and dry matter yieldmonitored 1, 3, and 5 years after establishment. Relative crowdingcoefficients were calculated for each to establish trends ofencroachment of the E+ on the E- plants in the mixed communities.Generally, dry matter yields of E+ tall fescue were greaterthan E- tall fescue regardless of whether they were grown inpure or mixed communities. As time progressed, the differencein dry matter yield between E+ and E- tall fescue grown in mixedcommunities was greater than that of the pure communities. Relativecrowding coefficients increased as time progressed. Relativecrowding coefficients at the Watkinsville location were greaterafter 5 years than those at the Plant Sciences Farm. Therefore,site specific conditions exist which affect the competitivenessof E- tall fescue and degree of encroachment by E+ tall fescue.Research is needed to identify which biotic, abiotic and managementvariables exacerbate encroachment of E+ tall fescue to betterdefine the conditions which best suit E- tall fescue.Copyright1998 Annals of Botany Company tall fescue, endophyte,Neotyphodium coenophialum,Festuca arundinacea, competition, population density     

Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems

Community structures of aphids and their parasitoids were studied in fruit crop habitats of eastern Belgium in 2014 and 2015. Quantitative food webs of these insects were constructed separately for each year, and divided into subwebs on three host‐plant categories, fruit crop plants, non‐crop woody and shrub plants and non‐crop herbaceous plants. The webs were analyzed using the standard food web statistics designed for binary data. During the whole study period, 78 plant species were recorded as host plants of 71 aphid species, from which 48 parasitoid species emerged. The community structure, aphid / parasitoid species‐richness ratio and trophic link number varied between the two years, whereas the realized connectance between parasitoids and aphids was relatively constant. A new plant–aphid–parasitoid association for Europe was recorded. Dominant parasitoid species in the study sites were Ephedrus persicae, Binodoxys angelicae and Praon volucre: the first species was frequently observed on non‐crop trees and shrubs, but the other two on non‐crop herbaceous plants. The potential influence, through indirect interactions, of parasitoids on aphid communities was assessed with quantitative parasitoid‐overlap diagrams. Symmetrical links were uncommon, and abundant aphid species seemed to have large indirect effects on less abundant species. These results show that trophic indirect interactions through parasitoids may govern aphid populations in fruit crop habitats with various non‐crop plants, implying the importance for landscape management and biological control of aphid pests in fruit agroecosystems.