The development and multiple uses of a standardised bioassay method to select hypocrealean fungi for biological control of aphids

A technically standardised bioassay method was designed, evaluated and used to assess virulence and host range of hypocrealean fungi against aphids. A track mounted sprayer was used to apply conidia because hand held versions of the same sprayer can be used for field applications, thereby allowing the outcome from laboratory experiments to predict activity in the field accurately. Eighteen fungal isolates were assessed in single concentration bioassays against the black bean aphid Aphis fabae Scopoli. Isolates comprised commercially available mycoinsecticides (based on Beauveria bassiana and Lecanicillium longisporum) and isolates of B. bassiana, Lecanicillium spp., Paecilomyces fumosoroseus and Metarhizium anisopliae. Aphid mortality was in excess of 80% for 15 isolates, and HRI 1.72 (L. longipsorum), Z11 (P. fumosoroseus), Mycotech strain GHA (B. bassiana) and ARSEF 2879 (B. bassiana) were studied further. Multiple concentration bioassays identified HRI 1.72 as the most virulent isolate against A. fabae with significantly smaller LC₅₀ and LT₅₀ values compared to other isolates. A precise LC₅₀ value (2.95 × 10² conidia ml⁻¹) was calculated for HRI 1.72 using a second multiple concentration assay with smaller concentrations of conidia. The four isolates were applied at a single concentration (1 × 10⁸ conidia ml⁻¹) against Myzus persicae, A. fabae, Acyrthosiphon pisum, Metopolophium dirhodum, Sitobion avenae and Rhopalosiphum padi. A ranking of aphid susceptibility was obtained, such that S. avenae > M. persicae, A. pisum, A. fabae > R. padi. Results indicate the importance of standardising bioassay methods to reduce bioassay variability without compromising the ability to use the bioassay to investigate fungus–host interactions under varying abiotic and biotic conditions.     

Aphid parasitoids detect that an alien plant was present nearby during their development

Abstract Glasshouse and laboratory experiments were conducted with Aphidius rhopalosiphi parasitizing Metopolophium dirhodum to test whether the presence in the same environment of another plant species (tomato or marigold) induced aerial allelopathy in wheat plants.
Emerging parasitoids were offered the choice of two odours of wheat plants in an olfactometer – wheat grown alone and wheat grown in the presence of the second plant species.
Female parasitoids responded more strongly than males, but both sexes preferred the odour of wheat grown in the environment in which they had developed (i.e. with or without the second plant species present).
Moving the tomato plants from the cages where they had been placed with wheat to the cages that had previously had wheat alone just before the aphid mummy formed showed that the odour environment the emerging parasitoid responded to was that of the mummy rather than that of the developing parasitoid larva. From this it was concluded that the parasitoids in the olfactometer were responding not only to wheat volatiles, but also to tomato volatiles absorbed on the surface of the mummy and encountered by the emerging adult parasitoid.
By excising the parasitoid pupa from the mummy formed on one wheat cultivar, and offering the emerging parasitoids the surface of aphid mummies formed on a different cultivar, it was confirmed that olfactometer responses represented a learning of the chemistry of the surface of the mummy encountered at or after emergence.     

Hopkins' 'host selection principle', another nail in its coffin

Abstract. Adult female parasitoids (Aphidius rhopalosiphi De Stef.) (Hymenoptera: Aphidiidae) reared on the aphid Metopolophium dirhodum (Walk.) (Homoptera: Aphididae) changed their responses to odours of two wheat cultivars ('Maris Huntsman' and 'Rapier') when the parasitized aphids had been moved from the former to the latter cultivar at various times after parasitization. If the aphids were moved after less than 6 days, the female parasitoids emerging from mummies by then formed on 'Rapier' responded positively to that cultivar, whereas parasitoids emerging from mummies transferred as still living aphids after 8 days on 'Maris Huntsman', responded positively to that cultivar rather than to 'Rapier' on which they had emerged. This appeared to be evidence for Hopkins' 'host selection principle', which states that chemical experience acquired by the larva of an endopterygote insect can be transferred through the pupal stage to the adult. However, discrimination in favour of either cultivar disappeared when the parasitoids were reared in aphids on both cultivars, and the emerging females were tested following excision of the pupae from the aphid mummies. The previous discrimination shown by adult parasitoids emerging from aphid mummies must therefore be determined by the chemicals contacted by a parasitoid on the skin of the mummy or while biting its way out of the dead aphid.     

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

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

Revisionary notes on the genus Metopolophium Mordvilko, 1914, with keys to European species and descriptions of two new taxa (Homoptera: Aphidoidea)

New and extensively revised keys are given to help identification of the European species of Metopolophium Mordvilko, 1914. The morphs keyed are (1) the apterous viviparous females from Gramineac, (2) the alate viviparous females and (3) the males and oviparous females of those species that overwinter as eggs on Rosa spp. Taxonomic notes are given on some individual species. Two new taxa, M. fasciatum sp. nov., and M. festucae (Theobald) cerealium subsp. nov. are described. Metopolophium myrmecophilum (Theobald) becomes a new synonym of M. festucae (Theobald), sensu stricto , and the resulting question of the possible conservation of the latter, which is the junior subjective synonym, is discussed. A revised checklist of the European species of Metopolophium is given.     

Wheat containing snowdrop lectin (GNA) does not affect infection of the cereal aphid <Emphasis Type="Italic">Metopolophium</Emphasis><Emphasis Type="Italic">dirhodum</Emphasis> by the fungal natural enemy<Emphasis Type="Italic">Pandora neoaphidis</Emphasis>

Studies were carried out to determine if susceptibility of the cereal aphid Metopolophium dirhodum to the fungus Pandora neoaphidis was affected by wheat expressing snowdrop lectin (GNA). Aphid infection did not differ significantly between the transgenic GNA and non-transformed lines (91 and 82%, respectively). Fecundity also did not differ between aphids on the two lines, and was ca. 18 nymphs adult⁻¹. Time to infection was ca. 5 days for M. dirhodum on both lines in two of three assays. Our results indicate that wheat expressing GNA would not compromise the efficacy of P. neoaphidis as a biocontrol agent.     

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

Abstract

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

Aphid flight and change in abundance of winter wheat pests

Composition, dominance and change in population density of species flying over and feeding on winter wheat fields was studied between 1982 and 1998 at Mosonmagyaróvár. There were 29 aphid species among flying insects. The ones imposing risk to winter wheat were as follows: Diuraphis noxia Kurdj., Metopolophium dirhodum Walk., Rho‐palosiphum padi L., Schizaphis graminum Rond., Sitobion avenae Fabr. Number of flying individuals changed year by year, depending principally on climatic factors (temperature, relative humidity, and rainfall). Flight was continuous from late April to harvest. In the average of 17 years flight peak was observed in June.

Establishment of the firsts alate individuals of aphids with holocyclic development can be expected from the second decade of April. As a result of the continuous reproduction, the peak in number of individuals was observed in the second decade of June. During the six years between 1993 and 1998 this value was 17.18 aphids/ plant. Every year there were deviations from the average data, e.g., in 1994 aphid number per plant was 33.61. These pests appeared on the ears in the first decade of June, their number was continuously increasing due to drying of leaves.

During the six years when detailed data were recorded, Rh. padi L. was the dominant species three times (1994: 70.4%; 1995: 82.6%; 1996: 87.9%), M. dirhodum Walk. took this role two times (1993: 67.1%; 1997: 84.8%) and S. avenae Fabr. only once (1998: 53%).

Considering seventeen years’ data, it is necessary to produce resistant varieties and/or seed dressing, or insecticide treatment to control the first alates.     

The value of three cereal aphid species as food for a generalist predator

The value of the cereal aphid species Metopolophium dirhodum (Wlk.), Sitobion avenae (F.) and Rhopalosiphum padi (L.) as prey for the linyphiid spider Erigone atra (Bl.) was assessed. Fecundity of females was determined for spiders fed on eight experimental diets: three single‐species aphid diets, a mixed diet of all three aphid species, three mixed diets with each aphid species in combination with fruit flies Drosophila melanogaster (Meig.), and pure D. melanogaster as a high quality comparison diet. The development and survival of first‐instar juveniles fed on three diets of single aphid species, and on a diet of Collembola were compared with those subjected to starvation. Prey value for adult females was assessed by egg production, hatching success and offspring size. In pure diets all three aphid species were of low value to the spiders, causing a rapid decline in egg production and supporting no growth of significance of first‐instar juveniles. No difference in value of aphid species of single‐species aphid diets was found in the fecundity experiment, while a ranking of aphid species of M. dirhodum > R. padi > S. avenae was revealed in the survivorship experiment. A mixed‐aphid diet was not found to be advantageous compared with single‐species aphid diets, and no advantage of including aphids in mixed diets with fruit flies was found. Metopolophium dirhodum and R. padi were neutral in mixed diets, while a diet of S. avenae and fruit flies caused reduced egg production compared with the pure diet of fruit flies, revealing a toxic effect of S. avenae on the spider. The value‐ranking of aphid species in mixed diets was similar to that of single‐species diets. A similar ranking of aphid species was found for different fitness parameters (fecundity of adult females and development of juveniles). A ranking of aphids by offspring size of mothers on aphid‐only diets was S. avenae > M. dirhodum > R. padi. All aphid‐fruit fly diets resulted in larger offspring than a diet of only D. melanogaster, with the overall largest offspring being produced on the diet of M. dirhodum and fruit flies.     

Improving methods to measure critical thermal limits in phloem‐feeding pest insects

The ability to accurately assess thermal tolerance in the laboratory without compromising ecological relevance is essential to predict the impacts of global climate change on phytophagous pest insects such as the phloem‐feeding aphids. One method to study thermal tolerance employs a temperature‐controlled column to measure critical thermal limits. However, assessments are commonly made with little relation to the natural environment of the study species. This study measured critical thermal minima (CT_min) for three cereal aphids – Sitobion avenae (Fabricius), Metopolophium dirhodum (Walker), and Rhopalosiphum padi (L.) (all Hemiptera: Aphididae) – in the absence and presence of host plant material to determine the best experimental design. Results revealed that CT_min measured in the presence of the host plant was significantly lower, suggesting that performing the measurement in the absence of the host plant could result in an underestimation of insect thermal tolerance. In addition, the study highlights the importance of understanding how an insect interacts with its environment, as this can reveal behavioural variation integral to differential survival at unfavourable temperatures.