Large‐scale migration synchrony between parasitoids and their host

1. Parasitoids are a valuable group for conservation biological control. In their role as regulators of aphid pests, it is critical that their lifecycle is synchronised with their hosts in both space and time. This is because a synchronised parasitoid community is more likely to strengthen the overall conservation biological control effect, thus damping aphid numbers and preventing potential outbreaks. One component of this host–parasitoid system was examined, that of migration, and the hypothesis that peak summer parasitoid and host migrations are synchronised in time was tested. 2. Sitobion avenae Fabricius and six associated parasitoids were sampled from 1976 to 2013 using 12.2‐m suction‐traps from two sites in Southern England. The relationship between peak weekly S. avenae counts and their parasitoids was quantified. 3. Simple regression models showed that the response of the peak parasitoids to the host was positive: generally, more parasitoids migrated with increasing numbers of aphids. Further, when averaged over time, the parasitoid migration peak date corresponded with the aphid migration peak. The co‐occurrence of the peaks was between 51% and 64%. However, the summer peak in aphid migration is not steadily shifting forward with time unlike spring first flights of aphids. Cross‐correlation analysis showed that there were no between‐year lagged effects of aphids on parasitoids. 4. These results demonstrate that the peak in migration phenology between host and parasitoid is broadly synchronised within a season. Because the threshold temperature for flight (> 12 °C) was almost always exceeded in summer, the synchronising agent is likely to be crop senescence, not temperature. Studies are needed to assess the effects of climate change on the mismatch potential between parasitoids and their hosts.     

Assessment of aphid lethal paralysis virus as an apparent population growth‐limiting factor in grain aphids in the presence of other natural enemies

The influence of aphid lethal paralysis virus (ALPV), Rhopalosiphum padi virus (RhPV), natural enemies and fungal infection on the population growth of Rhopalosiphum padi and Sitobion avenae in the wheat fields of the Western Cape Province of South Africa was investigated at two sites. Time‐specific life tables were compiled for R. padi at one site. During the logarithmic phase of the development of R. padi aphids, natural enemies were not present in high numbers and the apparent large‐scale mortality observed appeared to be due to other causes. During the decline phase of this aphid population, the population size was reduced by 49%. This reduction coincided with a calculated high mortality of 70 aphids per plant. A dramatic decline in R. padi numbers and a high incidence of ALPV present in the aphid population was experienced during this period. Virus assays were carried out by double‐antibody sandwich enzyme‐linked immunosorbent assay (DAS‐ELISA) and an indirect immunofluorescent technique. Entomophthorales‐type fungal infection of aphids also reached its highest level during the decline phase, but at a later stage than ALPV infection, with a calculated level of 21 aphids per plant. This suggested that the presence of ALPV limited population development in R. padi. Similar results were obtained with S. avenae.     

Interactions of Russian wheat aphid, a hymenopterous parasitoid and resistant and susceptible slender wheatgrasses

Interactions among three trophic levels of resistant and susceptible slenderwheat grasses, Elymus trachycaulum (Link) Goule ex Shinners ex. H.F. Lewis, Russian wheat aphid, Diuraphis noxia (Mordvilko), and a hymenopterous parasitoid were studied in the laboratory and greenhouse. These relationships were compared with a commercial susceptible wheat Triticum aestivum L. variety. Aphids reared on the resistant entries showed significantly lower weights and numbers. Significant reduction of parasitoid mummy weight and adult size was positively correlated with the effects on the aphids. Resistant entries also induced a longer prereproductive period for both the aphids and parasitoids. Numbers of aphids and aphid damage were significantly modified by the addition of parasitoids. Parasitism was higher on plants that did not have leaf rolling. These findings may indicate that antibiosis resistance studied here is not the most desirable because it decreases natural enemy vitality.     

Effects of Collembola and fertilizers on plant performance (Triticum aestivum) and aphid reproduction (Rhopalosiphum padi)

Effects of Collembola (Protaphorura fimata) on the development of wheat (Triticum aestivum) and the reproduction of aphids (Rhopalosiphum padi) were investigated at different soil nutrient concentrations in a laboratory experiment. Fertilization with N and NPK increased biomass and nitrogen content of wheat, aphid reproduction and abundance of Collembola. Presence of Collembola tended to decrease biomass of leaves and ears, and caused a delayed ear production of the plants. Aphid reproduction was significantly reduced in the presence of Collembola (−14%) and most pronounced in fertilizer treatments. We suggest that the reduction of aphid reproduction is caused by Collembola-mediated changes in resource allocation and growth of wheat.     

Aphid suppression by natural enemies in mulched cereals

Large populations of natural enemies are the basis for natural pest control. Effects of mulch on predator–prey interactions in arable fields are poorly known, despite its potential to enhance ground‐dwelling predators and thereby reduce pest infestations. We studied the densities of predators and parasitoids, and their impact on cereal aphids in the presence and absence of mulch. Released populations of the bird cherry aphid, Rhopalosiphum padi (L.) (Homoptera: Aphididae), and two naturally occurring aphid species, were monitored under experimentally reduced densities of: (i) ground‐dwelling predators, (ii) flying predators and parasitoids, and (iii) with straw mulch. The three treatments were applied in a 2 × 2 × 2 factorial design in a field of spring wheat (Triticum aestivum L.). The exclusion of ground‐dwelling predators increased aphid populations by 55% in June and 40% in July, respectively. Mulched plots had 25% lower aphid densities in June. This was presumably due to enhanced densities of spiders (Araneida) in mulched plots. The exclusion of flying predators and parasitoids led to 94% higher aphid populations in late July (109 vs. 56 individuals per 100 shoots), irrespective of mulch or ground predator manipulation. This was attributed to the larvae of gall midges Aphidoletes cf. aphidimyza (Rondani) (Diptera: Cecidomyiidae) and hoverflies (Diptera: Syrphidae). The results indicate that a scarcity of predators and a bare soil surface renders crops more susceptible to arthropod pests. Farming schemes should aim at enhancing both ground‐dwelling and flying predators for elevated levels of natural pest control.     

Annual predictions of the peak numbers of Sitobion avenae infesting winter wheat

Sitobion avenae is the most abundant aphid that infests the ears of winter wheat in central Europe. Control of this pest will benefit from prediction of its maximum abundances on ears. We attempted to predict the maximum numbers of this species infesting the ears using earlier counts of this species in ears and on leaves using data collected in the Czech Republic in 2002–2014. The numbers of aphids on particular leaves and the ears were recorded at weekly intervals. The maximum numbers infesting the ears were significantly related to aphid counts on the ears made 1 week, 2 weeks and even 3 weeks before the peak. A regression based only on plots where there were aphids (non‐zero aphid counts) recorded 3 weeks prior to the peak resulted in a critical number of ≥0.44 aphids/ear, which if exceeded resulted in a harmful maximum abundance of ≥5 aphids/ear at the peak. We also regressed maximum numbers infesting ears on numbers of S. avenae on leaves recorded 1, 2 and 3 weeks after earing, which all resulted in reliable predictions. Regression of maximum abundance on non‐zero aphid counts on the leaves in week 3 after earing revealed a critical number of ≥0.59 aphids/tiller. Zero aphid counts resulted in only 3% of cases of a harmful maximum abundance in ears. Using records of the numbers on flag leaves, which make up 58% of the S. avenae population present on the foliage, also provided reliable predictions of maximum abundance in ears. Predicting maximum numbers of aphids from earlier records of the numbers of aphids on leaves or ears is thus possible. The prediction may be further improved by increasing the precision with which the numbers of aphids initially infesting the crop are estimated.     

Tolerance of antibiotic and susceptible cereal seedlings to the aphids Metopolophium dirhodum and Rhopalosiphum padi

Some cereal seedlings exhibit antibiotic and antixenotic resistance to the aphids Metopolophium dirhodum (Walker) and Rhopalosiphum padi (L.), because the seedlings contain hydroxamic acids or gramine. The association between tolerance to aphids and aphid antibiosis was investigated for three cereals, Dollarbird wheat Vulcan wheat and Yagan barley. The dry biomass gained by the aphids and the simultaneous reduction in the biomass of the plants (biomass conversion ratio) quantified tolerance. Biomass production and the density dependence of biomass production by the aphids quantified antibiosis more effectively than fecundity. Vulcan wheat, which has more hydroxamic acid than Dollarbird wheat showed the highest level of antibiosis, and the barley was not antibiotic for either aphid. The biomass conversion ratio was a constant; the biomass of an infested plant was reduced by 3 mg for each mg of aphid biomass gained, regardless of aphid species, plant cultivar, or aphid density. The three plants showed no differential tolerance to the aphids, and therefore tolerance is not associated with antibiosis in this case.     

Fly disturbance suppresses aphid population growth

1. The presence of predators is known to suppress prey populations not only by consumptive but also by non-consumptive effects, as it stresses the prey inducing costly changes to behaviour and physiology. However, there is recent evidence that disturbance from non-predacious, non-competing commensals can also negatively affect herbivore performance. 2. Populations of cherry-oat aphids (Rhopalosiphum padi L.) were initiated with adult aphids in mesocosms containing seedling wheat grass. Following aphid establishment, fruit flies (Drosophila melanogaster Meigen) were added at a relatively high density to half of the mesocosms and the aphids were left for another 5 days to reproduce. The experiment was performed over two blocks at 24 ± 4 °C. It was hypothesized that a relatively high density of commensals would stress the aphids and reduce their fitness, causing lower population growth and resulting in lower population sizes. 3. Aphid numbers were significantly lower in mesocosms with commensal flies after 5 days of fly presence across the two experimental blocks, documenting that fly disturbance suppresses aphid fitness and population growth. 4. The negative effect of fruit flies on aphid population growth must have come from the disturbance that flies imposed on the aphids in their search for food, indicating that the flies stressed the aphids. Thus, our study indicates that commensals may stress herbivores that do not distinguish between enemies and other active species in their environment, adding in the overall herbivore top-down control through fitness costs.     

Interactions between tomato volatile organic compounds and aphid behaviour

Abstract

In the tritrophic system consisting of tomato, Solanum lycopersicum (L.), the aphid Macrosiphum euphorbiae (Thomas) and its natural enemy, the parasitoid Aphidius ervi (Haliday), it has been shown that the release of volatile organic compounds following aphid attack is responsible for attracting aphid parasitoids in wind tunnel experiments. The main compounds involved in these multitrophic interactions have been characterized and quantified. In this work, the possible activity of such compounds on plant direct defences against the aphid M. euphorbiae was assessed in laboratory tests. The selected compounds were applied to uninfested tomato plants, either by evaporation or contact, and performance of aphids, in terms of plant acceptance, fixing behaviour and aphid development, calculated in standard conditions. The results showed that two compounds, namely methyl salicylate and cis-hex-3-en-1-ol, alter aphid performance. These two compounds have been reported to be those eliciting the best response by A. ervi in terms of flight behavior (wind tunnel bioassay) and antennal stimulation (EAG bioassay).     

Natural occurrence of entomophthoroid fungi (Entomophthoromycota) of aphids (Hemiptera: Aphididae) on cereal crops in Argentina

The spectrum of entomophthoroid fungal species parasitising aphids on cereal crops and a study of the phenology and prevalence of these pathogens were investigated in Argentina. The studies were conducted at six different sites cultivated with crops of Triticum aestivum (wheat), Avena sativa (oats) and Sorghum bicolor (sorghum) during two consecutive years. Entomopathogenic fungi from the new phylum Entomophthoromycota were recorded from six aphid species on cereals in Argentina: Rhopalosiphum maidis, Rhopalosiphum padi, Rhopalosiphum rufiabdominalis, Schizaphis graminum, Sitobion avenae and Sipha maydis. Three species of entomophthoroid fungi were found infecting these aphid species: Pandora neoaphidis, Zoophthora radicans (Entomophthorales: Entomophthoraceae) and Neozygites fresenii (Neozygitales: Neozygitaceae). Entomophthoroid fungal infections occurred mostly in autumn–winter seasons (March–August), and coincided with periods of high relative humidity and comparatively low temperatures. This study represents the first base‐line characterisation of entomophthoroid fungi infecting aphids on cereal crops in Argentina.     

Semiochemicals associated to spacing behaviour of the bird cherry-oat aphid Rhopalosiphum padi L. (Hem., Aphididae) do not affect the olfactometric behaviour of the cereal aphid parasitoid Aphidius rhopalosiphi De Stephani-Pérez (Hym., Braconidae)

Volatiles produced by the interaction of Rhopalosiphum padi and wheat, and semiochemicals which elicit the spacing behaviour of R. padi on wheat and oat, were evaluated in an olfactometer against the cereal aphid parasitoid Aphidius rhopalosiphi . The parasitoid was attracted by volatiles produced by the R. padi -wheat interaction at high density of aphids, but not by the R. padi -wheat interaction at low density. Compounds produced by the interaction of wheat or oat that was infested with a high density of aphids (approximately 9 aphids/cm²), 6-methyl-5-hepten-2-one (MHO), 6-methyl-5-hepten-2-ol (MHOH), 2-tridecanone (2-T), and methyl salicylate (MS), neither attracted nor repelled A. rhopalosiphi as pure compounds or in the naturally occurring mixture. The results are discussed in terms of the use of semiochemicals and parasitoids in the integrated management of aphid pests.     

The effect of the systemic fungicide benomyl on survival and reproduction of the bird cherry aphid (Rhopalosiphum padi)

Weight gain and intrinsic rate of population increase (r_m) of Rhopalosiphum padi were measured on wheat plants given soil drenches of benomyl at various concentrations. Reduced weight gain occurred with concentrations as low as 3.125 ppm. Mortality of aphids significantly exceeded control mortality at 25 ppm, and no aphids survived concentrations above 50 ppm. Development time was extended at 12.5 ppm and above. Reductions in fecundity and r_m became statistically significant by 25 ppm. Topical application of benomyl at 100 ppm or above increased aphid mortality, which reached 97% at 400 ppm. Weight gain of aphids was also reduced by topical application at 100 ppm. A factorial experiment showed absence of interaction between the effects on aphid weight of soil drench application to plants and topical application to aphids.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.     

The Role of Natural Enemy Foraging Guilds in Controlling Cereal Aphids in Michigan Wheat

Insect natural enemies (predators and parasitoids) provide important ecosystem services by suppressing populations of insect pests in many agricultural crops. However, the role of natural enemies against cereal aphids in Michigan winter wheat (Triticum aestivum L.) is largely unknown. The objectives of this research were to characterize the natural enemy community in wheat fields and evaluate the role of different natural enemy foraging guilds (foliar-foraging versus ground-dwelling predators) in regulating cereal aphid population growth. We investigated these objectives during the spring and summer of 2012 and 2013 in four winter wheat fields on the Michigan State University campus farm in East Lansing, Michigan. We monitored and measured the impact of natural enemies by experimentally excluding or allowing their access to wheat plants infested with Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hemiptera: Aphidae). Our results indicate that the natural enemy community in the wheat fields consisted mostly of foliar-foraging and ground-dwelling predators with relatively few parasitoids. In combination, these natural enemy groups were very effective at reducing cereal aphid populations. We also investigated the role of each natural enemy foraging guild (foliar-foraging versus ground-dwelling predators) independently. Overall, our results suggest that, in combination, natural enemies can almost completely halt early-season aphid population increase. Independently, ground-dwelling predators were more effective at suppressing cereal aphid populations than foliar-foraging predators under the conditions we studied. Our results differ from studies in Europe and the US Great Plains where foliar foraging predators and parasitoids are frequently more important cereal aphid natural enemies.     

The role of refuge areas in the phenology of Rhopalosiphum padi in low rainfall cropping areas of South Australia

Extensive surveys of possible aphid habitats in South Australia indicated that irrigated perennial grass pastures in the Mount Lofty Ranges and Lower Murray Valley were summer refuges for Rhopalosiphum padi (L.) (Hemiptera: Aphididae). Large numbers of aphids build up in these pastures each year during autumn (April and May) with numbers peaking in May. The size of the May peak was related to the number of aphids surviving the summer. The proportions of alates were highest in May and August/September. Both peaks coincided with a photoperiod of between 11.2 and 11.5 h, and partial correlations suggested that aphid density, photoperiod and temperature were all significant determinants of alate production.     

Field manipulation of populations of individual staphylinid species in cereals and their impact on aphid populations

Abstract.

• 1 Four species of staphylinids were caged separately on wheat and their effect on the population development of the grain aphid, Sitobion avenae (F.), was investigated over two seasons.
• 2 A novel field cage design was used to exclude all but the staphylinid species under investigation.
• 3 Predator effects were compared with total-exclusion cages in which all predators and parasitoids were kept out.
• 4 During a high-density phase of aphid population development only Philonthus cognutus (Stephens) significantly influenced aphid population numbers.
• 5 At low aphid densities, Tachyporus obtusus (L.), T.chrysomelinus (L.) and P.cognatus reduced aphid population levels.
• 6 The experiments showed that Tachyporus spp. can reduce the numbers of cereal aphids prior to the exponential phase of aphid population increase and that P.cognatus causes some reduction at both the stages of aphid population growth investigated.

     

Host plant genotype determines bottom‐up effects in an aphid‐parasitoid‐predator system

Plant genotypes are known to affect performance of insect herbivores and the community structure of both herbivores and higher trophic levels. Still, only a limited number of studies demonstrate differences in the performance of predators and parasitoids because of plant genotypic effects and most of these focus on gall formers. We designed a greenhouse experiment to investigate the effects of host plant genotype on fitness components in a grass‐aphid‐carnivore system. We used clones of quackgrass [Elytrigia repens (L.) Desv. ex Nevski (Poaceae)], the aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae), the parasitoid wasp Aphidius colemani (Viereck) (Hymenoptera: Braconidae), and the predatory lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). The number of aphid offspring differed considerably among plant genotypes. These differences were only in part because of differences in the production of biomass among host genotypes. Therefore, genotypes may differ in their nutritional value for phytophages. The number of aphids attacked by the parasitoid also differed among genotypes and aphid numbers only partly accounted for this effect. Moreover, pupal development time of female parasitoids was affected by plant genotype. We found no differences in mortality, body size, or sex ratio of hatching wasps between genotypes of quackgrass. Development time of the larvae and larval weight of the predatory lacewings differed among genotypes, but not weight of pupae and adults. Generally, the proportion of the total variance explained by the plant genotype was smaller for parasitoids and predators than for aphids. Overall, our experiments indicated that the plant genotype affects tri‐trophic interactions, but also that the strength of these effects decreases along the food chain.     

A physiologically based model of pest–natural enemy interactions

The population dynamic processes in aphids and mites are very similar, because the two groups show strong similarities in their biology. Resource limitation, density-dependent emigration and natural enemies are major factors controlling aphid and mite populations, but an assessment of their relative importance has proven difficult. We used a physiologically based simulation model to investigate the relative impact of the three factors on aphid pest populations. The present simulation model includes winter wheat, three aphid species, Metopolophium dirhodum (Wlk.), Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hom.: Aphididae) and three parasitoids, Aphelinus abdominalis Dalman (Hym.: Apheliniidae), Aphidius rhopalosiphi De Stefani-Perez and Praon volucre (Hal.) (Hym.: Aphidiidae). We derived and parameterized the model from literature data and validated it against independent field data. The study showed that resource limitation and density-dependent alate production restricts aphid numbers in the field. The mortality due to parasitoids increased late in the season and reduced the peak aphid numbers only moderately. The modelling approach we used is appropriate for simulating other pest–natural enemy systems, such as the spider mite–predatory mite system. Using an object-oriented modelling framework as a template, acarologists can now efficiently develop the simulation model of their choice. This revised version was published online in November 2006 with corrections to the Cover Date.     

Seasonal incidence of aphid,Amphorophora ampullata Bukton (Homoptera: Aphididae) on fern,Hypolepis polypodioides (Blume) Hook (Hypolepidaceae) from Western Himalaya

Seasonal incidence of aphid, Amphorophora ampullata on Hypolepis polypodioides was recorded throughout the year from November 2012 to November 2013 at weekly interval. Peak incidence of aphid was recorded during third week of November 2012 (25.94 ± 2.39 aphids/pinna), later the aphid population gradually decreased from December 2012 onwards and reached below threshold level during the last week of January (0.1 ± 0 aphids/pinna). The aphid population starts building up again from first week of February 2013 (1.6 ± 0.13 aphids/pinna) and attained its peak in the last week of August (32.17 ± 1.22 aphids/pinna) then decreased gradually in the first week of September (20.82 ± 4.70 aphids/pinna). Aphid densities again increased gradually from second week of September (21.62 ± 3.02 aphids/pinna) to November 2013 and reached maximum aphid densities during November (56.55 ± 4.34 aphids/pinna). Among weather parameters, aphid population showed significant positive correlation with relative humidity during morning hours.     

Characterisation of bird cherry-oat aphid (Rhopalosiphum padi L.) behaviour and aphid host preference in relation to partially resistant and susceptible wheat landraces

The bird cherry-oat aphid (Rhopalosiphum padi L.) is a major pest of wheat (Triticum aestivum L.) and can cause up to 30% yield losses. Heritable plant resistance to aphids is both an economically and ecologically sound method for managing aphids. Here we report how the behaviour and performance of R. padi differs on two resistant, one susceptible wheat landrace and a susceptible elite wheat variety. Feeding behaviour differed among the genotypes, with aphids on resistant lines spending longer in the pathway phase and less time phloem feeding. These behaviours suggest that both inter- and intracellular factors encountered during pathway and phloem feeding phases could be linked to the observed aphid resistance. Locomotion and antennal positioning choice tests also revealed a clear preference for susceptible lines. Although feeding studies revealed differences in the first probe indicating that the resistance factors might also be located in the peripheral layers of the plant tissue, scanning electron microscopy revealed no difference in trichrome length and density on the surface of leaves. Aphids are phloem feeders and limiting the nutrient uptake by the aphids may negatively affect their growth and development as shown here in lower weight and survival of nymphs on resistant genotypes and decreased reproductive potential, with lowest mean numbers of nymphs produced by aphids on W064 (54.8) compared to Solstice (71.9). The results indicate that resistant lines markedly alter the behaviour, reproduction and development potential of R. padi and possess both antixenosis and antibiosis type of resistance.