Aphid Behaviour Research Articles

Raspberry viruses manipulate the behaviour of their insect vectors

AbstractMany insect herbivores and plant pathogens influence each other via plant‐mediated mechanisms. Although there is speculation that these interactions may be important in structuring terrestrial food webs, few studies have empirically demonstrated the mechanisms by which pathogens manipulate the behaviour of their insect vectors. We investigated how infection of red raspberry, Rubus idaeus L. (Rosaceae), with two viral pathogens, black raspberry necrosis virus (BRNV) and raspberry leaf mottle virus (RLMV), affected the behaviour of their vector, the large raspberry aphid, Amphorophora idaei Börner (Hemiptera: Aphididae: Macrosiphini). As semi‐persistently transmitted viruses, comparatively little is known about how such viruses affect vector biology. We also examined the effect of infection on plant volatile emissions and amino acid content, which could drive changes in aphid behaviour and performance. Virus‐infected plants were initially more attractive to the aphid and the insects remained on infected plants for 30 min, but were found equally on uninfected plants 12 h after inoculation. Twenty‐seven volatile compounds were identified. Two green leaf volatiles were emitted at higher concentrations by infected plants: (Z)‐3‐hexenyl acetate and 2‐hexenal. In dose‐response assays, (Z)‐3‐hexenyl acetate was attractive to the aphid at concentrations of 50 ng ml−1. When reared on infected plants, aphids took more than 3 days longer to reach adulthood compared with those on uninfected plants, although the number of offspring remained the same. Soluble amino acid (essential and non‐essential) concentrations in raspberry leaves increased more than two‐fold with virus infection. Amino acid composition was dominated by glutamate, accounting for 64 and 77% of the total in uninfected and infected leaves, respectively. Excessive glutamate may have underpinned the negative effects of viral infection on aphid performance. These results demonstrate the capacity of viruses to alter their host plant to manipulate vector behaviour, which may have evolved to be consistent with the transmission requirements of the virus.

The Impact of Plant Shaping on Aphid Behavior

The Impact of Plant Shaping on Aphid Behavior The paper provides a review of the studies focusing on the impact of plant trimming and pruning (especially in tree rows) and tree crown formation (in orchards and urban greenery) on the bionomy and number of aphids and some other hemipterans. The fresh, succulent shoots which appear after any trimming and pruning provide aphids with "eternal spring" conditions, i.e. the availability of young leaves and shoots preferred by aphids as a source of nutrition. The majority of aphid species acquiring nutrition from leaves feed on the top shoots. People shape garden greenery, forming beautiful, decorative tree crowns. Some shoots in orchards are regularly cut off; sometimes even apple trees are planted in rows. Instead of building traditional fences, hedges are planted and regularly trimmed. Trimmed plants have fresh, succulent shoots, which are an attractive source of nutrition for many aphids. Large numbers of aphids inhabit these rejuvenated plants. Cutting and trimming of plants often have an impact not only on the number of aphids, but also on their bionomy.

Changes in aphid probing behaviour as a function of insect age and plant resistance level

Aphids perform a series of behaviours to assess feeding suitability and, hence, to select a plant. Little information, however, is available on such behaviour after aphids have settled on a plant. Observation of probing behaviour over an extended period of time can improve our understanding of insect-plant interactions and is instrumental in the study of crop resistance. Here, we assessed the influence of aphid age and plant resistance level on aphid behaviour. An electrical penetration graph (EPG) technique was implemented to monitor the behaviour of potato aphid, Macrosiphum euphorbiae, alates on potato, Solanum tuberosum, and on both a susceptible and a resistant genotype of a wild Solanum species, S. chomatophilum. The behaviour was measured at daily intervals for the first seven days following adult emergence. The results indicated independent and interacting effects of aphid age and plant genotype on probing behaviour. Some behavioural discrepancies between susceptible and resistant genotypes were only observed after the first day, thus highlighting the limits of punctual one-day behavioural studies to assess plant resistance mechanisms. Our work supports the hypothesis that aphids continuously adapt their behaviour to the plant characteristics.

Preference of cereal aphids for different varieties of winter wheat

This paper reports on the development of a simple and robust preference meter (developed in-house) to score the host choice behavior of apterous aphids. With this tool, the preferences of two important cereal aphids Sitobion avenae (Fab.) and Metopolophium dirhodum (Walker) were investigated against four different varieties of winter wheat (Triticum aestivum L.) with a different susceptibility for Fusarium head blight (FHB). Differences in the choice behavior of both aphid species were observed for different wheat varieties. The preferred wheat variety of S. avenae and M. dirhodum was not the same. Also, both aphid species clearly had a differential preference for seedlings and ears. Using seedlings, M. dirhodum was about 1.8 times more rapid in making its choice than S. avenae. In separate experiments with ears, S. avenae was 4.5 times faster than in the experiments with seedlings. In the present study, we aim to highlight differences in preference behavior in relation to potential mechanisms for host selection.

Modulation of Aphid Vector Activity by Potato virus Y on In Vitro Potato Plants.

The effects of the infection of potato (Solanum tuberosum) plants by the nonpersistent Potato virus Y (PVY) were studied on the host plant colonization behavior of different colonizing (Myzus persicae) and noncolonizing (Aphis fabae, Brevicoryne brassicae, and Sitobion avenae) aphid species. The underlying questions of this study were to know how aphids respond when faced with PVY-infected plants and whether plant infection can modify the aphid behavior involved in PVY spread. Short-range orientation behavior was observed using a dual-choice set-up and aphid feeding behavior was monitored using the electrical penetration graph technique. None of the aphid species discriminated between healthy and PVY-infected plants. Nevertheless, most individuals of M. persicae landed on and probed only in one plant whereas noncolonizing aphid species exhibited interplant movements. Study of the aphid feeding behavior showed that PVY infection essentially modified phloem and xylem ingestion. M. persicae and S. avenae exhibited an increased duration of phloem phases on PVY-infected plants whereas A. fabae showed a decreased duration of phloem phases that benefited from an increased duration of xylem ingestion phases. None of these parameters were changed in B. brassicae. These data present evidence that aphids can respond to plants infected by nonpersistent viruses. Such behavioral modifications are discussed within the context of PVY spread in potato crops.

Electrical Penetration Graph Analysis of the Feeding Behavior of Soybean Aphids on Soybean Cultivars With Antibiosis

The soybean aphid, Aphis glycine Matsumura (Hemiptera: Aphididae), is a major pest of soybean. In the current study, we used the Electrical Penetration Graph technique to study feeding behavior of soybean aphids on antibiotic-resistant soybean lines KS1621, KS1613, and KS1642, and a susceptible soybean line, KS4202. We observed that soybean aphids spent significantly shorter periods of time in the sieve element phase but slightly more times in nonprobing phases in all three resistant lines than in the susceptible control. Our study suggests that resistance factors exist in the phloem of the resistant soybean lines, and that these lines may contain antixenosis in addition to antibiosis.

Sublethal effects of flonicamid and thiamethoxam on green peach aphid, Myzus persicae and feeding behavior analysis

The green peach aphid, Myzus persicae Sulzer, is an important sap-sucking pest of many plants, including Chinese cabbage. The objective of the present study was to determine the effects of sublethal concentrations of two insecticides (flonicamid and thiamethoxam) and the action mechanisms on the feeding behavior of M. persicae. The median lethal concentrations (LC50) of flonicamid and thiamethoxam for adult M. persicae were 2.56 and 4.02 mg/L, respectively. The sublethal concentrations of flonicamid were 0.44 mg/L (LC10) and 1.25 mg/L (LC30), and those of thiamethoxam were 1.19 mg/L (LC10) and 2.45 mg/L (LC30). The developmental period of M. persicae nymphs was 5.9 days at LC10 and 6.1 days at LC30 for both insecticides compared to 5.7 days for the control. Adult longevities at LC10 and LC30 of flonicamid were 13.2 and 13.7 days, respectively. Adult longevity at LC10 of thiamethoxam was 14.7 days. Control adult longevity was 11.6 days. Total fecundity was higher at LC10 (41.8 offspring/female) and LC30 (43.0 offspring/female) of flonicamid, and at LC10 (42.1 offspring/female) of thiamethoxam than that of the control (29.5 offspring/female). Feeding behavior analysis using an electrical penetration graph showed that sublethal doses of flonicamid and thiamethoxam had significant effects on the duration of phloem ingestion. However, higher doses of flonicamid induced starvation by inhibition of phloem ingestion and higher doses of thiamethoxam induced contact toxicity rather than inhibition of feeding behavior. This study provides the basis for a more efficient use of these pesticides in Korea.

Assessing aphids potato virus Y-transmission efficiency: A new approach

In order to develop an alternative method to optimize the relative efficiency factor (REF) assessment, the efficiency of transmission of Potato virus Y (PVY) by seven aphid species was examined. In vitro micropropagated potato plantlets were used to experiment on phenotypically and genetically homogeneous material. Species-specific acquisition access period (AAP) on a PVY-infected plantlet was assessed for each aphid species using electrical penetration graph (EPG) technique.Aphid probing behaviour determined by EPG showed that Macrosiphum euphorbiae and Myzus persicae exhibited the shortest AAPs (15 and 11min, respectively) whereas Rhopalosiphum padi, Sitobion avenae, Brevicoryne brassicae and Acyrthosiphon pisum exhibited the longest ones (more than 30min). The transmission rate obtained for M. persicae (83.3%) was higher than the ones reported in the literature. REFs assessment showed that A. pisum and B. brassicae were poor efficient vectors while M. euphorbiae and S. avenae seemed to be efficient ones even though their respective REF were significantly lower than that of M. persicae. The species R. padi and A. fabae did not transmit PVY.The hypothesis assessed for M. euphorbiae and S. avenae and consisting in the compensation of a weak PVY-transmission efficiency by a higher number of vectors, was not supported. The use of this new method for REF evaluation and the need to consider aphid behaviour for such an assessment was discussed.

Effect of Lupin Cyclitols on Pea Aphid Probing Behaviour

Effect of Lupin Cyclitols on Pea Aphid Probing BehaviourThe cyclitols: D-pinitol, D-chiro-inositol are naturally present in the tissues ofLupinus angustifolius. The effect of these cyclitols on the behaviour of the pea associated clone ofAcyrthosiphon pisumduring various stages of probing was studied. The main stage of probing studied was the stylet penetration in mesphyll and vascular bundle. D-pinitol, D-chiro-inositol and their mixture were exogenously applied to peaPisum sativumexplants and the aphid probing behaviour was evaluated using the Electrical Penetration Graph technique (EPG). Feeding of peas with cyclitols at a concentration of 10 mM, caused a selective accumulation of D-pinitol and D-chiro-inositol in stems, leaf petioles, and leaf blades. In aphid bodies, both cyclitols were traced, respectively, to the host plant treatment. The new cyclitols in pea tissues did not significantly affect the total duration and frequency of aphid activities during probing in peripheral as well as vascular tissues. However, the aphid behaviour on cyclitol-treated plants as compared to their behaviour on the control was slightly altered. Non-probing and probing in mesophyl prevailed among aphid activities during the initial period of stylet penetration. Aphids on D-pinitol+D-chiro-inositol-treated plants reached phloem vessels relatively later than aphids on the control and D-chiro-inositol plants. There were recurrent switches between E1 (salivation) and E2 (sap ingestion) patterns in some aphids during the phloem phase on D-pinitol and D-pinitol+D-chiro-inositol - treated plants. This may reflect difficulties in the uptake of the phloem sap, and point to lupin cyclitols as being responsible, at least in part, for the rejection ofL. angustifoliusas a host plant by the pea clone ofA. pisum.

Symbiotic Bacterium Modifies Aphid Body Color

Color variation within populations of the pea aphid influences relative susceptibility to predators and parasites. We have discovered that infection with a facultative endosymbiont of the genus Rickettsiella changes the insects' body color from red to green in natural populations. Approximately 8% of pea aphids collected in Western Europe carried the Rickettsiella infection. The infection increased amounts of blue-green polycyclic quinones, whereas it had less of an effect on yellow-red carotenoid pigments. The effect of the endosymbiont on body color is expected to influence prey-predator interactions, as well as interactions with other endosymbionts.

Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance

Although several wheat genes differentially expressed during the Russian wheat aphid resistance response have recently been identified, their requirement for and specific role in resistance remain unclear. Progress in wheat-aphid interaction research is hampered by inadequate collections of mutant germplasm and difficulty in transforming hexaploid wheat. Virus-induced gene silencing (VIGS) technology is emerging as a viable reverse genetics approach in cereal crops. However, the potential of VIGS for determining aphid defence gene function in wheat has not been evaluated. We report on the use of recombinant barley stripe mosaic virus (BSMV) to target and silence a WRKY53 transcription factor and an inducible phenylalanine ammonia-lyase (PAL) gene, both predicted to contribute to aphid defence in a genetically resistant wheat line. After inoculating resistant wheat with the VIGS constructs, transcript abundance was reduced to levels similar to that observed in susceptible wheat. Notably, the level of PAL expression was also suppressed by the WKRY53 construct, suggesting that these genes operate in the same defence response network. Both knockdowns exhibited a susceptible phenotype upon aphid infestation, and aphids feeding on silenced plants exhibited a significant increase in fitness compared to aphids feeding on control plants. Altered plant phenotype and changes in aphid behaviour after silencing imply that WKRY53 and PAL play key roles in generating a successful resistance response. This study is the first report on the successful use of VIGS to investigate genes involved in wheat-insect interactions.

Soybean Cyst Nematode Effects on Soybean Aphid Preference and Performance in the Laboratory

Herbivores on plants frequently interact via shared resources. Studies that have examined performance of herbivores in the presence of other herbivores, however, have often focused on above-ground feeding guilds and relatively less research has examined interactions between below- and above-ground consumers. We examine how soybean aphid, Aphis glycines (Matsumura) an above-ground phloem-feeding herbivore, interacts with a below-ground plant parasite, soybean cyst nematode, Heterodera glycines (Ichinohe) through their shared host plant, soybean (Glycine max L). Laboratory experiments evaluated the preference of alate (flight-capable) soybean aphids toward plants either infected with soybean cyst nematode or uninfected controls in a simple choice arena. Alate soybean aphids preferred uninfected soybean over soybean cyst nematode-infected plants: 48 h after the releases of alate aphids in the center of the arena, 67% more aphids were found on control soybean compared with nematode infected plants. No-choice feeding assays were also conducted using clip cages and apterous (flight-incapable) aphids to investigate effect of soybean cyst nematode infection of soybean on aphid performance. These studies had mixed results: in one set of experiments overall aphid population growth at 7 d was not statistically different between control and soybean cyst nematode-infected plants. A different experiment using a life-table analysis found that apterous aphids feeding on soybean cyst nematode-infected plants had significantly greater finite rate of increase (λ), intrinsic rate of increase (r(m)), and net reproductive rate (R(o)) compared with aphids reared on uninfected (control) soybean plants. We conclude that the below-ground herbivore, soybean cyst nematode, primarily influences soybean aphid behavior rather than performance.

Effects of systemic potato response to wounding and jasmonate on the aphid Macrosiphum euphorbiae (Sternorryncha: Aphididae)

AbstractPlant induced responses are activated by multiple biotic and abiotic stresses, and may affect the interactions between a plant and phytophagous insects. The objective of this work was to evaluate the effects of different stresses inflicted to potato plants (Solanum tuberosum) on the potato aphid (Macrosiphum euphorbiae). Abiotic wounding, biotic wounding by Leptinotarsa decemlineata and treatment with volatile methyl jasmonate (MeJA) were evaluated with regard to the orientation behaviour, the feeding behaviour and the development of the potato aphids. Dual‐choice olfactometry showed that plants treated with MeJA lost their attractiveness for the potato aphids, while both abiotic and biotic wounding did not alter the orientation of aphids. Electropenetrography revealed that the feeding behaviour of aphids was only slightly disturbed by a previous L. decemlineata wounding, while it was highly disturbed by mechanical wounding and MeJA treatment. Aphid nymph survival was reduced on mechanically wounded plants, the pre‐reproductive period was lengthened and the fecundity reduced on plants treated with MeJA. Our results bring new information about the effects of various stresses inflicted to S. tuberosum on M. euphorbiae. We showed that wounding and MeJA treatment induced an antixenosis resistance in potato plants against M. euphorbiae, which may influence aphid colonization processes.

Phloem sap intricacy and interplay with aphid feeding

Aphididae feed upon the plant sieve elements (SE), where they ingest sugars, nitrogen compounds and other nutrients. For ingestion, aphid stylets penetrate SE, and because of the high hydrostatic pressure in SE, phloem sap exudes out into the stylets. Severing stylets to sample phloem exudates (i.e. stylectomy) has been used extensively for the study of phloem contents. Alternative sampling techniques are spontaneous exudation upon wounding that only works in a few plant species, and the popular EDTA-facilitated exudation technique. These approaches have allowed fundamental advances on the understanding of phloem sap composition and sieve tube physiology, which are surveyed in this review. A more complete picture of metabolites, ions, proteins and RNAs present in phloem sap is now available, which has provided large evidence for the phloem role as a signalling network in addition to its primary role in partitioning of photo-assimilates. Thus, phloem sap sampling methods can have remarkable applications to analyse plant nutrition, physiology and defence responses. Since aphid behaviour is suspected to be affected by phloem sap quality, attempts to manipulate phloem sap content were recently undertaken based on deregulation in mutant plants of genes controlling amino acid or sugar content of phloem sap. This opens up new strategies to control aphid settlement on a plant host.

Role of leaf glandular trichomes of melon plants in deterrence of Aphis gossypii Glover

External characteristics of the leaf epidermis and their effects on behaviour of Aphis gossypii Glover were evaluated in two Cucumis melo L. genotypes, 'Bola de Oro' (aphid susceptible) and TGR-1551 (aphid resistant) in order to explore their role in the early rejection of TGR-1551 by this aphid. No differential effects of epicuticular waxes on aphid behaviour were observed. The type, distribution and number of trichomes on melon leaves were also studied. Pubescence in melon, measured as the number of non-glandular trichomes per cm(2), was not sufficient to prevent aphid settling. However, there was a high density of type I glandular trichomes on leaves of the aphid-resistant genotype. According to microscopic observations and stain testing, these trichomes store and secrete phenols and flavonoids. Free-choice tests were conducted to determine the effect of these glandular trichomes on A. gossypii preference, revealing that aphids reject leaf disks of TGR-1551 from the onset of the experiment. Additional experiments after removal of leaf type I glandular trichome exudates showed that A. gossypii preferred washed TGR-1551 leaf disks over unwashed disks, while this effect was not observed in experiments using washed and unwashed 'Bola de Oro' leaf disks. These results suggest that a high density of glandular trichomes and chemicals secreted by them deter A. gossypii and disturb aphid settling on TGR-1551.

Modification of Macrosiphum euphorbiae colonisation behaviour and reproduction on potato plants treated by mineral oil

AbstractAlthough mineral oil spray is one of the most effective ways to control the transmission of non‐persistent aphid‐borne viruses in the field, its mode of action is poorly understood. In this study, the effects of mineral oil treatment of potato plants on host selection behaviour, growth, and reproduction of potato aphids, Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae), were investigated. The effects were assessed 30 min, 1 day, and 7 days after treatment, (1) on aphid orientation behaviour by using a Y‐tube olfactometer, and (2) on aphid feeding behaviour by using the electrical penetration graph (EPG) technique. Olfactory experiments showed that the oil had a repulsive effect only 30 min after spraying. EPG experiments showed a slight modification of the aphid feeding behaviour mainly 7 days after treatment. The number of both salivation and sap ingestion events during the phloem phases were increased 7 days after treatment. In addition, irrespective of the time after treatment, xylem ingestion time was increased. Clip cage experiments were set up to assess potential effects of the oil treatment on aphid survival and population parameters. Nymphal mortality was increased on treated plants, whereas fecundity of surviving insects was enhanced. The antagonistic effects of oil treatment on aphids are discussed in a plant protection context.

Differences in defensive behaviour between host‐adapted races of the pea aphid

1. Host races, i.e. host‐adapted populations in partial reproductive isolation, have been reported in a growing number of insect herbivores including aphids. The pea aphid Acyrthosiphon pisum encompasses distinct races highly specialised on various Fabaceae plants. Races have been well documented at both the ecological and genetic level. However, little is known about possible behavioural differences between host races other than those involved in plant choice.2. The aim of this study was to determine whether pea aphid host races differ in the behavioural response to the aphid alarm pheromone that was used to simulate immediate predation risk. The behaviour of aphids towards a synthetic alarm pheromone applied in their vicinity was measured in several pea aphid clones originating from various legumes including Medicago sativa, Pisum sativum, Trifolium pratense, and Vicia faba. To control for the influence of plant traits, experiments were conducted on the preferred host plant and on the universal host plant Vicia faba.3. Host races differed in their defensive responses, with stronger behavioural responses in host races originating from M. sativa and T. pratense compared with those coming from P. sativum and V. faba. These differences in behaviour are inherent to the pea aphid host race but not dependent on the test plant.4. Our work shows that host‐plant specialisation may involve behavioural traits in addition to host choice. Possible mechanisms of how different defensive behaviours might have evolved are discussed.

Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon?

Ca2+-binding proteins in the watery saliva of Megoura viciae counteract Ca2+-dependent occlusion of sieve plates in Vicia faba and so prevent the shut-down of food supply in response to stylet penetration. The question arises whether this interaction between aphid saliva and sieve-element proteins is a universal phenomenon as inferred by the coincidence between sieve-tube occlusion and salivation. For this purpose, leaf tips were burnt in a number of plant species from four different families to induce remote sieve-plate occlusion. Resultant sieve-plate occlusion in these plant species was counteracted by an abrupt switch of aphid behaviour. Each of the seven aphid species tested interrupted its feeding behaviour and started secreting watery saliva. The protein composition of watery saliva appeared strikingly different between aphid species with less than 50% overlap. Secretion of watery saliva seems to be a universal means to suppress sieve-plate occlusion, although the protein composition of watery saliva seems to diverge between species.

Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior

The leaf surface is the contact point between plants and the environment and plays a crucial role in mediating biotic and abiotic interactions. Here, we took a phylogenetic approach to investigate the function, trade-offs, and evolution of leaf surface traits in the milkweeds (Asclepias). Across 47 species, we found trichome densities of up to 3000 trichomes cm(-2) and epicuticular wax crystals (glaucousness) on 10 species. Glaucous species had a characteristic wax composition dominated by very-long-chain aldehydes. The ancestor of the milkweeds was probably a glaucous species, from which there have been several independent origins of glabrous and pubescent types. Trichomes and wax crystals showed negatively correlated evolution, with both surface types showing an affinity for arid habitats. Pubescent and glaucous milkweeds had a higher maximum photosynthetic rate and lower stomatal density than glabrous species. Pubescent and glaucous leaf surfaces impeded settling behavior of monarch caterpillars and aphids compared with glabrous species, although surface types did not show consistent differentiation in secondary chemistry. We hypothesize that pubescence and glaucousness have evolved as alternative mechanisms with similar functions. The glaucous type, however, appears to be ancestral, lost repeatedly, and never regained; we propose that trichomes are a more evolutionarily titratable strategy.

Planter Skips and Impaired Stand Favors Potato Virus Y Spread in Potato

High incidence of virus infection in potato crops can cause stand loss, reduced yields, and undersized tubers, leading to reduced quality and downgrading or rejection of potato seed lots. Initial colonization of potato fields by aphid vectors of potato viruses is predominately concentrated on field margins. In fields with poor stands, there are gaps in the crop canopy that can be attractive to alighting aphids. Thus, occurrence of stand gaps could render ineffective any pest management tactic that exploits the colonization behavior of aphids, such as barrier crops or reflective mulches. Field studies were undertaken to determine if the occurrence of localized stand gaps in potato fields would increase potato virus Y (PVY) infections and, if so, whether there was a relationship between gap size and PVY spread. PVY infection was 13% around stand gaps of ≤0.6 m2, while PVY infection was 29% around gaps ≥0.6 m2. Our results indicate that a stand gap equivalent to a loss of three or more consecutive plants within a row favored PVY spread. Trials were conducted to compare effects of roguing (physical removal of plants), seeding with oats to reduce potato canopy/soil contrast, and insecticide applications to gaps on PVY spread. Roguing, seeding gaps with oats and insecticides did not prevent PVY spread. This research indicates that suboptimal plant stands increase PVY incidence and may be contributing to the current PVY epidemic.