Role of ants in structuring the aphid community on apple

1. The aphids Dysaphis plantaginea Passerini, Aphis spp. (Aphis pomi De Geer and Aphis spiraecola Patch), and Eriosoma lanigerum Hausmann are commonly found together in apple orchards. Ants establish a mutualistic relationship with the myrmecophilous aphids D. plantaginea and Aphis spp. but not with E. lanigerum. 2. Field surveys and one experiment manipulating the presence of ants and the aphid species were conducted to test the hypothesis that ants play a role in structuring the community of these aphids on apple. 3. Ants tended D. plantaginea and Aphis spp. but not E. lanigerum colonies. In the field, D. plantaginea performed better in the presence of ants while no effect was observed in Aphis spp. Contrarily, populations of Aphis spp. in the manipulative experiment performed better in the presence of ants while no differences were observed for D. plantaginea. Such differences between field and manipulative conditions could be related to thermal tolerance, phenology, and life cycles. In contrast, populations of E. lanigerum were reduced in the presence of ants. 4. Ants also had a significant negative effect on the abundance of natural enemies, which could partially explain the benefits to the tended aphids. However, while ants did not provide a benefit to Aphis spp. when it was reared alone, in the presence of other species ant attendance increased Aphis abundance by 256% and simultaneously reduced E. lanigerum abundance by 63%. Therefore, ants benefited Aphis by reducing competition with other aphid species, which involves a different mechanism, explaining the benefit of ant attendance. Considering all the aphid species together, ants had a net positive effect on aphid abundance, which was consequently considered harmful for the plant. 5. Our results highlighted the role that ants play in structuring apple aphid communities and give support to the observed pattern that ants can benefit tended aphids while simultaneously reducing the abundance of untended herbivores.     

Flower strips increase the control of rosy apple aphids after parasitoid releases in an apple orchard

Mass releases of two parasitoid species, Aphidius matricariae and Ephedrus cerasicola, may provide an alternative measure to pesticides to control the rosy apple aphid Dysaphis plantaginea in organic apple orchards. As an exploratory study, we tested if the presence of flower strips between apple tree rows could improve the action of three early parasitoid releases––and of other naturally present aphid enemies––on the control of aphid colonies and the number of aphids per tree. Apple trees located at various distances from parasitoid release points were monitored in plots with and without flower strips in an organic apple orchard over two years, along the season of aphid infestation (March to July). Our case study demonstrated that the presence of flowering plant mixes in the alleyways of the apple orchard reduced the presence of D. plantaginea by 33.4%, compared to plots without flower strips, at the infestation peak date. We also showed a negative effect of increasing the distance to parasitoid release points on aphid control. However, our results at the infestation peak date suggest that the presence of flower strips could marginally compensate for the detrimental effect of increasing distance to the release point, probably by improving the persistence and dispersal capacities of natural enemies. Despite high variations in aphid population dynamics between years, we conclude that combining flower strips with early parasitoid releases in apple orchards is promising for biological control of the rosy apple aphid, although the method merits to be further refined.     

Colonization of apple orchards by predators of <Emphasis Type="Italic">Dysaphis plantaginea</Emphasis>: sequential arrival,response to prey abundance and consequences for biological control

Episyrphus balteatus (DeGeer) (Diptera: Syrphidae), Adalia bipunctata (L.) (Coleoptera: Coccinellidae) and Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae) are the three most abundant natural enemies of Dysaphis plantaginea Passerini (Homoptera: Aphididae) in Asturian (NW Spain) apple orchards. They attack this aphid in sequence: E. balteatus arrived first, followed by A. bipunctata and then by A. aphidimyza. The cecidomyiids arrived too late to have a regulating effect. The syrphids laid an average of 2.3 ± 1.7 eggs per aphid colony and the coccinellids 18.4 ± 9.9 regardless of the degree of the infestation rates of the apple shoots. This value corresponds to the size of an egg batch laid by one female. Therefore, these aphid predators did not respond numerically to the abundance of the pest. The results of this study indicate that natural populations of syrphids and ladybird beetles are unable to control D. plantaginea, and therefore a more complex strategy than waiting for natural enemies is required.     

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.     

Effects of prey aphid species on the abundance of a parasitoid and two predator species in aphid colonies attended by ants on citrus

This study focused on three species of enemies, the parasitoid wasp Lysiphlebus japonicus Ashmead (Hymenoptera: Aphidiidae), the ladybird Scymnus posticalis Sicard (Coleoptera: Coccinellidae) and the predatory gall midge Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), all of which are able to exploit aphids attended by ants. I experimentally evaluated the effects of prey aphid species on the abundance of each of the three enemy species in ant‐attended aphid colonies on citrus. The aphids compared were Aphis gossypii Glover versus Aphis spiraecola Patch in late spring, and Toxoptera citricidus (Kirkaldy) versus A. spiraecola in late summer (all, Hemiptera: Aphididae). Colonies of the three aphid species were attended by the ant Pristomyrmex punctatus Smith (Hymenoptera: Formicidae). The initial number of attending ants per individual aphid did not differ significantly between the colonies of the two aphid species compared in each season. Between A. gossypii and A. spiraecola, there was no significant difference in the number of mummies formed by the parasitoid or foraging larvae of each of the two predators per aphid colony. A significant difference was detected between T. citricidus and A. spiraecola for each of the three enemy species, with a far greater number of L. japonicus mummies in T. citricidus colonies and distinctly more larvae of each of the two predators in A. spiraecola colonies. Thus, the abundance of each of the three enemy species in ant‐attended aphid colonies was significantly influenced by the species of the prey aphids, with the three enemies showing different responses to the three aphid species.     

Effects of augmentative releases of eggs and larvae of the ladybird beetle, Adalia bipunctata, on the abundance of the rosy apple aphid, Dysaphis plantaginea, in organic apple orchards

The impact of augmentative releases of larvae and eggs of the indigenous ladybird beetle Adalia bipunctata (L.) (Coleoptera: Coccinellidae) against the rosy apple aphid Dysaphis plantaginea Pass. (Homoptera: Aphididae), a major pest insect on apple trees, was assessed in field experiments in Switzerland, during 1997. In a first experiment, eggs and larvae were released on 3-year old apple trees infested with five aphids at four different predator-prey ratios (0:5, 1:5, 1:1, 5:1). In a second experiment, eggs and larvae were released at a predator-prey ratio of 5:1 on branches of apple trees naturally infested with aphids. In both experiments, the interaction with ants was taken into account and the releases were done at two different times in spring. The results showed that an augmentative release of larvae significantly prevented the build-up of colonies of D. plantaginea. Significant reductions in aphid numbers were recorded at the two highest predator-prey ratios, 1:1 and 5:1. Larvae were efficient just before flowering of apple trees at a time when growers normally have to spray their trees. On trees where ants were present the larvae of A. bipunctata were significantly less efficient. Effects of eggs of A. bipunctata, however, were less reliable. At the first date of release (5 April), they did not hatch, probably as a consequence of bad weather conditions.     

The potential of three native insect predators to control the rosy apple aphid, Dysaphis plantaginea

The potential of three aphidophagous predators, Adalia bipunctata, Aphidoletes aphidimyza, and Episyrphus balteatus to control the rosy apple aphid, Dysaphis plantaginea Pass., a major pest on apple in Europe, was assessed by means of laboratory and field cage experiments in Northern Switzerland. Under laboratory conditions, all three predators efficiently preyed upon D. plantaginea on apple seedlings. The searching success of larvae of A. bipunctata for individual aphids was not dependent on the size of branches of apple trees varying in leaf surface area from 150 cm² to 960 cm². Fifty and 70% of individual aphids were found and killed 6 hours and 48 hours, respectively, after release of single second instar larva of A. bipunctata. In a first field cage experiment in 1996, A. bipunctata, and to a lesser extent E. balteatus, proved to be effective and consistent predators of D. plantaginea during spring conditions, being little affected by cool temperatures and wet weather. In a subsequent field cage experiment in 1997, larvae of A. bipunctata and E. balteatus were released singly and in combination on aphid infested apple seedlings to study interactions between these two promising control agents. Both species had a significant negative effect on aphid population increase. The two species did not significantly interact and thus, their joint effect is best explained by an additive model. Combined releases of the two predator species reduced aphid densities to 5% of the control. This indicates the potential for augmentative releases of these native aphid predators to control D. plantaginea.     

The induction of leaf-roll galls by the apple aphids Dysaphis devecta and D. plantaginea

Dysaphis devecta causes the leaves of its host plant to roll laterally whereas D. plantaginea causes them to roll longitudinally. Both species of aphid are phloem feeders. D. devecta prefers to feed on the smaller veins in the lamina whereas D.plantaginea chooses the midrib. However, groups of D. devecta or D. plantaginea confined to the stem of an apple seedling induced young leaves several centimetres away to develop leaf rolls characteristic of each species. A single larva of D. devecta or D. plantaginea can induce a leaf-roll or a stem-bend on an apple seedling within 24 h. It is suggested that characteristic abnormalities in leaves attacked by D. devecta and D. plantaginea are caused by specific substances in the saliva of each aphid.     

Influence of the margin vegetation on the conservation of aphid biological control in apple orchards

The influence of three margin strip treatments (wildflower strips, grass strips and spontaneous vegetation) adjacent to apple orchards on the biological control of Dysaphis plantaginea Passerini (Hemiptera: Aphididae) was compared during two consecutive years. The wildflower strips provided the highest amount of floral resources. Within the margin strips, hoverflies responded positively to higher resource provisioning whereas ladybird abundance did not differ between strip treatments. Within the orchards, the presence of parasitoids, hoverflies, and ladybirds in aphid colonies and the predation of sentinel aphids were not significantly affected by the adjacent strip treatments. The number of natural enemies observed in aphid colonies was mainly driven by aphid number. Aphid numbers were higher close to the margin strips suggesting that aphid colonization from orchard edges may counteract the positive effect of wildflower strips on natural enemy abundance and on a reduction of aphid infestation. The results confirm the positive influence of floral resource provisioning by wildflower strips on the conservation of aphid natural enemies, but also suggest that effects of wildflower strips on aphid regulation inside orchards are not very strong compared with spontaneous vegetation naturally occurring in the margins.     

Isolation of microsatellite markers from the rosy apple aphid Dysaphis plantaginea

We report the development of five polymorphic microsatellite loci from the aphid Dysaphis plantaginea, a serious pest on apple. Using a multimotif enrichment protocol, we have isolated loci that are proving to be valuable tools for studying aphid movement at both between‐county and within‐orchard scales.     

Defence variation within a guild of aphid-tending ants explains aphid population growth

• Mutualism studies often focus on the service provided by single species, while variation in benefits provided by multiple partners is less understood. Ant-aphid food-for-protection mutualisms are suitable to study the implications of intra-guild service variation because they often involve several ant species with varying levels of aggressiveness.
• We studied an aphid species and its associated ant guild to address whether intra-guild defence variation against aphid natural enemies explains aphid performance on plants (thistles). We surveyed plants with natural abundances of aphids associated with different ant species and estimated aphid population growth. We conducted confrontation experiments between ant species and aphid natural enemies (ladybugs and hoverfly larvae). In plants patrolled by the most aggressive ant species, we determined the ant's probability of expelling aphid natural enemies and tested whether ant exclusion affects the abundance of aphids and their natural enemies.
• The ant Dorymyrmex tener was the most abundant and frequent species on plants and the most aggressive against aphid natural enemies. Aphid populations grew faster on plants patrolled by D. tener compared to plants patrolled by Camponotus distinguendus or D. richteri. Field experiments confirmed that D. tener effectively expels aphid natural enemies from plants. When D. tener was excluded, the density of aphids decreased, while the abundance of aphid natural enemies increased.
• The disruption of aphid predation by aggressive and numerically dominant ant species is a determinant of aphid population dynamics. This study illustrates the importance of considering intra-guild service variation to better understand multi-partner mutualisms.

     

QTL analysis for aphid resistance and growth traits in apple

The rosy apple aphid (Dysaphis plantaginea), the leaf-curling aphid (Dysaphis cf. devecta) and the green apple aphid (Aphis pomi) are widespread pest insects that reduce growth of leaves, fruits and shoots in apple (Malus × domestica). Aphid control in apple orchards is generally achieved by insecticides, but alternative management options like growing resistant cultivars are needed for a more sustainable integrated pest management (IPM). A linkage map available for a segregating F₁-cross of the apple cultivars ‘Fiesta’ and ‘Discovery’ was used to investigate the genetic basis of resistance to aphids. Aphid infestation and plant growth characteristics were repeatedly assessed for the same 160 apple genotypes in three different environments and 2 consecutive years. We identified amplified fragment length polymorphism (AFLP) markers linked to quantitative trait loci (QTLs) for resistance to D. plantaginea (‘Fiesta’ linkage group 17, locus 57.7, marker E33M35–0269; heritability: 28.3%), and to D. cf. devecta (‘Fiesta’ linkage group 7, locus 4.5, marker E32M39–0195; heritability: 50.2%). Interactions between aphid species, differences in climatic conditions and the spatial distribution of aphid infestation were identified as possible factors impeding the detection of QTLs. A pedigree analysis of simple sequence repeat (SSR) marker alleles closely associated with the QTL markers revealed the presence of the alleles in other apple cultivars with reported aphid resistance (‘Wagener’, ‘Cox’s Orange Pippin’), highlighting the genetic basis and also the potential for gene pyramiding of aphid resistance in apple. Finally, significant QTLs for shoot length and stem diameter were identified, while there was no relationship between aphid resistance and plant trait QTLs. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Ant attendance of the cotton aphid is beneficial for okra plants: deciphering multitrophic interactions

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Do weaver ants affect arthropod diversity and the natural‐enemy‐to‐pest ratio in horticultural systems?

High biodiversity is an important component of sustainable agricultural systems, and previous studies have found that increases in the diversity of the natural enemies of pests are associated with decreases in pest populations. Weaver ants are well known for their highly territorial and aggressive behaviour and for their control efficiency of many insect pests in tropical crop trees. Because of this, the ants have been used as a key component in integrated pest management (IPM) programmes for tropical crop trees. In implementing the IPM programmes, we received a number of enquiries related to whether weaver ants have negative effects on arthropod diversity and other natural enemies in orchard systems due to their aggressive behaviour. To answer these questions, we regularly sampled canopy arthropods in cashew and mango orchards in the Northern Territory of Australia in 1996, 2002 and 2003. We sampled, using a vacuum sampler, orchards with and without weaver ants. Cashew and mango plots with abundant weaver ants had similar or higher canopy arthropod and natural enemy diversity and similar ratios of natural enemies to insect pests, compared with plot where the weaver ant was absent. The study also showed that the application of insecticides reduced arthropod diversity and the ratio of natural enemies to insect pests in a mango orchard. However, insecticide spray did not affect natural enemy diversity and abundance, which may be related to a high immigration rate of natural enemies in small plots surrounded by areas that were not sprayed.     

Coccinellid immigration to infested host patches influences suppression of Aphis glycines in soybean

Generalist natural enemies may be well adapted to annual crop systems in which pests and natural enemies re-colonize fields each year. In addition, for patchily-distributed pests, a natural enemy must disperse within a crop field to arrive at infested host patches. As they typically have longer generation times than their prey, theory suggests that generalist natural enemies need high immigration rates to and within fields to effectively suppress pest populations. The soybean aphid, Aphis glycines Matsumura, is a pest of an annual crop and is predominantly controlled by coccinellids. To test if rates of coccinellid arrival at aphid-infested patches are crucial for soybean aphid control, we experimentally varied coccinellid immigration to 1 m² soybean patches using selective barriers and measured effects on A. glycines populations. In a year with low ambient aphid pressure, naturally-occurring levels of coccinellid immigration to host patches were sufficient to suppress aphid populations, while decreasing coccinellid immigration rates resulted in large increases in soybean aphid populations within infested patches. Activity of other predators was low in this year, suggesting that most of the differences in aphid population growth were due to changes in coccinellid immigration. Alternatively, in a year in which alate aphids continually colonized plots, aphid suppression was incomplete and increased activity of other predatory taxa contributed to adult coccinellid predation of A. glycines. Our results suggest that in a system in which natural enemy populations cannot track pest populations through reproduction, immigration of natural enemies to infested patches can compensate and result in pest control.     

The aphid-tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons

Some aphid species are attended by ants, which protect aphids against enemies, but ants sometimes prey on the aphids they are attending depending on the resource conditions. A previous study indicated that the ant Lasius niger preys less on the aphid individuals that experienced ant attendance than on those that did not. This observation leads to the hypothesis that ants transfer some substances to the aphids they attend and selectively prey on the aphids without the substances. In this study, we focus on cuticular hydrocarbons (CHCs), which are used by ants as nestmate recognition substances, and test whether ants discriminate the aphids on the basis of CHCs. We confirmed that the ant Lasius fuji preyed less on the aphids that were attended by their nestmates than those that were not attended. Glass dummies treated with CHCs from attended aphids were attacked less by ants than those treated with CHCs from non-attended aphids. The CHC profiles of ant attended aphids resembled those of the ants, suggesting that ants’ CHCs are transferred to the aphids’ body surface through ant attendance. These results support the hypothesis that ants “mark” their attended aphids with their CHCs and the CHCs reduce ant predation intensity.     

Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica

The use of crop varieties resistant or tolerant to insect pests or other stress factors is one approach in non‐chemical crop‐protection. Knowledge of the biochemical and molecular background of insect–plant interactions is a prerequisite for optimizing breeding for resistance. However, the resistance genes involved in plant–aphid interactions have so far only been identified and characterized in very few plant species. Our work aims to elucidate the molecular and biochemical mechanisms involved in resistance of apple trees, Malus domestica L. (Rosaceae), against its primary aphid pest, the rosy apple aphid, Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), which is considered a serious economic pest of apple. Gene expression in both resistant and susceptible apple cultivars after infestation with rosy apple aphids was investigated by employing the cDNA‐AFLP method (cDNA–Amplified Fragment Length Polymorphism). From approximately 12 500 cDNA fragments detected on polyacrylamide gels, 21 bands were apparently up‐ or down‐regulated only in the resistant cultivar ‘Florina’ after aphid infestation compared to the susceptible cultivar ‘Topaz’ and/or mechanically wounded or non‐infested leaves. These fragments were cloned, sequenced, and the pattern of gene expression for six fragments was subsequently verified by virtual Northern blots. Sequence comparisons of these fragments to GenBank accessions revealed homologies to already known genes, most of them isolated from Arabidopsis thaliana L. Among them, a putative RNase‐L‐inhibitor‐like protein, a pectinacetylesterase, an inositol‐phosphatase‐like protein, a precursor of the large chain of the ribulose‐1,5‐biphosphate‐carboxylase, and defence‐related genes such as a vacuolar H(+)‐ATPase subunit‐like protein and an ADP‐ribosylating enzyme were identified. The results are discussed in relation to a putative role of these genes in conferring aphid resistance in apple trees.     

Principles of formation of the environment friendly program of management of arthropod pests and their enemies in an apple orchard agroecosystem in the North Caucasus

Ecological inefficiency of conventional IPM programs for apple orchard protection in the North Caucasus results from arbitrary use of compounds producing opposite ecological effects, i.e., broad-spectrum chemical insecticides after environment-friendly selective ones, which destroys the apple orchard agroecosystem. The investigation was aimed at developing an effective and ecologically acceptable program with alternation of environment-friendly compounds which act along the same vector to preserve the populations of natural enemies of the pests and thus to stabilize the apple orchard agroecosystem, i.e., create an ecological type of orchard. In this kind of orchards, broad-spectrum chemical pesticides are prohibited whereas selective biological compounds (including synthetic ones) and methods are welcomed. The test runs of the resulting pest and enemy management (PEM) programs based both on bioregulators (Insegar, Match, Dimilin) and bio-insecticides (Phytoverm™, Lepidocid™, etc.) in 2007 and 2009 demonstrated their high efficiency: the apple fruit damage by codling moth was 1.2% and 0.3%, respectively. The test of sticky bands fixed on apple tree trunks to prevent ants from getting to the crowns showed a significant increase in the abundance of predaceous bugs which sharply reduced the green apple aphid population.     

Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards

Abstract 1. The Argentine ant, Linepithema humile, tends honeydew‐excreting homopterans and can disrupt the activity of their natural enemies. This mutualism is often cited for increases in homopteran densities; however, the ant’s impact on natural enemies may be only one of several effects of ant tending that alters insect densities. To test for the variable impacts of ants, mealybug and natural enemy densities were monitored on ant‐tended and ant‐excluded vines in two California vineyard regions. 2. Ant tending increased densities of the obscure mealybug, Pseudococcus viburni, and lowered densities of its encyrtid parasitoids Pseudaphycus flavidulus and Leptomastix epona. Differences in parasitoid recovery rates suggest that P. flavidulus was better able to forage on ant‐tended vines than L. epona. 3. Densities of a coccinellid predator, Cryptolaemus montrouzieri, were higher on ant‐tended vines, where there were more mealybugs. Together with behavioural observations, the results showed that this predator can forage in patches of ant‐tended mealybugs, and that it effectively mimics mealybugs to avoid disturbance by ants. 4. Ant tending increased densities of the grape mealybug, Pseudococcus maritimus, by increasing the number of surviving first‐instar mealybugs. Parasitoids were nearly absent from the vineyard infested with P. maritimus. Therefore, ants improved either mealybug habitat or fitness. 5. There was no difference in mealybug distribution or seasonal development patterns on ant‐tended and ant‐excluded vines, indicating that ants did not move mealybugs to better feeding locations or create a spatial refuge from natural enemies. 6. Results showed that while Argentine ants were clearly associated with increased mealybug densities, it is not a simple matter of disrupting natural enemies. Instead, ant tending includes benefits independent of the effect on natural enemies. Moreover, the effects on different natural enemy species varied, as some species thrive in the presence of ants.     

In-field production of parasitoids of Dysaphis plantaginea by using the rowan aphid Dysaphis sorbi as substitute host

A system was developed to provide the parasitic wasp Ephedrus persicae Froggatt (Hymenoptera: Braconidae: Aphidiinae), which attacks the rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), with the alternative host Dysaphis sorbi Kaltenbach (Homoptera: Aphididae) in apple orchards. Rowan trees (Sorbus aucuparia L.) arranged along the side of an unsprayed orchard were artificially infested in late February 2002 with eggs of D. sorbi. Colonies of D. sorbi successfully developed from the introduced eggs and persisted on several trees until the end of June. The only primary parasitoid species emerging from a sample of mummified aphids collected in spring from the infested rowan trees was the braconid wasp species E. persicae. In a host-switching experiment, nymphs of D. plantaginea proved suitable for female parasitoids originating from mummified D. sorbi. A series of mummies collected from the rowan trees in early summer contained diapausing parasitoids and hyperparasitoids that only hatched in April of the following spring. These observations suggest the possibility of establishing a local population of E. persicae in apple orchards, so that D. plantaginea can be readily attacked by diapause-emerging parasitoids in early spring.