Conservation biological control of rosy apple aphid, Dysaphis plantaginea (Passerini), in eastern North America

Because of the potentially serious damage rosy apple aphid, Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), can cause to apple fruit and branch development, prophylactic insecticides are often used for control. If biological control could be relied on, the amount of pesticide applied in orchards could be reduced. This study examined biological control of rosy apple aphid in eastern West Virginia and the potential for enhancement through conservation biological control, in particular, the effect of interplanting extrafloral nectar-bearing peach trees. By 20 d after first bloom, only 2% of fundatrices initially present survived to form colonies based on regression of data from 687 colonies. Exclusion studies showed that many of the early colonies were probably destroyed by predation; the major predator responsible seemed to be adult Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Mortality before apple bloom was most important in controlling rosy apple aphid population growth but by itself is not sufficiently reliable to prevent economic injury. Interplanting of extrafloral nectar-bearing trees did not increase biological control, and interplanting with 50% trees with extrafloral nectar glands reduced biological control. The number of leaf curl colonies in the 50% interplanted orchards was lower than in monoculture orchards, suggesting a preference of alate oviparae for more diverse habitats, supporting the resource concentration hypothesis but not at a level sufficient to prevent injury. Predation and parasitism after the formation of leaf curl colonies was not adequate to control rosy apple aphid populations.     

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.     

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.     

Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia,USA

Spirea aphid populations and their predators were studied on apple to identify predators of importance in controlling aphid populations. Methods included random and non-random sampling from apple orchards in West Virginia, USA, sentinel aphid colonies, laboratory feeding studies, and predator exclusion studies. Aphidoletes aphidimyza (Diptera: Cecidomyiidae), chrysopids (Neuroptera: Chrysopidae), Harmonia axyridis (Coleoptera: Coccinellidae), and Orius insidiosus (Hemiptera: Anthocoridae) were the most abundant predators associated with spirea aphid colonies on apple. Parasitoids were all but absent in the study. Abundance of all predators was density dependent with greater responses to aphid populations at the orchard scale than to tree or individual colony scales. A. aphidimyza, O. insidiosus, chrysopids, and syrphids (Diptera) had the greatest degree of density dependence on aphid populations, and spiders showed inverse density dependence. Exclusion of predators with both cages and insecticides produced significantly higher aphid populations. Because of high abundance, good synchrony with aphid populations, and high impact per individual, H. axyridis adults were the most important spirea aphid predator on apple.     

Susceptibilities of apple aphid and spirea aphid collected from apple in the Pacific Northwest to selected insecticides

Laboratory bioassays using leaf disks of apple dipped in test solutions of insecticides demonstrated that the apple aphid, Aphis pomi De Geer, and the spirea aphid, Aphis spiraecola Patch, differed significantly in susceptibility to a number of insecticides registered for control of aphids on apple (Malus spp.). Compared with A. pomi, A. spiraecola was approximately four- and three-fold less susceptible to pirimicarb and lambda-cyhalothrin, respectively, whereas there was little difference in response to dimethoate. Pymetrozine is thought to act on aphids primarily as a feeding inhibitor. Exposure of aphids to this material generated data that fit the probit model for only half the tested clones. However, the LC50 value for one clone of A. spiraecola was nearly 1,000 times higher than the value for one clone of A. pomi. Although the results from these trials did not indicate that either species had developed significant levels of resistance to the test materials, differences in LC50 levels of > 10-fold suggest insecticide tolerances and the possibility of control failures in the future. The demonstrated differences in susceptibility to insecticides between these two morphologically similar species also should be considered during the evaluation of new products for use on apple.     

Baseline susceptibilities to imidacloprid for green apple aphid and spirea aphid (Homoptera: Aphididae) collected from apple in the Pacific northwest

Susceptibilities to the neonicotinyl insecticide imidacloprid were determined for clones of apple aphid, Aphis pomi De Geer, and spirea aphid, Aphis spiraecola Patch, collected from conventional and organic apple orchards and from crab apple and wild apple in Washington state and British Columbia over a period of 6 yr. For aphids collected during 1996--1998, adults were dipped in test solutions by using the Food and Agriculture Organization protocol, and third instars and adults were reared on treated apple leaf disks. During the final 3 yr of study, bioassays involved only third instars on treated leaf material. Tests showed that A. spiraecola was significantly more tolerant to imidacloprid compared with A. pomi. Depending on the bioassay method and aphid developmental stage, average LC50 values for A. spiraecola were 4.4 -5.7 times higher than those for A. pomi established under the same test conditions. Clones of both species from Washington were marginally more tolerant to imidacloprid than clones from British Columbia, but the differences were generally not significant. Average measures of susceptibility for clones from organic orchards or unsprayed trees also did not differ from those for clones from conventional orchards, and there was no evidence for increasing LC50 values over the 6 yr of study. Differences in susceptibility to insecticides between these two anatomically similar species should be considered during the testing of new products for use on apple.     

Importance of early arrival of adult <Emphasis Type="Italic">Harmonia axyridis</Emphasis> for control of <Emphasis Type="Italic">Aphis spiraecola</Emphasis> on apple

The biological control of aphid populations may only be possible when natural enemies arrive soon after aphid colonization. This study was done to identify how quickly adult Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) need to arrive at newly established spirea aphid [Aphis spiraecola Patch (Homoptera: Aphididae)] colonies on apple (Malus domestica Borkh.) to provide population control. A total of 100 newly established spirea aphid colonies were caged in an experimental apple orchard in West Virginia, USA. A single adult H. axyridis was added to each of ten caged colonies at day 0, 5, 10, 15 and 20 days after caging. An additional ten caged colonies were opened for exposure to natural levels of predation at each of the treatment intervals as a control. The single H. axyridis eliminated the aphid colonies significantly more quickly than natural predation for up to ten days after colony establishment. The probability of an aphid colony producing alates was significantly lower in the presence of a single H. axyridis adult than when exposed to natural predation for the first ten days. Adult H. axyridis beetles are capable of completely controlling individual spirea aphid colonies on apple only if they are abundant enough to find colonies within one week of colony establishment.     

Resistance of apple cultivars to Dysaphis plantaginea (Hemiptera: Aphididae): role of tree phenology in infestation avoidance

To test the importance of flowering phenology in damage caused to apple cultivars by rosy apple aphid, Dysaphis plantaginea (Passerini) (Hemiptera: Aphididae), susceptibility of 16 cultivars was compared in greenhouse conditions after infestation with aptera and in the field after natural tree colonization. Flowering phenology was recorded in the field for all the cultivars. In both greenhouse and field trials, there were differences among cultivars with respect to aphid infestation and damage. However, damage in the greenhouse and field was not significantly correlated. Flowering phenology was also different among cultivars. Flowering order among cultivars was significantly negatively correlated with aphid infestation and damage in field, i.e., early leafing cultivars showed higher infestation and damage than late-leafing cultivars. If egg hatching occurs before bud bursting, neonate larvae will suffer a high mortality because they cannot feed on these late cultivars. A later recolonization of these trees is hampered because (1) winged aphids cannot live on apple but only on the secondary host, (2) apterous forms have a limited dispersal capability, and (3) aphid predators progressively increase in the orchard. Therefore, synchronization between egg hatching and bud bursting is of critical importance in the success or failure of infestation.     

Effects of autumn kaolin treatments on the rosy apple aphid, Dysaphis plantaginea (Pass.) and possible modes of action

Abstract:  Autumn applications of the repellent processed-kaolin particle film (Surround® WP) might be an alternative to the insecticides commonly used in spring to control the rosy apple aphid, Dysaphis plantaginea (Pass.) (Hom., Aphididae). To assess the mode of action and the impact of kaolin on autumn forms of D. plantaginea , trials were conducted in field cages and in open-fields in autumn 2003. Choice and no-choice experiments in field cages showed that winged aphids landed in significantly lower numbers and gave birth to significantly fewer females on kaolin-treated branches compared with the untreated control. In a first open-field trial, single applications at 10 different dates and with two different concentrations of kaolin were conducted after harvest to assess the influence of the kaolin concentration on the autumn forms of D. plantaginea . No differences were found between the different concentrations and spraying dates. In a second open-field trial, single and multiple applications of kaolin were tested at different dates after harvest. Repeated applications of kaolin significantly reduced females in autumn and fundatrices in spring, whereas single kaolin treatments had no significant effect on D. plantaginea . None of the kaolin treatments reduced aphids below the economic threshold. In conclusion, kaolin showed promising results to control autumn forms of D. plantaginea. However, with a more detailed forecasting model for the autumnal flight of this aphid, treatments could be conducted more precisely and more effectively, especially in years with exceptional climatic conditions, such as in 2003.     

Laboratory and field studies supporting the development of Heringia calcarata as a candidate biological control agent for Eriosoma lanigerum in New Zealand

Studies supporting a project seeking to introduce Heringia calcarata (Loew) (Diptera: Syrphidae) to New Zealand (NZ) to supplement biological control of woolly apple aphid (WAA), Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae) are reported. Annual surveys of H. calcarata presence and abundance in a Virginia, USA apple orchard revealed a bimodal distribution, with peaks in mid-June and mid-September. In the field, female H. calcarata oviposited on sentinel apple shoots infested with WAA, providing an efficient method for egg collection and larval production. Similarly, most field-collected females readily deposited viable eggs on WAA colonies in laboratory cages, demonstrating that mated females will oviposit in captivity. Survivorship of eggs and larvae transported to NZ was good, yielding adult flies in containment in Auckland. Adult, virgin female H. calcarata reared from eggs in captivity developed mature oocytes, providing an important step toward future mating studies in containment. Oviposition and larval feeding studies examined aspects of the intraguild interactions between H. calcarata and Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae), the sole biological control agent of WAA in NZ. Field tests using paired sentinel apple shoots with a non-parasitized or parasitized WAA colony revealed that although H. calcarata deposited eggs on both parasitized and non-parasitized colonies, fewest eggs were deposited on heavily parasitized colonies. Feeding studies showed that larval H. calcarata consumed fewer mummified aphids or aphids in an earlier stage of parasitization than non-parasitized aphids.     

Seasonal coincidence between rosy apple aphid fundatrices and their parasitoids: implications for an early biological control of Dysaphis plantaginea

The potential contribution of the aphid parasitoid Ephedrus persicae Froggatt (Hymenoptera: Braconidae, Aphidiinae) in regulating stem mothers of the rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae) was investigated in culture conditions using both species' phenological emergence data in spring and host stage suitability trials. In 2003, emergence of E. persicae started on April 1st, i.e., 108.2 degree-days (base: 4.5 degrees C; start date: January 1st) later than its host on March 10th. When less than 3% of parasitoids had emerged on April 12th, more than 97% of D. plantaginea stem mothers had moulted beyond their 1st instar. The latest parasitoids left their diapause mummies in late April as the majority of fundatrices had reached the adult stage. Parasitisation trials demonstrated the suitability for E. persicae of all developmental stages of rosy apple aphid fundatrices, including mature individuals. No offspring were deposited by fundatrices parasitised as Ist-instar nymphs but later instars did produce a progeny whose size was substantially reduced compared with unparasitised individuals, and scaled against their age at the time of parasitisation. Although the temperature accumulation required for emergence in spring is reached later for E. persicae than for its host aphids, thus allowing part of the stem mother population to temporarily escape parasitisation and reach maturity, the marked reduction in fecundity of individuals parasitised even as late-instar nymphs does confer to E. persicae a non-negligible role in potentially regulating D. plantaginea.     

Three homopteran pests of citrus as prey for the convergent lady beetle: suitability and preference

The convergent lady beetle, Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinellidae), is an important predator of soft-bodied insect pests in many regions of the United States, but generally uncommon in Florida citrus. Certain citrus producers in Florida recently initiated releases of commercially available H. convergens from California against the Asian citrus psyllid Diaphorina citri Kuwayama, vector of Huanglongbing or citrus greening disease. However, there is little information on potential efficacy of this predator against the psyllid or other pests of citrus. Preference, development, and reproduction by H. convergens was evaluated on freshly collected nymphs of D. citri, brown citrus aphid Toxoptera citricida Kirkaldy, green citrus aphid Aphis spiraecola Patch, and frozen eggs of the flour moth Ephestia kuehniella Zeller. Larvae preferred D. citri over T. citricida in two-way choice tests and consumed more D. citri or A. spiraecola than T. citricida in no-choice tests. Adults consumed equal numbers of all three species in both tests. Development times of larvae at 25.5±0.05°C on A. spiraecola were longer than on the other three diets. Larval survival and pupation times did not differ among diets. Females lived longer than males irrespective of diet, and longevity of both genders was greatly increased on E. kuehniella compared with D. citri and A. spiraecola. Life table analysis indicated that H. convergens should increase on all three species, with a greater potential on psyllids than aphids. Further studies are warranted to assess establishment and persistence of this potential biological control agent in the Florida citrus environment.     

The effect of ant attendance on the success of rosy apple aphid populations, natural enemy abundance and apple damage in orchards

1 The rosy apple aphid, Dysaphis plantaginea, is the most serious pest of apple in Europe and, although conventionally controlled by insecticides, alternative management measures are being sought. Colonies of D. plantaginea are commonly attended by ants, yet the effects of this relationship have received little attention. 2 An ant exclusion study was conducted in two distant orchards within the U.K. At both sites, ants were excluded from a subset of D. plantaginea infested trees at the beginning of the season and populations were monitored. The number of natural enemies observed on trees was also recorded and, before harvest, the percentage of apples damaged by D. plantaginea calculated. 3 Overall, the exclusion of ants reduced the growth and eventual size of D. plantaginea populations. On trees accessed by ants, greater numbers of natural enemies were recorded, presumably because aphid populations were often greater on such trees. However, this increased natural enemy presence was diluted by the larger aphid populations such that individual aphids on ant‐attended trees were subjected to a lower natural enemy pressure compared with those on ant‐excluded trees. 4 At harvest, apple trees that had been accessed by ants bore a greater proportion of apples damaged by D. plantaginea. There were also differences in cultivar susceptibility to D. plantaginea damage. 5 The present study highlights the importance of the ant–D. plantaginea relationship and it ia suggested that ant manipulation, whether physically or by semiochemicals that disrupt the relationship, should be considered as a more prominent component in the development of future integrated pest management strategies.     

Evaluation of green lacewings, Chrysoperla plorabunda (Fitch) (Neurop., Chrysopidae), for augmentative release against Toxoptera citricida (Hom., Aphididae) in citrus

Larvae of the lacewing Chrysoperla plorabunda (Fitch) were evaluated in laboratory and field tests for potential to control the brown citrus aphid, Toxoptera citricida (Kirkaldy) in inundative releases. Larvae surviving to pupation consumed an average of 1676, 1297, 392, 165 and 130 1st–4th instar T. citricida nymphs and apterous adults, respectively, and the mean developmental time was 27.0, 23.0, 16.5, 13.8 and 18.3 days, respectively. The average pupation rate was 37.5%, but only 6.3% of pupae yielded adults. Developmental time and survival to pupation varied with the life stage of aphids fed to larvae, 4th instars yielding the highest survival and shortest developmental time. Development of C. plorabunda was compared on diets of T. citricida and Aphis spiraecola . Only 6.3% of larvae completed development on T. citricida , whereas 37.5% yielded adults on A. spiraecola . Larvae consumed more of the brown T. citricida than the green A. spiraecola in a choice test on a white background, but no preference was evident when aphids were offered on a black background. Two separate field trials were performed in citrus groves with T. citricida infestations in which an average of 275 and 116 C. plorabunda larvae/tree were released, respectively. The rate of T. citricida colony maturation (= survival to alate production) was very low in the first trial, and relatively high in the second trial, but did not differ between control and release trees in either trial. The most apparent cause of aphid colony mortality was predation by the coccinellids Cycloneda sanguinea L. and Harmonia axyridis Pallas. Despite acceptance of T. citricida in the laboratory, very few C. plorabunda larvae were observed feeding on aphid colonies on release trees.     

Assessment of aphid colonies by hoverflies. III Pea aphids andEpisyrphus balteatus (de Geer) (Diptera: Syrphidae)

The syrphid flyEpisyrphus balteatus (de Geer) migrating from maple trees to leguminous plants in mid-April, assesses the qualitative and quantitative value of pea aphid colonies for securing successful development of her offspring. She selects young and “promising” pea aphid colonies of small size. This generally agrees with the “buy-futures” ovipositional tactic the syrphid fly adopts when it utilizes the maple aphids. The advantage of a “buy-futures” ovipositional tactic found in many syrphid species is discussed in comparison with other aphidophagous insects.     

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.     

Effect of hunger on the allocation of time among pea plants by the larvae of an aphidophagous hover fly,Eupeodes corollae [Dipt: Syrphidae]

We observed the movement of predatory larvae of the syrphid flyEupeodes corollae (F.) (formerlyMetasyrphus corollae) among small pea plants with and without aphids. Starved larvae spent longer time than well-fed larvae on similar plants and both groups of larvae stayed longer on plants with aphids than on plants without aphids. On plants with aphids, larvae which failed to capture prey left the plant sooner than those which captured aphids. The capture of at least one aphid on a plant increased the persistence of syrphid larvae. The average rate of energy gain was higher for well-fed larvae than for starved larvae because starved larvac stayed on plants even when their rate of return was lower. When larvae that had captured aphids left plants, their rate of energy gain, tended to be lower than at any time following capture of the 2^nd, aphid. The 1^st aphid was captured in less time than similar larvae spent on plants without aphids. Time between captures of aphids by well-fed larvae was less than the time such larvae spent on plants without aphids. Among starved larvae, the intercatch intervals were similar to the time on plants without aphids. We discuss the significance of these results relative to current predator foraging theory and the efficiency ofE. corollae as a biological control agent.      

Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae

Voracity and feeding preferences of adult Coccinella septempunctata L. and Harmonia axyridis Pallas (Coleoptera: Coccinellidae, tribe Coccinellini) were evaluated in the laboratory on a common prey, the spirea aphid, Aphis citricola van der Goot (Homoptera: Aphididae), and on the twospotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae), a prey previously unrecorded for these two predators. The experiments were carried out in the laboratory on apple saplings (Malus domestica Borkhausen). Adult males and females of H. axyridis consumed significantly more mites than adults of C. septempunctata. For H. axyridis, males consumed 41.3 spider mites in 24 h and females 48.4, whereas for C. septempunctata males consumed 14.1 prey and females 15.2. The consumption of spirea aphids by the males was similar for the two species. Consumption by the females was significantly greater for H. axyridis (46.5) than for C. septempunctata (22.2). The two coccinellids showed a significant preference for A. citricola in the presence of T. urticae. This preference was more pronounced for C. septempunctata. The total number of prey consumed and the percentage of exploited biomass decreased significantly for C. septempunctata and stayed relatively constant for H. axyridis as the number of mites increased in the prey ratio. Our results suggest that T. urticae is only an alternative prey for both predators, and that H. axyridis should be more efficient than C. septempunctata in a prey assemblage with aphids and mites.     

Genome mapping of an apple scab,a powdery mildew and a woolly apple aphid resistance gene from open-pollinated Mildew Immune Selection

Apple is host to a wide range of pests and diseases, with several of these, such as apple scab, powdery mildew and woolly apple aphid, being major causes of damage in most areas around the world. Resistance breeding is an effective way of controlling pests and diseases, provided that the resistance is durable. As the gene pyramiding strategy for increasing durability requires a sufficient supply of resistance genes with different modes of action, the identification and mapping of new resistance genes is an ongoing process in breeding. In this paper, we describe the mapping of an apple scab, a powdery mildew and a woolly apple aphid gene from progeny of open-pollinated mildew immune selection. The scab resistance gene Rvi16 was identified in progeny 93.051 G07-098 and mapped to linkage group 3 of apple. The mildew and woolly aphid genes were identified in accession 93.051 G02-054. The woolly aphid resistance gene Er4 mapped to linkage group 7 to a region close to where previously the genes Sd1 and Sd2, for resistance to the rosy apple leaf-curling aphid, had been mapped. The mildew resistance gene Pl-m mapped to the same region on linkage group 11 where Pl2 had been mapped previously. Flanking markers useful for marker-assisted selection have been identified for each gene.