Selection of hibernation sites by Anthonomus pomorum: preferences and ecological consequences

The apple blossom weevil, Anthonomus pomorum (L.) (Coleoptera: Curculionidae), has a long period of aestivo-hibernation in the adult stage lasting from summer to early spring of the following year. Potential hibernation sites within an apple orchard consist of high-stem rough-bark trees or dwarf smooth-bark trees. Field release-recapture experiments in 2 consecutive years showed that 64 and 47% of the weevils remained in the vicinity of the release sites in an area of high-stem trees and dwarf trees, respectively. The dispersing weevils moved over an average distance of 5.5 m in the dwarf tree area, as compared to 3.8 m in the high-stem tree area. The prevalent direction of dispersal was along tree rows in both areas. Some weevils displayed, after release in mid-July, a directional dispersal to the adjacent forests. Others, released in the dwarf tree area, dispersed towards the area of high-stem rough-bark apple trees. Experiments simulating various hibernation sites demonstrated that the litter of dry leaves was the most preferred overwintering shelter, yielding a relatively high survival rate. Branches with rough bark ranked second, while branches with smooth bark, grass and pure soil were not favourable for overwintering. Flight tendency in newly emerged weevils of summer generation was significantly higher in June/July than in August/September. This corresponds to the dispersal behaviour in the field. The timing of spring colonisation of apple trees was similar for weevils overwintering within the orchard and for those from outside. These results suggest that modern, dwarf apple orchards offer unfavourable conditions for overwintering, but that the relatively small proportion of weevils which manage to reach the adjacent forests find optimal hibernation sites there.     

Spring colonisation of orchards by Anthonomus pomorum from adjacent forest borders

The early-season dispersal of the overwintered apple blossom weevil, Anthonomus pomorum (L.) (Coleoptera: Curculionidae), is a crucial stage in the colonisation of dwarf apple orchards adjacent to forests. We have conducted release-recapture studies with 1700 to 4000 marked weevils at two orchard sites in Switzerland over 2 years to characterise the spatial and temporal pattern of the dispersal process. The dispersal and colonisation of orchards in spring by overwintered weevils is dependent upon the prevailing temperature.An orientated dispersal from the forest border to the centre of the orchard was observed consistently, irrespective of the angle of the apple tree rows with respect to the forest border or of climatic conditions. The average dispersal distance of the weevils was 19 m. Approximately one third of the weevil population remained on the first tree encountered, the remainder of the population moved over short distances mainly along the tree rows. This dispersal pattern led to a strong edge effect with higher numbers of weevils occurring at the edges adjoining the forests as compared to the centre of orchards. The relevance of these findings to population dynamics and management of the pest is discussed.     

Plant genotype and the preference and performance of herbivores: cultivar affects apple resistance to the florivorous weevil Anthonomus pomorum

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Significance of shelter traps for spring monitoring of Anthonomus pomorum in apple orchards

The significance of the apple blossom weevil, Anthonomus pomorum L. (Coleoptera: Curculionidae), as a potential threat to apple, Malus domestica Borkh., has increased over the past two decades in many regions of Europe. The apple blossom weevil immigrates into orchards and colonises apple trees in early spring. Females deposit single eggs into closed blossom buds, which leads to capped blossoms. This study was designed to test the suitability of transparent shelter traps for the surveillance of colonisation under different population pressures, and to assess the quantitative relationship between number of weevils caught and: (1) absolute injury, expressed as number of infested buds, as well as (2) relative injury, expressed as a percentage of infested buds relative to all buds on the tree. The findings with the new shelter traps were contrasted to results from limb jarring. Numbers of weevils caught with the transparent shelter trap were positively correlated with absolute injury, as well as with relative injury across the five study sites, whereas weevil counts with limb jarring were not correlated with absolute injury, but only with relative injury. Our data validate the transparent shelter trap as a method for accurately monitoring the course of spring colonisation of A. pomorum and demonstrate its potential for predicting injury by the weevils to blossom buds. In contrast, the significance of limb jarring for monitoring both the time course of colonisation and subsequent injury is limited. The significant linear relationship between the number of weevils caught in shelter traps and the relative injury allows for predictions of potential damage before oviposition takes place, i.e., early enough for an insecticide application where necessary.     

Suitability of the maize weevil and angoumois grain moth as hosts for the parasitoidsAnisopteromalus calandrae andPteromalus cerealellae

Two parasitoids,Pteromalus cerealellae (Ashmead) andAnisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), were compared for their ability to parasitize two important internally-developing insect pests of stored maize (Zea mays L.). Parasitism byP. cerealellae was greater on Angoumois grain moth,Sitotroga cerealella (Olivier), than on maize weevil,Sitophilus zeamais Motschulsky, in no-choice experiments.Anisopteromalus calandrae parasitized more maize weevils than didP. cerealellae. The former parasitoid parasitized only a few Angoumois grain moths successfully in maize, but parasitized many in wheat if the hosts were younger than 3 weeks old. Thus, both host age and type of grain affect suitability for parasitism. The effects of parental host (species on which the female developed) and experimental host (species exposed to parasitism) on parasitism rate ofP. cerealellae were tested in a host-switching experiment. Parasitism by parasitoids reared on maize weevils was 23% lower than that of parasitoids reared on Angoumois grain moth. This effect was independent of which host the filial generation of parasitoids was tested on. However, the experimental host species had a much greater effect on parasitoid fecundity than the parental host species. Female progeny had smaller body sizes when emerging from maize weevil than from Angoumois grain moth, which may explain the parental host effect on fecundity. There was also a slight intergenerational effect of host species on parasitoid body size.     

Influence of Clavicipitaceous Endophyte Infection in Ryegrass on Development of the ParasitoidMicroctonus hyperodaeLoan (Hymenoptera: Braconidae) inListronotus bonariensis(Kuschel) (Coleoptera: Curculionidae)

Laboratory experiments were conducted to examine the effect of ryegrass infection by the endophytic fungusAcremonium loliiLatch, Christensen and Samuels onMicroctonus hyperodaeLoan, a parasitoid ofListronotus bonariensis(Kuschel). Progression of parasitoids through the larval instar stages was shown to depend on adequate nutrition of the weevil host. Compared to confinement on endophyte-free ryegrass, parasitized weevils held on nonpreferred diets comprising leaf segments from endophyte-infected ryegrass and switchgrass contained parasitoid larvae with retarded development. Similarly, development of parasitoid larvae was retarded in hosts feeding on artificial diet containing diterpenes and alkaloids ofA. loliiorigin. Several diterpenes incorporated into the diet reduced survival of the parasitoid larvae. Attack rate of parasitoids was reduced when the quality of potential host weevils was compromised by confinement on nonpreferredA. lolii-infected ryegrass or without food for 14 days.     

Early‐Season Headspace Volatiles from Apple and Their Effect on the Apple Blossom Weevil Anthonomus pomorum

Apple volatiles emitted at early phenological stages are little investigated, although they may influence behavior of early‐season pests. The apple blossom weevil Anthonomus pomorum is a herbivore pest of orchards in Europe. It colonizes apple trees in early season and oviposits into developing flower buds, often leading to economic damage. Using in situ radial diffusive sampling and thermal desorption, followed by GC/MS analysis, headspace volatiles from apple twigs with flower buds at three early phenological tree stages were identified and quantified. The volatile blend consisted of 13 compounds for the first, and increased to 15 compounds for the third phenological stage sampled. These blends included benzenoids, terpenes, and derivatives of fatty acids. A recombined synthetic blend served as the odor source in a still‐air dual‐choice olfactometer bioassay, in which individual male and female weevils were tested. Results from this behavioral test document an attraction of both sexes to odors of their host plant, suggesting that apple volatiles emitted in early season serve as olfactory cues for host location of A. pomorum in the field.     

A biological assessment of Apophua simplicipes (Hymenoptera: Ichneumonidae) as a parasitoid of the oblique banded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae)

Apophua simplicipes (Cresson) (Hymenoptera: Ichneumonidae) is a common parasitoid of the oblique banded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae) in organically managed apple orchards in the southern interior of British Columbia, Canada. The biological characteristics of a laboratory colony of A. simplicipes were studied. When held at 15 and 25°C and provided with honey water, individual females survived an average of 60.6±6.1 and 29.8±4.7 days, oviposited 196.7±50.7 and 326.6±51.3 eggs and parasitized a total of 163.4±40.4 and 229.4±35.8 hosts, respectively. Females oviposited into first through fourth instar oblique banded leafrollers, with significantly more parasitism occurring in the first two instars compared to the third and fourth instars. No parasitoid larvae survived past the first larval stage in parasitized fourth instar hosts. Apophua simplicipes did not parasitize larvae of three-lined leafroller, Pandemis limitata (Robinson) (Lepidoptera: Tortricidae) which is sympatric with oblique banded leafrollers in orchards in the southern interior of British Columbia. Female predation and host feeding from wounds on early instars of both leafroller species was observed under laboratory conditions. In addition, early instar hosts exited diet feeding sites in response to the probing activity of the ovipositing wasps. A similar escape reaction in the orchard may cause a leafroller larva to move away from its feeding site, making it more vulnerable to predation or movement off the tree. Apophua simplicipes larvae emerged from fifth and sixth instar hosts. Parasitized oblique banded leafroller hosts consumed significantly less meridic diet than unparasitized female larvae from fifth instar through to parasitoid emergence or leafroller pupation. Our laboratory results suggest that A. simplicipes may reduce field populations of oblique banded leafroller and decrease pest feeding damage.     

Differential susceptibility and suitability of domestic and wild apple species for a florivorous weevil and its parasitoids

Crop plant domestication can change plant resistance to herbivores leading to differences in pest pressure experienced by crop plants and their wild relatives. To compare resistance to herbivores between domesticated and wild fruit trees, we quantified direct resistance and indirect resistance to a pest insect, the florivorous apple blossom weevil Anthonomus pomorum (Coleoptera: Curculionidae), for the cultivated apple Malus domestica and two wild apple species, the European crab apple M. sylvestris and the exotic M. kirghisorum. We measured weevil infestation and performance (weight, sex ratio), and weevil parasitism by parasitoid wasps for different cultivars of M. domestica and for the two wild apple species. To explain weevil and parasitoid responses to different apple species, we quantified tree characteristics including nitrogen content, size of flower buds, bark roughness, tree size, tree phenology and tree position. We found significant differences in susceptibility to weevil infestation between apple species, with lowest infestation (highest apple resistance) in M. domestica and highest infestation in M. kirghisorum. The suitability of apple species also varied significantly: weevils emerging from M. sylvestris were significantly lighter than those from M. kirghisorum. Parasitism of A. pomorum by different parasitoid species was significantly higher in M. sylvestris than in M. domestica. Infestation, weevil weight and parasitism were positively related to tree characteristics: infestation to bud nitrogen content and bark roughness, weevil size to nitrogen content and bud size, and parasitism to tree height and bud density. Our study revealed marked differences between apple species in susceptibility and suitability for the pest herbivore, but also for antagonistic parasitoids. Whereas direct resistance appeared to be higher in cultivated apple, indirect resistance via parasitoids was apparently higher in wild apple trees. Our findings suggest that wild and cultivated apple trees possess different resistance traits that may be combined to optimize resistance in commercial apple cultivars.     

Strategy for orchard use of Bacillus thuringiensis while minimizing impact on Choristoneura rosaceana parasitoids

Trials were conducted to study how spring Bacillus thuringiensis Berliner subsp. kurstaki treatments on apple may be timed to maximize the survival of parasitoids of the obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lepidoptera: Tortricidae), found in the southern interior of British Columbia, Canada. Orchard collections verified that second through fourth instar obliquebanded leafrollers were found in varying proportions from pink through the petal fall stage of apple development when spring B. thuringiensis treatments are applied vs. lepidopteran pests. Laboratory‐reared second through fourth instar obliquebanded leafrollers, unparasitized and parasitized by one of three native parasitoid species, were fed untreated apple leaves or leaves treated with B. thuringiensis. The highest mortality of unparasitized obliquebanded leafrollers occurred when fourth instars were exposed to B. thuringiensis‐treated leaves; B. thuringiensis‐induced mortality in the unparasitized second and third instars was less than 50%. The consumption of B. thuringiensis‐treated leaves by host larvae significantly increased the percentage of dead host larvae in all parasitized and unparasitized treatments. However, because of the low susceptibility of this leafroller species to B. thuringiensis, relatively high numbers (38–43%) of three obliquebanded leafroller parasitoid species were able to survive the consumption of B. thuringiensis by second and third instar host larvae. Fourth instar obliquebanded leafrollers were found at the full bloom and petal fall stage of apple development in the orchard, at which time B. thuringiensis treatments are recommended for optimal leafroller control. The highest parasitoid mortality due to host mortality was recorded in Apophua simplicipes Cresson (Hymenoptera: Ichneumonidae) and Macrocentrus linearis (Nees) (Hymenoptera: Braconidae), when the hosts were treated as fourth instars. Both of these parasitoids emerge from fifth and sixth instar obliquebanded leafrollers. Bacillus thuringiensis did not have as negative an impact on Apanteles polychrosidis Viereck (Hymenoptera: Braconidae), which emerges when the host is in the fourth instar. When leafroller mortality and parasitism were combined, the B. thuringiensis treatment did not significantly increase host elimination above that of parasitism alone, except for larvae parasitized by A. simplicipes that were in the fourth instar. The consumption of B. thuringiensis by unparasitized larvae was shown to slow larval development.     

Temporal and spatial variability of rosy apple aphid Dysaphis plantaginea populations: is there a role of the alternate host plant Plantago major?

• 1 The rosy apple aphid Dysaphis plantaginea (Passerini) (Homoptera: Aphididae) is a pest of economic importance to the apple industry worldwide, particularly in organic apple orchards where no acceptable controls are available. In the Similkameen Valley of British Columbia, Canada, the rosy apple aphid population size varies widely between orchards and between years. To explain this variation, potential environmental correlates of aphid density were evaluated. The architecture of the alternate host was also evaluated for its effect on rosy apple aphid summer survival and reproduction.
• 2 The percentage of trees infested by rosy apple aphids among orchards was in the range 8–94% for trees having at least one cluster with more than ten aphids in 2007 and in the range 0–39% in 2008.
• 3 A general linear model correlating aphid densities to the environmental variables of abundance of the alternate host (plantain Plantago spp.), foliar nitrogen, tree age and planting density, and reduced by stepwise regression, indicated that foliar nitrogen and tree age explained 33% of the variation. Abundance of the summer, alternate food plant, plantain, was not related to later aphid densities on apple trees.
• 4 Plantain architecture, however, influenced aphid numbers and 25‐fold more aphids were found on low‐lying plantain leaves than on more upright leaves. Experimental manipulation of leaf angle and leaf size showed that significantly more aphids occurred on low angle, large leaves. Finally, mowing that encouraged low lying plants prior to spring aphid migration was associated with a four‐fold greater number of both winged and wingless aphids on the plantain.

     

Superparasitism and mutual interference in the egg parasitoid Anagrus delicatus (Hymenoptera: Mymaridae)

Abstract.

• 1 In nature, interference among Anagrus delicatus (Hymenoptera: Mymaridae) parasitoids reduced the per-capita number of hosts parasitized. Interference increased with parasitoid density.
• 2 Anagrus delicatus did not avoid parasitizing hosts that had recently been parasitized by conspecific wasps. Evidence indicated that this superparasitism was largely a random process, increasing with the ratio of parasitized to unparasitized hosts.
• 3 Individual parasitoid efficiency, the number of hosts killed per wasp per unit time, decreased with increasing wasp density. This occurred whether wasps searched the patch together (simultaneously) or one by one (sequentially), and was the result of an increase in time spent superparasitizing hosts at higher wasp density. This is known as indirect mutual interference.
• 4 Increasing numbers of parasitoids together on the same patch caused a significant decline in the rate and per-capita number of hosts parasitized. However, there was not a correspondent decline in searching efficiency with increasing wasp density (i.e. no direct mutual interference).
• 5 These forms of parasitoid density dependence should contribute to the stability of the host—parasitoid interaction.

     

Phenological analysis of spring colonisation of apple trees by Anthonomus pomorum

Adult apple blossom weevils, Anthonomus pomorum (L.) (Coleoptera: Curculionidae), leave their overwintering sites within and outside orchards to colonise apple trees in early spring. This study was conducted to characterize the temporal pattern of spring colonization of apple trees by overwintered weevils in relation to climatic conditions and apple bud stages, based on multiple mark-release-recapture experiments and field observations of foraging activities of weevils. The process of spring colonization of apple trees by overwintered weevils was related to thermal time totals above 0 °C. The dispersal into orchards initiated when the thermal time totals reached 161±27 (s.d.) degree-days (DD) calculated from January 1, or 117±16 DD from February 1. The daily dispersal speed of individual weevils within orchards was determined primarily by the maximum daily temperature, whereas crawling, feeding, and mating activities of weevils on apple trees were influenced by the mean evening temperature between 18:00 and 22:00 hours. On the other hand, the spring colonization of overwintered weevils was not synchronized with any specific apple bud stage, though the level of female foraging and reproductive activities on apple trees was related to apple bud stages. The overwintered weevils initiated dispersal into orchards over a wide range of bud developmental stages from little silver greenish tip B (51) to the mouse-ear stage C3 (54). These findings are discussed in relation to the ecology and pest management of this insect.     

Effects of pepper (Capsicum chinense) genotypic diversity on insect herbivores

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Can chemical cues from blossom buds influence cultivar preference in the apple blossom weevil (Anthonomus pomorum)?

The post-hibernating adults of the apple blossom weevil, Anthonomus pomorum (L.), show preferences for certain cultivars in mixed apple tree orchards. The degree of infestation of various cultivars was positively correlated with the density of flower buds at a comparable phenological stage, but the numbers of collected beetles were not linearly proportional to the bud density of different cultivars. Hence other possible factors, namely chemical ones, were investigated. Chromatographic analysis of apple tree bud emanations showed that volatiles from two different apple cultivars that show a different attractiveness to the beetles, differed in chemical composition. Several less volatile components of the bud emanation bouquet elicited antennographic responses in both male and female antennae. Four terpene hydrocarbons, namely 3-carene, perillene, caryophyllene and (E,E)--farnesene, were identified among the components that produced distinct electrophysiological responses in the antennae. These findings support a hypothesis that the adult weevils use chemical cues for olfactory discrimination during host-searching behaviour.     

Impact of spinosad on ichneumonid‐parasitized Choristoneura rosaceana larvae and subsequent parasitoid emergence

The impact of low levels of spinosad on the obliquebanded leafroller, Choristoneura rosaceana Harris (Lepidoptera: Tortricidae), and the koinobiont endoparasitoid, Apophua simplicipes Cresson (Hymenoptera: Ichneumonidae), was assessed when the parasitoid was in the larval stage within second‐ and fourth‐instar hosts. These are developmental stages that would be exposed to spring orchard treatments of the insecticide. Oral spinosad LC₅₀ levels for unparasitized obliquebanded leafroller hosts were <1% of the recommended orchard treatment levels. Apophua simplicipes survival was significantly reduced within parasitized spinosad‐treated second‐ and fourth‐instar larval hosts. Both the leafroller host and parasitoid were much more susceptible (ca. 65‐fold) to spinosad when larval hosts fed on spinosad‐treated leaf material as opposed to being treated topically. When hosts were exposed to extremely low doses of spinosad, a small percentage of parasitoids was able to survive to emerge as adults. These laboratory trials predict that applications of spinosad may reduce biological control of C. rosaceana populations by ichneumonid endoparasitoids developing within treated hosts.     

The developmental strategies and related profitability of an idiobiont ectoparasitoid Sclerodermus pupariae vary with host size

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Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus

Abstract.

• 1 The ability to use flexible decision rules can be an advantage to parasitoid females searching for patchily-distributed hosts. In a series of laboratory experiments the hypothesis that Opius dimidiatus, a solitary parasitoid of the chrysanthemum leafminer (Liriomyza trifolii), adjusts the time she allocates to searching for her larval hosts in response to both patch qualities and experiences with hosts was tested by varying such patch parameters as area, presence of host mines and density of host mines, and by allowing ovipositions and encounters with parasitized hosts.
• 2 Though leaf area was not a factor, the presence of host mines in a leaf did increase the time a female O.dimidiatus spent searching, over time spent on unmined leaves.
• 3 When host mine density was increased, females responded by increasing their search period in a density-dependent manner, suggesting a perception of patch quality.
• 4 Ovipositions in hosts caused females to reset their‘giving-up time’(GUT), or increase search intensity, by adding an amount of search time that increased with each successive oviposition. Conversely, encounters with parasitized (unsuitable) hosts incremented the GUT, but by an amount that decreased with each successive encounter.

     

Kaolin particle films suppress many apple pests, disrupt natural enemies and promote woolly apple aphid

Multiple applications of hydrophobic kaolin particle film in apple orchards suppressed numbers of blossom weevil (Anthonomus pomorum), brown leaf weevil (Phyllobius oblongus), attelabid weevil (Caenorhinus pauxillus), leafhoppers (Empoasca vitis and Zygina flammigera) and green apple aphid (Aphis pomi) colonies. The kaolin treatments reduced the apple sawfly (Hoplocampa testudinea) fruit infestation on cultivar J. Grieve, and the fruit damage caused by oyster scale (Quadraspidiotus ostreaeformis), mussel scale (Lepidosaphes ulmi), early caterpillars, leaf rolling moths (Tortricidae), fruitlet‐mining tortrix moth (Pammene rhediella) and codling moth (Cydia pomonella). There was no effect on the number of colonies of rosy leaf curling aphid (Dysaphis devecta), nor on the fruit damage caused by common earwig (Forficula auricularia) and apple sawfly on cv. G. Delicious. The level of infestation of rosy apple aphid (Dysaphis plantaginea), leaf miner moths (Phyllonorycter blancardella, Lyonetia clerkella), and agromyzid flies (Phytomyza heringiana) increased in the kaolin‐treated plots. Kaolin treatments promoted woolly apple aphid (Eriosoma lanigerum) infestation, which became severe, while it reduced the abundance of polyphagous predators like F. auricularia, predaceous Heteroptera and Coleoptera, the red velvet mite (Allothrombium fuliginosum), spiders (Araneae) and the abundance of common black ant (Lasius niger). The treatments also reduced parasitism of the apple sawfly by the ichneumonid Lathrolestes ensator. Many weeks after ending the kaolin treatments, the number of predaceous Coleoptera and especially the number of spiders remained low in the kaolin‐treated plots.     

Varying degree of physiological integration among host instars and their endoparasitoid affects stress‐induced mortality

In natural populations of insect herbivores, genetic differentiation is likely to occur due to variation in host plant utilization and selection by the local community of organisms with which they interact. In parasitoids, engaging in intimate associations with their host during immature development, local variation may exist in host quality for parasitoid development. We compared the development of a gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae), collected in The Netherlands, in three strains and three caterpillar instars (L1–L3) of its main host, Pieris brassicae L. (Lepidoptera: Pieridae). Hosts had been collected in The Netherlands and France, and were reared in the laboratory for one generation. We also used an established Dutch laboratory strain that had not been exposed to parasitoids for at least 24 generations. Parasitoid survival to adulthood was inversely correlated with host instar at parasitism. Adult parasitoid body mass was largest when hosts were parasitized as L1 and smallest when hosts were parasitized as L3, whereas egg‐to‐adult development time was quickest on L3 hosts and slowest on L1 hosts. Higher survival and faster development of C. glomerata on French L2 hosts also showed that there is variation in host‐instar‐related suitability. Many L2 and most L3 caterpillars that were parasitized exhibited signs of pathogen infection and perished within a few days of parasitism, whereas this never happened when hosts were parasitized as L1 or in non‐parasitized control caterpillars. Our results reveal that, irrespective of the host strain, L1 hosts are optimally synchronized with C. glomerata development. By contrast, the high precocious mortality of L3 larvae may be due to stress‐induced regulation by the parasitoid in order to ‘force’ its developmental program into synchrony with the developing parasitoid larvae. Our results underscore a potentially important role played by pathogens in mediating herbivore–parasitoid interactions that are host‐instar‐dependent in their expression.