Primary parasitoids of red scale (Aonidiella aurantii) in Australia and a review of their introductions from Asia

We used morphological and molecular differences to confirm the identities of red scale (Aonidiella aurantii) and yellow scale (A. citrina), and their primary parasitoids, in Australia. An extension to the distribution of yellow scale was confirmed. Six primary parasitoids of red scale were identified: Aphytis chrysomphali, A. lingnanensis, A. melinus, Comperiella bifasciata, Encarsia citrina, and E. perniciosi. With the exception of A. lingnanensis, these parasitoids, and a species of Aphelinus, were detected in association with red scale during studies in citrus orchards in coastal New South Wales between 2009 and 2012. Two races of A. melinus were recorded: one from the Indian Subcontinent, the other previously only recorded in China. The studies, and reviews of historical records, led us to conclude that 4 parasitoids, A. lingnanensis, C. bifasciata, and both species of Encarsia, were present in Australia before successful or unsuccessful formal introductions between 1902 and 1970. The A. melinus race previously recorded in China may also have been present before the Indian Subcontinent race was formally introduced in 1961. We suggest the possibility that the natural distribution of some of the parasitoids may include East and Southeast Asia, and parts of Australasia. We found no reports of native armored scales being recorded on species and hybrids of Citrus introduced to Australia, and no reports of introduced armored scales being recorded on native Rutaceae, including 6 species of Citrus. However, we subsequently recorded yellow scale on Geijera parviflora, a native rutaceous tree.     

Disruption of parasitism of the California red scale (Homoptera: Diaspididae) by three ant species (Hymenoptera: Formicidae)

The relative influence of the southern fire ant, Solenopsis xyloni McCook, Argentine ant, Linepithema humile (Mayr), and native gray ant, Formica aerata (Francoeur), on parasitism of California red scale, Aonidiella aurantii Maskell, was studied in the laboratory for two parasitoids, Comperiella bifasciata Howard and Aphytis melinus DeBach. All three ant species reduced percentage parasitism by C. bifasciata and both percentage parasitism and host mutilation by A. melinus. Southern fire ant was the least disruptive and native gray ant the most disruptive. Southern fire ant removed 12% of scale from the lemons, presumably to feed on them, while the other ant species did not exhibit significant removal of scale compared to the controls. Percentage parasitism of California red scale exhibited by C. bifasciata was more than 2-fold the level exhibited by A. melinus. Percentage mutilation of California red scale, including probing and host feeding, was nearly 5-fold higher for A. melinus than C. bifasciata. Because A. melinus required a longer total host examination + oviposition period in the absence of ants than C. bifasciata and because oviposition occurs as the last act in a sequence of behaviors, disruption by the ants had a more significant negative effect on oviposition by A. melinus.     

Effect of a new insect growth regulator,RO 13-5223, on hymenopterous parasites of scale insects

The insect growth regulator, RO 13-5223, applied at concentrations up to 0.1% a.i., did not affect the normal development of immature stages of 2 hymenopterous parasites:Metaphycus bartletti Annecke & Mynhardt andAphytis holoxanthus DeBach, parasitoids ofSaissetia oleae (Olivier) andChrysomphalus aonidum (L.), respectively. Spraying citrus trees at the rate of 7.5 g. a.i./tree had no adverse effect on the activity of the following parasitoids:Aphytis chrysomphali (Mercet) andComperiella bifasciata Howard, an ecto- and endoparasite of the California red scale,Aonidiella aurantii Maskell, respectively;Aphytis hispanicus (Mercet) andProspaltella inquirenda Silvestri, an ecto- and endoparasite of the citrus chaff scale,Parlatoria pergandii Comstock, respectively.     

Effect of the California red scale Aonidiella aurantii sex pheromone on the natural parasitism by Aphytis spp. in Mediterranean citrus

Mating disruption has proved successful against California red scale (CRS), Aonidiella aurantii Maskell (Hemiptera: Diaspididae) in Mediterranean citrus. Although mating disruption does not affect negatively the parasitism by Aphytis melinus DeBach (Hymenoptera: Aphelinidae), a CRS parasitoid introduced to the Mediterranean, there is no information regarding its potential effect on the native Aphytis species. In the present study, the effect of CRS mating disruption on the field parasitism inflicted by Aphytis spp. has been assessed and compared to a mineral oil and a control treatment. In order to confirm the effectiveness of the mating disruption we also evaluated its effect on the captures of the CRS males and on fruit infestation. Moreover, the potential role of the CRS sex pheromone as kairomone for the Aphytis species was also evaluated by comparing captures of parasitoids on sticky traps with or without pheromone. Significantly lower CRS male captures and fruit damage were registered in the mating disruption respect to the control or oil treatments indicating that mating disruption was effective. In September, when compared to the control, parasitism by Aphytis spp. was significantly lower in the mating disruption and mineral oil treatments and crucially no Aphytis chrysomphali Mercet were registered in the mating disruption treatment. Finally, while the captures of both A. melinus and Aphytis lepidosaphes (Mercet) were not significantly different between traps with or without pheromone, A. chrysomphali captures were significantly higher in traps baited with CRS pheromone. These results suggest a possible kairomonal effect of the CRS pheromone on A. chrysomphali.     

Competitive displacement betweenAphytis spp. [Hym. Aphelinidae] parasites of the California red scale in cyprus

In Cyprus,Aphytis chrysomphali (Mercet) andAphytis melinus DeBach are the only significant parasites of the California red scale,Aonidiella aurantii (Maskell).A. chrysomphali, presumably native, has been virtually displaced byA. melinus from the interior dry areas of the island after the importation of the latter in 1961. Presently the former parasite dominates only in some of the coastal areas with a mild and rather humid climate.Aphytis ? coheni DeBach that initially displacedA. chrysomphali in the release areas, was replaced by the latter parasite and was occasionally found in small numbers only in one location. Traces ofAphytis ?lingnanensis Compere were also found in some locations. Two otherAphytis spp., imported from California, were released and recovered but it is too early to determine their permanent establishment and significance.     

Establishment Of Comperiella Bifasciata (Hym.: Encyrtidae) On Aonidiella Aurantii (Hom.: Diaspididae) In Cyprus

Reference is made to the introduction, rearing, colonization and establishment of Comperiella bifasciata Howard to improve the effectiveness of biological control of the California red scale,Aonidiella aurantii (Maskell), in Cyprus. The parasitoid was colonized during 1985- 89 and in 1993- 94 it was recovered in all the surveyed areas. It has been permanently established and is more abundant in orchards with microclimatic conditions characteristic of intermediate and interior areas whereAphytis melinus DeBach is the dominant red scale parasite.Aphytis chrysomphali (Mercet) prevails only in some of the coastal areas with mild and rather humid microclimates. In the surveyed orchards the overall adult relative abundance of the three main parasitoids, A. melinus, A. chrysomphali and C. bifasciata was 54.1%, 42.1%, and 3.8%, respectively.     

Biological control of arthropod pests in citrus orchards in China

China has a very long history of biological control in citrus. Hundreds years ago, predatory ants (Oecophylla smaragdina Fabricius) were used to manage pests by Chinese citrus growers. Considerable effort has been placed on the use of biological control in citrus plant landscapes during last three decades. Many scientific studies have now been published, and some additional implementations have already working. In this paper, we review the research, development and application of biological control of citrus insect pests in China. In addition, the importance of biological control for the future control of citrus insect pests is also discussed.     

Observations on circular purple scaleChrysomphalus aonidum (Linn.), and two introduced parasites in western Transvaal citrus orchards

Circular purple scale,Chrysomphalus aonidum (Linn.) is localized in its appearance in South African citrus orchards. It mainly occurs along the Natal Coast, the Western Transvaal and the Transvaal Lowveld. In the Western Transvaal its importance was highlighted by the development of biological and integrated programmes chiefly directed against red scale [Aonidiella aurantii (Mask.)]. This paper reports on an attempt at the biological control of circular purple scale in the Western Transvaal by introducingComperiella bifasciata. The eggs ofC. aonidum, at 26.7°C and 50% relative humidity, hatches within two to three days. The female has two and the male four moults. The first eggs are laid approximately 43 days after settling of the crawler.C. aonidum has 4 broods a year. C. bifasciata, circular purple scale strain, is uniparental. The adults can live for only one day without food, but from 3–22 days in the laboratory when fed on honey. The photopositive adults lay the eggs internally in female scales, male scales being seldom parasitized. The eggs hatch in 3–4 days of which a female parasite lays an average of 37. The larval stages occupy 13–15 days and the pupal stage 7 days. Superparasitism does occur in which case only one larva reaches maturity. The length of the life cycle varies in various stages ofC. aonidum, the shortest was in scales 25–35 days old. ThoughC. bifasciata was established after release in citrus orchards, it maintained itself at very low levels or disappeared in competition withAphytis holoxanthus.     

Testing intraguild predation theory in a field system: does numerical dominance shift along a gradient of productivity?

Although ecological theory exists to predict dynamics in communities with intraguild predation (IGP), few empirical tests have examined this theory. IGP theory, in particular, predicts that when two competitors interact via IGP, with increasing resource productivity: (1) the IG predator will increase in abundance as the IG prey declines, and (2) increasing dominance of the IG predator will cause resource density to increase. Here, we provide a first test of these predictions in a field community consisting of a scale insect and its two specialist parasitoids, Aphytis melinus (the IG predator) and Encarsia perniciosi (the IG prey). The shared resource, California red scale, is a pest of citrus, and its productivity varies across a threefold range among citrus cultivars. We examined both absolute and relative densities of parasitoids along this natural gradient of scale productivity in three citrus cultivars (orange, grapefruit and lemon). Although both parasitoid species were found in all three cultivars, their abundances reflected those predicted by IGP theory: the IG prey species dominated at low productivity and the IG predator dominated at high productivity. This relationship was caused by an increase in Aphytis density with productivity. In addition, the density of scale increased with the dominance of the IG predator. These results from a field system demonstrate the important dynamic outcomes for food webs with IGP.     

Effect of temperature and parasite density on three species ofAphytis (Hymenoptera: Aphelinidae), parasitising California red scale

Summary Three species ofAphytis parasites of California red scale,Aonidiella aurantii (Maskell) were each confined at different densities with approximately equal numbers of scale insects at several constant temperatures to determine the effect of these factors on progeny production and distribution and the search rate. Egg location on the host body by the parasites was unaffected by temperature or parasite density.A. melinus laid its eggs both dorsally and ventrally in equal proportions whileA. lingnanensis andA. chrysomphali laid their eggs ventrally. Progeny production byA. melinus andA. lingnanensis increased at the higher temperature; that ofA. chrysomphali did not. Unlike the other species,A. chrysomphali failed to oviposit at 32°C. Although increasing parasite density reduced progeny production in bothA. melinus andA. lingnanensis, they were able to maintain an almonst constant search rate. This was due to their ability to distribute their eggs among the hosts more regularly at the higher parasite densities. While the mechanism of this process is easy to understand forA. melinus which behaved as a gregarious parasite, it is unclear forA. lingnanensis, which is almost a solitary parasite. The progeny production and the search rate ofA. chrysomphali dropped significantly with increasing parasite density.     

Role of imidacloprid in integrated pest management of California citrus

Portions of three commercial citrus orchards were treated for 1 yr with foliar imidacloprid or for 2 yr with a systemic formulation in a replicated plot design to determine the impact of this neonicotinoid on the San Joaquin Valley California citrus integrated pest management (IPM) program. Foliar-applied imidacloprid had little effect on California red scale, Aonidiella aurantii (Maskell); cottony cushion scale, Icerya purchasi Maskell; or citrus red mite, Panonychus citri (McGregor), populations. Short-term suppression of the parasitoids Aphytis melinus DeBach and Comperiella bifasciata Howard; vedalia, Rodolia cardinalis (Mulsant); and the predacious mite Euseius tularensis (Congdon) were observed. Suppression of natural enemies allowed scales and mites to maintain higher populations in the treated areas compared with the nontreated areas. Thus, foliar imidacloprid did not exhibit control of these citrus pest species, and it disrupted biological control. Systemically applied imidacloprid suppressed California red scale and citricola scale populations 2-3 mo after treatment. Suppression of parasitoids of the California red scale also was observed. Thus, treatments of systemic imidacloprid applied in areawide management programs for invasive pests would provide a benefit of California red scale and citricola scale suppression. However, this treatment provided only single-season control of citricola scale, it was somewhat disruptive of biological control, and it did not suppress densities of either scale as low as a treatment of the organophosphate chlorpyrifos for citricola scale or the insect growth regulator pyriproxyfen for California red scale. Insecticides with longer periods of efficacy and greater IPM compatibility than imidacloprid should be used for a sustainable IPM approach in California citrus.     

Parasitic wasps attracted by the sex pheromone of their coccid host

Sticky traps baited with live virgin females of the California red scale, placed in citrus groves to capture male scales, also attracted parasitic wasps ofAphytis spp. The number of wasps captured per trap (>500) reached up to 75 % of all insects caught in some citrus groves not treated with pesticides. Laboratory experiments withAphytis melinus andA. coheni and other wasps, carried out simultaneously in two different olfactometers, showed that the two species ofAphytis were highly responsive to the sex pheromone of California female red scales.     

Effects of two insect growth regulators and a neonicotinoid on various life stages of <Emphasis Type="Italic">Aphytis melinus</Emphasis> (Hymenoptera: Aphelinidae)

The effect of two insect growth regulators and a neonicotinoid insecticide were tested on immature stages and adults of the parasitoid Aphtyis melinus DeBach (Hymenoptera: Aphelinidae), a key natural enemy of California red scale, Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae), in California. No significant effects of the insect growth regulators on survival or development to the adult stage were found when the parasitoid was treated at any of the egg, larval, or pupal stages. The broad-spectrum neonicotinoid acetamiprid also showed no significant effect on the development of A. melinus to the pupal stage, probably because immature stages of this ectoparasitoid are protected under the cover of its armored scale host. However, 48 h exposure of adults to acetamiprid residues following emergence resulted in high levels of wasp mortality. Aphytis melinus adults treated with either of the two insect growth regulators as larvae survived 48 h exposure to pesticide residues as adults and showed levels of fecundity comparable with control insects. We conclude that the two insect growth regulators are compatible with augmentative releases of A. melinus but that treatments of acetamiprid should be avoided in situations where biological control by this parasitoid is important.     

Host recognition and selection by Aphytis species: Response to California red, oleander, and cactus scale cover extracts

One or more chemicals associated with the host's cover appear to play a major role in host recognition by Aphytis species. Aphytis melinus DeBach, A. lingnanensis Compère, A. coheni DeBach and Comperiella bifasciata Howard, all parasitoids of diaspidid scale-insects, were found to respond to water extracts of California red scale covers, Aonidiella aurantii (Mask.); A. melinus and A. lingnanensis responded to water extracts of cactus scale covers, Diaspis echinocacti (Bouché); and A. chilensis Howard to water extracts of oleander scale covers, Aspidiotus nerii Bouché. A. lingnanensis responded to water extracts of cactus scale covers only if it had been reared on this scale. A. melinus also responded to ethanol extracts of California red scale covers while A. lingnanensis did not. A. melinus failed to respond to water extracts of California red scale covers after a single ovipositional experience on California red scale. Such kairomones might prove useful in screening natural enemies as potential biological control agents for specific hosts as well as in elucidating the mechanisms by which parasitoids of scale-insects differentiate among potential hosts.

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Résumé Aphytis lingnanensis, A. melinus, A. coheni et Comperiella bifasciata réagissent tous à des extraits aqueux d'Aonidiella aurantii, tandis qu'A. chiliensis réagit aux extraits aqueux d'Aspidiotus nérii. La réaction de A. coheni aux extraits aqueux d'A. aurantii confirme les écrits de Quednau et Hübsche (1964). Nous n'avons pas été capables d'observer une réaction de A. chrysomphali aux extraits aqueux d'A. aurantii. Comme nous n'avons pas essayé de traiter les boucliers avec d'autres solvants, nous ne pouvons pas affirmer l'absence de réponse de cet aphélinide aux kairomones de cette cochenille.Que A. melinus et A. lingnanensis aient été élevés sur Aspidiotus nerii ou sur Aonidiella aurantii, ils ne réagissent pas aux extraits aqueux d'A. nerii; qui est accepté comme hôte par ces deux aphélinides au laboratoire. Ces résultats suggèrent que d'autres éléments, comme la forme ou la texture, jouent aussi un rôle important dans la détermination des hôtes. A. melinus et A. lingnanensis réagissent tous deux aux extraits aqueux de boucliers de Diaspis echinocacti; cependant, après élevage sur D. echinocacti, seul A. lingnanensis réagit à l'extrait. La réaction de A. melinus à l'extrait de D. echinocacti suggère que cet aphélinide est préadapté chimiosensoriellement à déceler cette cochenille, dont la distribution est néotropicale tandis que celle de A. melinus orientale. A. melinus a été élevé à partir de D. echinocacti récoltés dans la nature. La réaction de A. lingnanensis aux extraits de D. echinocacti uniquement lorsqu'il a élévé dessus, suggère qu'un conditionnement préimaginal peut aussi jouer un rôle dans la détermination de l'hôte.

     

A ten-year study of population dynamics of citrus pests in the pesticide-reduced orchard

To determine the effectiveness of a pest management system that uses pesticides at a low level, we censused populations of seven insect pests and three plant diseases from 1980 to 1989 in a citrus orchard which was managed with a pesticide-reduced and pesticide-free protocols, in Wakayama Prefecture, Japan. In the orchard, we controlled the pests solely by spraying petroleum oil once a year from 1980 to 1985, by not spraying insecticide in 1986, and spraying only germicide in 1987. The arrowhead scale population remained much lower level at which citrus trees begin to wither when petroleum oil was sprayed, whereas it rapidly increased and began to wither trees during the years without spraying petroleum oil. The Indian wax scale population rapidly increased only during a 2-year period and then declined. Although the infection level of the sooty mold was unusually high on the trees where the density of the scale was high, this pathogen did little damage to citrus trees. The population of the red wax scale gradually increased throughout the census period but did not reach the level at which citrus trees begin to be damaged. Other pests also caused negligible damages to citrus trees. The results indicated that the pesticide-reduced pest management system which was proposed by Inoue and Ohgushi (1976, 1977) is valid for the prevention of the outbreak of the arrowhead scale, and that is has the sufficient control efficiency for the other pests in citrus orchards.     

Discovery of a CI-inducing Wolbachia and its associated fitness costs in the biological control agent Aphytis melinus DeBach (Hymenoptera: Aphelinidae)

Wolbachia is an endosymbiotic bacterium that infects a large percentage of arthropods and can affect the fitness of its host. Here we verified for the first time that the biological control agent Aphytis melinus DeBach is infected with a Wolbachia that causes complete cytoplasmic incompatibility, and conducted an insectary and field survey to determine the infection frequency. A. melinus appears to suffer fitness costs associated with infection based on measurements of longevity and fecundity. We also quantified the Wolbachia titers of A. melinus reared at different temperatures and found that, although not completely cured, increased temperature resulted in a significant reduction in the number of Wolbachia copies found in an individual wasp. Implications of our results for biological control are discussed.     

Priming Aphytis: behavioral modification of host selection by exposure to a synthetic contact kairomone

The introduced parasitoid, Aphytis melinus DeBach (Hymenoptera: Aphelinidae), utilizes a kairomone, O-caffeoyltyrosine, to recognize California red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae). Wasps used in augmentative release programs for California red scale on California citrus are reared on oleander scale, Aspidiotus nerii Bouché (Homoptera: Diaspididae), themselves reared on squash. The goals of this study were: 1) to determine if long-term rearing on oleander scale had caused A. melinus to develop a preference for oleander scale, and 2) to determine if the preference of oleander-reared A. melinus for California red scale might be enhanced by exposing them to synthetic O-caffeoyltyrosine prior to release. Wasps that were removed from their hosts as pupae and allowed to emerge as adults isolated from their hosts retained a strong preference for California red scale regardless of rearing host. This preference was reduced if wasps were allowed to emerge from oleander scale, thus acquiring early adult experience with oleander scale. The preference for California red scale was restored, however, by exposing wasps reared on oleander scale to synthetic O-caffeoyltyrosine prior to bioassay. Exposure of A. melinus reared in commercial insectaries to O-caffeoyltyrosine prior to release may be a means to improve the effectiveness of such wasps in augmentative release programs to control California red scale.     

中国南方害虫生物防治50周年回顾

综述了中国南方50年来害虫生物防治的研究与应用概况,特别是大卵（蓖麻蚕卵）繁殖赤眼蜂防治甘蔗螟虫的成功先例,为后来国内应用柞蚕卵繁殖赤眼蜂提供了宝贵经验。应用平腹小蜂防治荔枝蝽,解决了荔枝生产的主要害虫问题;引进澳洲瓢虫、孟氏隐唇瓢虫、松突圆蚧花角蚜小蜂均是我国生物防治成功的例证;以生物防治为主的水稻害虫综合防治研究坚持了20多年,从生产实践和理论方面均取得显著的成绩;在昆虫病原微生物的研究与应用方面,利用苏云金杆菌以色列变种防治蚊虫、松毛虫质多角体病毒的发现和应用、斜纹夜蛾核多角体病毒的分离以及中试和工厂化生产、昆虫病原线虫的大量繁殖与应用,取得了一批有应用价值的成果;在分子生物学研究方面,利用基因重组扩大了病原微生物的毒力与杀虫谱。总结和继承我国乃至世界上最早的以虫治虫（黄蚁防治柑桔害虫）的经验,对促进我国生物防治事业的发展具有重要意义。     

Volatile cues used by the parasitoid, Aphytis melinus, for host location: California red scale revisited

Aphytis melinus DeBach (Hymenoptera: Aphelinidae) is a biological control agent of diaspidid scale insects. The parasitoid has a narrow host range but its hosts are polyphagous. We determined the source of volatile cues the wasp uses to locate its few host species when those hosts occur on more than one host plant species. We addressed four questions in regard to the use of volatile cues in host location of California red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae): (1) Does A. melinus use volatile cues to assist in host location? (2) Are these cues innately recognized or learned? (3) Are cues produced by female California red scale, or from other sources? (4) Are the cues specific to the host or host plant? These questions were tested through the use of a Y-tube olfactometer. Female A. melinus used volatile cues to orient toward both infested and uninfested host plant material. Wasps learned these cues by associating odors from the host plant with host presence. They had no innate preferences for scale insect or host plant volatile stimuli. Contrary to previous studies, we found no evidence of orientation toward the female-produced sex pheromone of California red scale, nor to volatile cues from the attacked host stage. Wasps given experience with scale insects growing on lemon fruit subsequently oriented toward lemon and orange fruit and leaves. The scale species with which the wasp was given experience did not affect this preference. Wasps given experience with California red scale growing on squash did not orient toward infested lemon fruit. The host ranges of the parasitoid and its hosts are used to explain the adaptive value for the evolution of learned rather than fixed responses to cues used in foraging behavior.     

Biological control of insect pests in apple orchards in China

Apple is one of the most important fruits in China, and both yield and quality are greatly affected by insect pests. According to surveys, there are more than 200 species of natural enemies in apple orchards. Few, however, have been closely studied. Major natural enemies including parasitoids, predators and pathogens are briefly described in this review, especially focusing on two parasitoids of Trichogramma dendrolimi Matsumura and Aphelinus mali Haldeman, predatory mites and a pathogenic fungus of Beauveria bassiana (Balsamo) Vuillemin as case studies. Augmentation, one important strategy of biological control, supplements the natural control provided by the existing natural enemy community in apple orchards, and greatly increases their efficiency in controlling pests. Conservation biological control is also widely applied in four major apple-producing areas. Based on habitat manipulation, the ground cover planting system helps regulate the microclimate and enhance the biodiversity of apple orchards, effectively conserving the richness and diversity of beneficial insect species. Certain achievements have been made in the main biological control strategies including successful introduction of some exotic natural enemies such as A. mali and Typhlodromus occidentalis Nesbitt, augmentative production and application of biological control agents such as T. dendrolimi, B. bassiana and Bacillus thuringiensis, and further research in conservation of establishing adaptive ground cover planting patterns to local environment. Challenges, however, still exist. Biological control of insect pests in apple orchards is an important part of integrated pest management programs, requiring more research and application in China.