Brood size, sex ratio and egg load of Metaphycus lounsburyi (Hymenoptera: Encyrtidae) when parasitizing adult females of black scale Saissetia oleae (Hemiptera: Coccidae) in the field

Black scale Saissetia oleae (Olivier) (Hemiptera: Coccidae) is a widespread olive pest in California and Europe. Metaphycus lounsburyi (Howard) (Hymenoptera: Encyrtidae) is often one of its main parasitoids. Augmentative releases of M. lounsburyi have been proposed in those areas in which biological control is ineffective. In this paper, we study the relationship between black scale and M. lounsburyi in the field. According to our data, M. lounsburyi parasitizes mainly ovipositing females of black scale. Parasitism rates of ovipositing females reach high levels. In those scales, M. lounsburyi develops as a gregarious parasitoid, with an average of 13 and a maximum of 40 parasitoids developing per scale. The secondary sex ratio is female biased (proportion of males = 0.13) and appears to be brood size dependent. Metaphycus lounsburyi eggs are encyrtiform; however, its egg load is much higher than other Metaphycus that also parasitize black scale. The implications of these results on the behavioral ecology of M. lounsburyi and its use in biological control of black scale are discussed.     

A survey of black scale,Saissetia oleae [Hom.: Coccidae] parasitoids [Hym.: Chalcidoidea] in southern California

A survey of black scaleSaissetia oleae (Olivier) parasitoids present in southern California was conducted between September 1987 and September 1989. From 308 collections of black scale-infested citrus, olive, and oleander twigs from 19 sites in southern California, 1,610 specimens were collected. Nine primary and six secondary parasitoid species were identified. Four primary species were abundant in southern California:Metaphycus bartletti Annecke & Mynhardt,M. helvolus (Compere),Scutellista caerulea (Fonscolombe) (=S. cyanea Motschulsky), andDiversinervus elegans Silvestri. The most common secondary parasitoids wereMarietta mexicana (Howard),Cheiloneurus noxius Compere, andTetrastichus minutus (Howard). In the coastal region of southern California,M. bartletti was the most abundant parasitoid, followed in order byD. elegans, S. Caerulea, andM. helvolus. In the intermediate and interior regions,M. helvolus was most abundant.D. elegans was second most abundant in the intermediate region, but was rare in the interior region.M. bartletti was second in abundance in the interior region and third in the intermediate region.      

The role of augmentative releases of indigenous parasitoid Metaphycus lounsburyi (Hymenoptera: encyrtidae) in enhancing the biological control of Saissetia oleae (Homoptera: coccidae) on olive in Egypt

The Mediterranean black scale, Saissetia oleae (Olivier) (Homoptera: Coccidae) is the most important pest of olive in Egypt. Indigenous parasitoid Metaphycus lounsburyi (Howard) (Hymenoptera: Encyrtidae) from different localities in Egypt, were manipulated, reared and mass produced for classical biological control in Egypt, more than 193130 parasitoids were released. Several releases were made between May 1999 to April 2001. Increases of the parasitism from 17.4 to 42.0 and from 6.4 to 19.2 during the first year (1999–2000) and the second year (2000–2001), respectively in the Northern Coast. This parasitoid became established in some of the release sites in El-Arish and Matruh Governorates.     

Parasitoids as a bioagent to eliminate the insecticides to control the main pests-infested economic crops

Hemipterous insects are one of the important pests that attack different economic plants. A study was conducted to evaluate the biological control potential of these pests by augmentation with parasitoids, such as Microterys flavus (Howard), Metaphycus lounsburyi Howard (Encyrtidae), Encarsia sophia (Girault and Dodd), Coccophagus scutellaris (Dalman), Aphytis melinus DeBach (Aphelinidae) and Aphidius ervi Haliday (Braconidae). All the species were mass reared and monthly releases were made in fields of citrus, olive, tomato, sugar cane, mango and squash during each of 11 consecutive years (1999–2009). About 5,830,000 individuals of M. flavus, M. lounsburyi, E. sophia, C. scutellaris, A. melinus and A. ervi were released in the fields of Gharbiya, Marsa Matrouh, Daqahlyia, Qena, Qalyubiya and Behira governorates in Egypt on citrus, olive, tomato, sugar cane, mango and squash which were naturally infested by Ceroplastes floridensis Comstock, Saissetia oleae (Olivier) (Coccidae), Bemisia tabaci (Gennadius) biotype Q (Aleyrodidae), Pulvinaria tenuivalvata (Newstead) (Coccidae), Aulacaspis tubercularis (Newstead) (Diaspididae) and Aphis craccivora Koch (Aphididae), respectively. Population of the parasitoids and parasitism increased in field plots where releases were made when compared with where no releases were made. The maximum rate of parasitism reached 61.4, 92.1, 45.7, 59, 91 and 55.2% in the field treatment where releases were made, while parasitism peaked at 8.2, 13.5, 6, 2, 16 and 17.5% where no releases were made. The populations of M. flavus, M. lounsburyi, E. sophia, C. scutellaris, A. melinus, A. ervi were significantly correlated with the populations of C. floridensis, S. oleae, B. tabaci, P. tenuivalvata, A. tubercularis and A. craccivora during the field seasons. Additional parasitism was caused by natural infestations of Metaphycus helvolus (Compere) and M. lounsburyi (Howard) (C. floridensis), Scutellista cyanea (Motschulsky) (S. oleae), Encarsia lutea (Masi) and Eretmocerus mundus (Mercet) (B. tabaci biotype Q), Encarsia citrina (Craw) (A. tubercularis) and Aphelinus demyaati Abd-Rabou (A. craccivora). These observations enhance the understanding of the usefulness of these parasitoids after augmentation in the field.     

Encapsulation of parasitoid eggs in soft scales (Homoptera: Coccidae)*

Abstract. 1. The Mediterranean black scale Saissetia oleae (Olivier) was the most suitable host for the imported Metaphycus aff. stanleyi Compere and Metaphycus helvolus (Compere) and for the local Metaphycus flavus (Howard). 2. Difficulties were encountered in the mass rearing of the introduced parasitoids, particularly M. aff. stanleyi, on the hemispherical scale Saissetia coffeae (Walker) and on the brown soft scale Coccus hesperidum L., because many of the eggs were encapsulated. 3. Although all the eggs of M.aff.stanleyi were encapsulated shortly after being deposited in S.coffeae, some larvae developed, broke out of the capsule and developed normally. 4. The incidence of parasitized scales containing only encapsulated eggs of any of the three Metaphycus species, increased with the stage of the host.     

Seasonal and Scale Size Relationships between Citricola Scale (Homoptera: Coccidae) and Its Parasitoid Complex (Hymenoptera: Chalcidoidea) on San Joaquin Valley Citrus

The phenology of citricola scale, Coccus pseudomagnoliarum (Kuwana), and its associated parasitoid complex were studied on citrus in the San Joaquin Valley of central California over the period April 1995–March 1997. A total of 10,237 parasitoid specimens of 10 species were collected. Two of these species, Marietta mexicana (Howard) and Encyrtus lecaniorum (Mayr), each recovered from individually isolated scales, represent new parasitoid records for citricola scale. A third species, Encarsia citrinus citrinus (Craw), may represent a new parasitoid record, but this requires further confirmation because a single (male) specimen was recovered from individually isolated scales. The three most dominant parasitoid species, Coccophagus lycimnia (Walker), Metaphycus helvolus (Compere), and Metaphycus luteolus (Timberlake), accounted for the majority (>97%) of the specimens recovered. In contrast to the situation on citrus in southern California, where citricola scale is under effective biological control and is very rarely seen, citricola scale on citrus in the San Joaquin Valley is reemerging as a major pest, especially in groves employing integrated pest management with minimal use of broad-spectrum insecticides. Possible reasons uncovered in this study for the lack of effective biological control of citricola scale in the San Joaquin Valley include: (i) reduced presence of Metaphycus spp. because of hyperparasitism by the heteronomous hyperparasitoid C. lycimnia; (ii) absence of alternate hosts for those species of Metaphycus present; and (iii) absence of hosts of suitable size for Metaphycus at critical times of the year. Recommendations for improving the level of biological control in the San Joaquin Valley are discussed.     

Control ofSaissetia oleae (Hom.: Coccidae) in Cyprus through establishment ofMetaphycus barletti andM. Helvolus (Hym.: Encyrtidae)

In Cyprus the black scale,Saissetia oleae (Olivier) is a pest primarily of olive,Olea europaea L., but it also attacks several other plants, among which areCitrus spp. and oleander,Nerium oleander L. The parasitoidsMetaphycus bartletti Annecke &; Mynhardt andMetaphycus helvolus (Compere) have been imported from France, massreared and permanently established in Cyprus. Following limited releases of these parasitoids, populations ofS. oleae have been reduced from outbreak levels to almost non-existence and remained at such low levels even after discontinuation of these releases.     

Sequences of sex allocation and mortality in clutches of Metaphycus parasitoids of soft scale insects and the prevalence of all‐female broods

1. In many gregarious or quasi‐gregarious parasitoids that experience local mate competition, precise sex ratios with low variance are observed. Precise sex ratios can be achieved by laying male and female eggs in non‐random sequences. 2. Developmental mortality can also alter sex ratios of emerging offspring, and subsequently influence sex ratio optima. 3. The present study investigates sex allocation by Metaphycus flavus Howard, M. luteolus Timberlake, and M. angustifrons Compere (Hymenoptera: Encyrtidae), endoparasitoids of soft scale insects, in the laboratory. 4. All three Metaphycus species had precise secondary sex ratios when parasitising brown soft scale, Coccus hesperidum, L. in the laboratory. Moreover, we documented that all three species lay fertilised (= female) eggs first followed by unfertilised (= male) eggs at the end of the oviposition bout. However, there were significant differences in sex allocation sequences among species. 5. Mortality rates of eggs allocated within an oviposition bout also varied considerably, indicating that there is a significant interspecific variation in sequence position‐specific mortality. 6. Using a stochastic Monte Carlo simulation approach, we provide evidence that the incidence of all‐female broods in these parasitoid wasps appears mainly due to developmental mortality and not due to decisions by the ovipositing female. In two species the prevalence of all‐female broods was independent of clutch size, contrary to what is expected from theory. The influence of mortality on optimal sex allocation in these parasitoids is discussed.     

Survey of brown soft scale Coccus hesperidum L. parasitoids in southern California citrus

The parasitoid complex of brown soft scale, Coccus hesperidum L., a multivoltine soft scale, was determined in southern California citrus over the period February 2004–March 2006. The survey was conducted by placing brown soft scale-infested yucca leaves in the canopy of citrus trees and subsequently rearing individually isolated parasitized scales in the laboratory. A total of 14 species parasitized brown soft scale in the field, the most abundant ones belonging to the genus Metaphycus Mercet (75%). The most abundant parasitoid species was Metaphycus angustifrons Compere (38% parasitism), and this is a new record of establishment for this species in California. Coccophagus species accounted for only 11% parasitism. There were important spatio-temporal differences across the parasitoid complex survey locations. We also found that the five most abundant encyrtid parasitoid species showed preferences for scales of different sizes. Our results have implications for biological control of citricola scale, Coccus pseudomagnoliarum (Kuwana), an important pest of citrus in the San Joaquin Valley of central California. Notably, this species is nearly absent in southern California. Brown soft scale is considered to be an alternate host for parasitoids of citricola scale, a univoltine soft scale, at times when the latter species is unavailable for parasitism.     

Behavioral responses to host foodplants of two populations of the insect parasitoid Cotesia congregata (Say)

To test the hypothesis that natural enemy populations differ in their behavioral responses to plants or to plant allelochemicals, we compared two populations of the gregarious larval endoparasitoid, Cotesia congregata (Say) (Hymenoptera: Braconidae) that differed in their historical and present exposure to tobacco. The major hosts for both populations were Manduca sexta L. and M. quinquemaculata (Haworth) (Lepidoptera: Sphingidae), but these hosts were typically encountered on tobacco by parasitoids in one population (Upper Marlboro) and on tomato by parasitoids in another population (Wye). Early in the season, Wye parasitoids preferred to oviposit in M. sexta on tomato rather than on tobacco and Upper Marlboro parasitoids showed no preference; neither population showed any preference later in the season. Neither of the strains originating from the two populations showed a landing preference for tobacco or tomato in flight chamber trials, but Upper Marlboro parasitoids searched longer on tobacco than on tomato, and Wye parasitoids searched longer on tomato. When nicotine solutions were applied to tobacco leaf, searching responses of Upper Marlboro parasitoids were enhanced by 0.001–1.0% nicotine, and searching responses of Wye parasitoids were decreased by 0.01–1.0% nicotine. We speculate that population differences in searching responses to tobacco and nicotine may explain the differential parasitism responses found early in the season.     

The establishment ofMetaphycus helvolus (Compere) [Hym. Encyrtidae] onSaissetia oleae (Bern.) [Hom. Coccidae] in olive groves in Greece

Résumé Une souche pure de l'EncyrtideMetaphycus helvolus Compere a été importée de Californie par airfret et directement relachée sur des Oliviers attaqués par la CochenilleSaissetia oleae Bern. près de Chania (Crète) en octobre 1962. En dépit du très rigoureux hiver qui suivit et, malgré les applications périodiques d'insecticides dirigées contre d'autres ravageurs, le parasite introduit est maintenant bien établi. En un an, le nombre desSaissetia fut notablement réduit dans le site du lacher originel; en 1964 et 1965, la Cochenille y était pratiquement inexistante. Une légère recrudescence de la population de Cochenille s'est manifestée en automne 1966 mais les Insectes étaient bien parasités. Fin 1966 et début 1967,M. helvolus s'était spontanément installé jusqu'à 24 km du point d'introduction et se rencontrait dans l'ensemble de la zone de Chania. L'espèce s'est probablement dispersée au-delà mais l'échantillonnage n'a pas été réalisé dans d'autres zones. L'espèce endémiqueMetaphycus flavus How. n'a pas été retrouvée en 1966–1967 dans la zone de Chania alors que ce parasite était commun auparavant. Il a été apparemment remplacé parM. helvolus.

---

---

This study was made possible by financial support from the Greek Ministry of Agriculture within the framework of a project for the control of olive pests. The contribution of the second author was made possible by his appointment as a Fulbright Research Scholar at the Benaki Phytopathological Institute, Kiphissia, Athens, Greece. Support for a portion of these studies was given by NSF Grant G-20870. The authors gratefully acknowledge the help of Mr. N. Psyllakis of the Agricultural Research Station of Chania, who made some of the recovery attempts. Especial thanks are due to Mr. Howard Lorbeer, Manager of the Fillmore Citrus Protective District Insectary, who furnished theM. helvolus for our studies.     

Status of biological control by egg parasitoids of Diaprepes abbreviatus (Coleoptera: Curculionidae) in citrus in Florida and Puerto Rico

Eggs of Diaprepes abbreviatus (L.) were routinely monitored in citrus groves at ten locations in Florida during 1997 and 1998 to study egg parasitism. One citrus location was studied in Puerto Rico. No native parasitoids were recovered from 1,337 D. abbreviatus egg masses studied in Florida citrus. In contrast, an average of 35.5% (range 12.5 to 68.8%) parasitism of egg masses was reported in Puerto Rico. The parasitoids Aprostocetus gala, Horismenus spp, and Quadrastichus haitiensis were recovered from the eggs of D. abbreviatusfstudied in Puerto Rico. The Horismenus parasitoids were suspected hyperparasitoids. Releases of the parasitoid Ceratogramma etiennei from Guadeloupe were initiated during 1998 at each of the Florida research sites. By the end of 1998, C. etiennei had been recovered from D. abbreviatus eggs at two of nine locations in Florida citrus. The parasitoid was recovered from 1 of 34 egg masses at one of these locations during the month of September and from 3 of 34 egg masses at the other location during the month of November. Whether or not C. etiennei establishes itself at one or more locations in Florida remains to be seen.     

Mass rearing and augmentative releases of the native parasitoid Chouioia cunea for biological control of the introduced fall webworm Hyphantria cunea in China

The fall webworm, Hyphantria cunea Drury, is an economically important introduced pest in China. A native pupal endoparasitoid, Chouioia cunea Yang (Hymenoptera: Eulophidae, Tetrastichinae) causes considerable mortality of H. cunea pupae in some areas of China. Alternative hosts of C. cunea were tested to find potential substitute hosts for mass rearing the parasitoid. Antheraea pernyi Guerin-Meneville (Lepidoptera: Saturniidae) was chosen as a surrogate host as a single pupa produced an average of 6552 wasps and a maximum of 11,256 per pupa. A mass-rearing technique and successful release program of this parasitoid is described. Parasitism by C. cunea in the areas where it was released averaged 67.74% and was usually over 80%. Other native parasitoids, such as Coccygomimus disparis (Viereck), C. parnasae (Viereck) (Hymenoptera: Ichneumonidae) and Exorita japonica Townes (Diptera: Tachnidae), caused the total average parasitism to exceed 90% on average, reaching a maximum of 96.28% in the release areas. These successful releases indicate that an introduced pest species can also be controlled by the mass-rearing and release of native parasitoids in the country of introduction.     

The influence of two endoparasitic wasps, <Emphasis Type="Italic">Hyposoter didymator</Emphasis> and <Emphasis Type="Italic">Chelonus inanitus</Emphasis>, on the growth and food consumption of their host larva <Emphasis Type="Italic">Spodoptera littoralis</Emphasis>

The influence of parasitism by Hyposoter didymator (Thunberg; Hymenoptera: Ichneumonidae) and Chelonus inanitus (Linnaeus) (Hymenoptera: Braconidae) on the growth and food consumption of their host Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) was studied in the laboratory. Parasitised larvae consumed significantly less artificial diet than unparasitised ones. Egg parasitisation by C. inanitus affected host larval consumption from the second day after emergence and it was significantly different from that of unparasitised ones. H. didymator, however, started to reduce larval consumption 4 days after parasitisation on the third instar host larvae. The overall reduction achieved by the larval endoparasitoid H. didymator is higher than that caused by the egg-larval endoparasitoid C. inanitus. The final body weight of a parasitised host larva by H. didymator and C. inanitus was only 6.7 and 13.0% of the maximum weight of an unparasitised sixth instar larva respectively. Moreover, parasitised larvae never reached the last instar. Results indicated that parasitised larvae might cause considerable less damage to the host plant than unparasitised ones.     

Insect natural enemies of coffee green scales [Hemiptera: Coccidae] in Kenya and their potential for biological control ofCoccus celatus andC. viridis in Papua New Guinea

Coffee green scales,Coccus celatus De Lotto andC. viridis (Green), are major pests of coffee in Papua New Guinea (PNG). Surveys for insect natural enemies of coffee green scales were conducted in Kenya to find species suitable for introduction to PNG. Natural enemy communities in Kenya were found to be diverse, particularly those located in the central highlands where 3 primary parasitoids,Metaphycus stanleyi Compere,M. baruensis Noyes andDiversinervus stramineus Compere (Encyrtidae), were dominant onC. celatus andC. alpinus De Lotto. It is suggested that these 3 parasitoids may be potential biological control agents forC. celatus. Several insect predators were found associated withC. celatus in the central highlands but most were only common in ant-free scale populations. An aphelinid primary parasitoid,Coccophagus rusti Compere, was the only natural enemy ofC. viridis located. This species, however, could be of potential as a biological control agent, especially in view of its previous use in biological control against soft scales.      

Post-release survey to assess impact and potential host range expansion by Amitus hesperidum and Encarsia perplexa, two parasitoids introduced for the biological control of the citrus blackfly, Aleurocanthus woglumi in Dominica

Four years after the release of two exotic parasitoids, Amitus hesperidum Silvestri (Hymenoptera: Platygasteridae) and Encarsia perplexa Huang and Polaszek (Hymenoptera: Aphelinidae) for the classical biological control of the citrus blackfly (CBF), Aleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae) in Dominica, a survey was conducted to assess establishment as well as potential nontarget effects especially on Aleyrodidae and other related taxa. CBF populations were low to non-existent in 50 of 51 field sites examined. At the site where CBF was encountered, both E. perplexa and A. hesperidum were present and CBF populations were declining. The two parasitoids were not among the several species collected on nontarget Aleryodidae and Hemiptera. It is concluded that E. perplexa and A. hesperidum have kept CBF populations under effective biological control in Dominica and there is no evidence of any nontarget effects on other Aleyrodidae or their natural enemies. Handling Editor: Dirk Babendreier.     

Augmentative releases of Metaphycus sp. nr flavus against citricola scale on oranges in the San Joaquin Valley of California: are early releases better than late ones?

We conducted an augmentative release trial with the encyrtid parasitoid Metaphycus sp. nr flavus (Howard) against citricola scale, Coccus pseudomagniolarum (Kuwana), in three citrus orchards in the San Joaquin Valley of California. Three parasitoid release timings (14 October-13 November, 4 January-5 February, and 26 February-16 March; hereinafter "early," "intermediate," and "late") were compared with a no-release check. Approximately 2,400 female parasitoids were released per central release tree. Late releases were associated with reduced scale survival on the release trees but no evidence of scale suppression was found on adjacent trees. Early and intermediate releases resulted in less pronounced scale suppression than late releases. Intermediate and late, but not early, releases were associated with an increase in the numbers of recovered female M. sp. nr flavus. Early releases, however, increased the numbers of recovered male Metaphycus spp. Thus, at the time of early releases, the scales may have been too small for the production of female parasitoids. A multiple regression model relating the degree of scale mortality in one orchard to the levels of recovered female Metaphycus helvolus (Compere), M. sp. nr flavus, or M. luteolus (Timberlake) (these latter two species are morphologically indistinguishable), and Coccophagus spp., suggested that the number of Coccophagus spp. females followed by M. helvolus females, were most strongly associated with scale mortality.     

Effects of host age on the performance of >Diadromus collaris, a pupal parasitoid of >Plutella xylostella

The ichneumonid >Diadromus collaris(Gravenhorst) (Hymenoptera: Ichneumonidae) is amajor solitary, pupal endoparasitoid of thediamondback moth, >Plutella xylostella(Linnaeus) (Lepidoptera: Plutellidae).Experiments to examine parasitism of the hostpupae of different ages by the parasitoid wereconducted in the laboratory. >Diadromuscollaris preferred host pupae that were in thefirst half of their pupal development. Survivalfrom larva to adult, and size and parasitizingcapacity of the resultant female adultsdecreased dramatically as host pupal ageincreased. When ovipositions were made intohost pupae that were in the last quarter oftheir development, all parasitoids died beforeadult emergence. The performance of >D.collaris, as affected by host pupal age,agrees with the simple diet theory thatpredicts female wasps should select hosts ofhigher nutritional quality for oviposition.     

Effects of temperature and host age upon the encapsulation of Metaphycus stanleyi and Metaphycus helvolus eggs by brown soft scale Coccus hesperidum

Encapsulation of eggs inserted by Metaphycus stanleyi (Hymenoptera: Encyrtidae) into the brown soft scale Coccus hesperidum (Homoptera: Coccidae) became more frequent as the host matured. This occurred with both laboratory reared and field-collected parasites. After parasitism for 24 hr at 27°C, encapsulation frequency did not differ in hosts reared at 20° or at 27°C, but significantly increased in hosts reared at 33°C. When parasitism and rearing were carried out at the same temperature, the percentage of eggs encapsulated increased from 48.7% at 27°C to 94.1% at 33°C. With M. helvolus, the percentage of eggs encapsulated was considerably higher than with M. stanleyi; e.g., 99.3 vs 48.7%, respectively, at 27°C. At 20° and 27°C, some M. helvolus development occurred in the larvae of brown soft scale but none at 33°C; the adult stages of the host encapsulated all the parasite eggs at these temperatures.     

Distribution ofGeotrichum candidum citrus race in citrus groves and non-citrus fields in Japan

The presence ofGeotrichum candidum citrus race, the citrus sour rot pathogen, was examined in soils of citrus groves and non-citrus fields of Japan. Soil samples were collected from 223 sites (118 sites in citrus groves, and 105 sites in fields cultivated with 33 species of non-citrus plants and in evergreen broad-leaved forest) in 11 main citrus-growing prefectures, and Hokkaido, a non-citrus-growing area. Of 236 soil samples from citrus groves, 95.76% containedG. candidum citrus race and 0.42% contained the non-citrus race; while of 210 samples from non-citrus fields, 62.85% and 4.76% contained the citrus race and the non-citrus race respectively. All of the citrus race isolates obtained either from citrus groves or non-citrus fields were pathogenic on lemon (Citrus limon) and satsuma mandarin (Citrus unshiu), but some of these isolates failed to infect orange (Citrus sinensis). The non-citrus races were pathogenic on ripe tomato fruit (Lycopersicon esculentum) and ripe muskmelon fruit (Cucumis melo var.reticulatus). Results indicated that citrus sour rot pathogen is widely distributed in citrus groves and non-citrus fields of diverse plant species in Japan.