Serguei V. Triapitsyn

Egg parasitoids of Homalodisca coagulata (Homoptera: Cicadellidae).

The glassy-winged sharpshooter, Homalodisca coagulata (Say), is native to the southeastern United States. It has existed in southern California since about 1990 (Sorensen & Gill 1996), and has become an economic problem as a vector of the pathogenic bacterium Xylella sp., that is the cause of leaf scorch disease in oleander. H. coagulata also feeds on citrus and many other plants. In October 1995, the mymarid wasp Gonatocerus ashmeadi Girault was reared from egg clusters of H. coagulata collected on citrus leaves in Santa Paula, California (Triapitsyn & Phillips 1996). This finding prompted us to conduct a limited survey of egg parasitoids of H. coagulata in California and also in the southeastern United States to assess the feasibility of a biological control program against this pest. Prior to this study, published information concerning natural enemies of H. coagulata was limited to the work by Turner & Pollard (1959) in Georgia. Egg masses of H. coagulata are rather conspicuous and thus easy to locate on the underside of leaves. The female leafhopper covers its eggs with a white, chalky material, which may have a bactericidal effect, and spreads this material over the eggs using the tarsi. Parasitized eggs turn black before parasitoids exit through characteristic emergence holes. To obtain parasitoids, leaves with H. coagulata egg masses were collected and held in plastic containers. Upon emergence, parasitoids were placed directly in 70% ethyl alcohol and later identified by the senior author. In California (1996-1997), parasitized H. coagulata eggs were collected on various ornamental plants on the University of California, Riverside campus. Eggs collected early in spring were not parasitized. During summer, G. ashmeadi was found in all samples from southern California and in rather large numbers (up to 80% of eggs were parasitized in Riverside in the July 1997 samples). Three other species of Gonatocerus-G. capitatus Gahan, G. incomptus Huber and G. novifasciatus Giraultwere collected in very small numbers, and only early in spring in Fillmore by University of California Cooperative Extension (Ventura Co.) researchers. Gonatocerus capitatus and G. novifasciatus have not been previously reared from eggs of H. coagulata whereas G. incomptus was a known parasitoid of this sharpshooter species in Georgia (Huber 1988). Earlier studies in Monticello, Florida (R. F. M., unpublished data) estimated average parasitism of H. coagulata eggs there at ca. 80%. During July and August 1997, we collected egg masses of H. coagulata from crape myrtle (Lagerstroemia indica L.) and citrus trees grown at the University of Floridas North Florida Research and Education Center. In July samples, more than 90% of ca. 300 emerged parasitoids were G. ashmeadi. One female was identified as G. morrilli (Howard), and the rest belonged to an undescribed Zagella sp. (Trichogrammatidae). In August samples, however, Zagella sp. was by far the dominant parasitoid of H. coagulata eggs. The genus Zagella

DISTRIBUTION AND PLANT ASSOCIATION RECORDS FOR HOMALODISCA COAGULATA (HEMIPTERA: CICADELLIDAE) IN FLORIDA

Scientific Notes DISTRIBUTION AND PLANT ASSOCIATION RECORDS FOR HOMALODISCA COAGULATA (HEMIPTERA: CICADELLIDAE) IN FLORIDA M ARK S. H ODDLE 1 , S ERGUEI V. T RIAPITSYN 1 AND D AVID J. W. M ORGAN 2 Department of Entomology, University of California, Riverside, CA 92521 California Department of Food and Agriculture, Mt. Rubidoux Field Station 4500 Glenwood Drive, Riverside, CA 92501 The glassy-winged sharpshooter, Homalodisca coagulata (Say) is the focus of a major classical bi- ological control program in California. This insect presents a serious threat to several agricultural commodities and potentially native plants as well because of its ability to vector the xylem-inhabit- ing bacterium Xylella fastidiosa, the causative or- ganism of “scorch like” diseases such as Pierce’s Disease of grapes and oleander leaf scorch, a seri- ous malady of oleanders (Purcell & Saunders 1999). Homalodisca coagulata is an invasive pest in California and its native range is the southeast- ern and northeastern regions of the USA and Mex- ico, respectively (Triapitsyn & Phillips 2000). Homalodisca coagulata probably was translocated to southern California as egg masses via the move- ment of ornamental plants in the late 1980’s (So- rensen & Gill 1996) and without an accompanying natural enemy fauna; inordinate populations of glassy-winged sharpshooters have resulted. During foreign exploration by MSH and SVT for H. coagulata and associated egg parasitoids in Florida in August 2001, the authors visited the Florida State Collection of Arthropods, Bureau of Entomology, Florida Department of Agriculture and Consumer Services in Gainesville. Following discussion with colleagues there, specimen re- ceipt vouchers for H. coagulata were provided that had been sent in for identification by lay peo- ple, ornamental, horticultural, and agricultural growers from around Florida. A total of 229 re- ceipts were catalogued for adult H. coagulata over the period 1958-2001 inclusive, and chits con- tained information on date of collection, locality, host plant, and sex of specimens. These data were used to determine possible host plant records, dis- tribution densities, and submission frequencies for H. coagulata for different areas of Florida. Homalodisca coagulata was collected from at least 72 plant species in 71 genera contained in 37 families and Citrus spp. were the most com- mon plants from which adult H. coagulata were captured (Table 1). Of these plant association records in Table 1 it is uncertain which can sup- port development of H. coagulata from egg to adulthood. Adult H. coagulata are vagile and known to be highly polyphagous while the rela- tively immobile immature stages have a nar- rower host range (Turner & Pollard 1959). Citrus may be over-represented in this dataset because of regular pest surveys in this economically im- portant crop. To determine if regional differences in numbers of H. coagulata specimens sent in for identification existed, Florida was divided into thirds: (1) top third was north of 29° Latitude; (2) middle third was 27°-29°; and (3) the bottom third was south of 29°. Specimen receipts for each county in each section of the state were assumed to have been submitted for identification accord- ing to a poisson distribution and proportions were compared using a Log-likelihood Ratio Test (i.e., G-test). Pair-wise comparisons between regions from which specimens were received were made using χ 2 as sample sizes were large (Sokal & Rohlf 1995). The G-test was also used to determine if the frequency with which samples were submitted from each region significantly differed. Significant differences in the number of specimens received by region existed ( χ 2 = 11.03; df = 2; P = 0.004). Sig- nificantly more specimens were received for iden- tification from north Florida, intermediate numbers from central Florida, and fewest speci- mens came from south Florida (Fig. 1). No signifi- Fig. 1. Proportion (±95% CI) of specimens and sub- missions of adult Homalodisca coagulata from north, central, and south Florida to the Florida State Collec- tion of Arthropods in Gainesville for identification over the period 1958-2001. Bars with the same letters (upper case [specimen comparisons] or lower case [submission comparisons]) are not significantly different from each other at the 0.05 level of significance.

Key to the Holarctic species of Anagrus Haliday (Hymenoptera: Mymaridae) with a review of the Nearctic and Palaearctic (other than European) species and descriptions of new taxa.

The Holarctic species of the genus Anagrus Haliday are keyed. The Palaearctic species, other than the European ones revised earlier by Chiappini (1989), and 10 out of 11 valid species described from the Nearctic region are reviewed, based on a study of their type material. Two new species, A. rilensis Donev sp. n. and A. longitibialis Donev sp. n., are described from Bulgaria. A new specific synonymy is proposed: A. giraulti Crawford, 1913 with A. nigriventris Girault, 1911 (described as A. armatus var. nigriventris). New replacement name: A. oregonensis S. Triapitsyn nom. n. pro A. nigriceps Girault, 1915 (A. armatus var. nigriceps) nec Smits van Burgst, 1914. A. spiritus Girault, 1911 and A. columbi Perkins, 1905 are reinstated as valid species. A checklist of 68 presently recognized species of Anagrus is given in accordance with their distribution in different biogeographic regions.

Biology of Zagella delicata (Hymenoptera: Trichogrammatidae), an Egg Parasitoid of the Sharpshooter Tapajosa rubromarginata (Hemiptera: Clypeorrhyncha: Cicadellidae) in Argentina

Abstract Research on biological control of glassy-winged sharpshooter (GWSS) Homalodisca coagulata (Say) started in the 1990s. This sharpshooter, vector of Pierce’s disease bacteria Xylella fastidiosa Wells, expanded its geographical distribution and it has become a very serious pest problem in several crops, especially grapes, in southern California. In 2000, a survey of sharpshooter egg parasitoids was initiated in Argentina. Fourteen species of egg-parasitoids were collected. We report here on laboratory studies of adult longevity, oviposition preference, sex ratio, and development time of Zagella delicata De Santis. Field result of the incidence on its hosts and seasonal occurrence also are provided. Zagella delicata produced one adult per host egg. The overall results indicated that 72.5% of the sharpshooter eggs exposed to Z. delicata were parasitized. Wasps emergence was 43.8%. In host plant searching preference tests, Z. delicata females parasitized 66.7% of host eggs on sugar cane, 57.0% of eggs on corn and 4.5% on citrus leaves. The development time (from oviposition to adult emergence) averaged 23.5 ± 1.2 days. The average adult longevity was 10.3 ± 5.8 days. Females lived longer than males (females: 12.2 ± 5.6 days, males: 6.2 ± 3.7 days). The sex ratio in the laboratory was 1: 2.1 (males/females). In a hyperparasitism test, no adults of Z. delicata emerged from eggs previously exposed to Gonatocerus tuberculifemur. Seasonal sampling carried out in San Miguel de Tucumán showed that Z. delicata occurred from spring to fall, with maximum abundance at the beginning of the spring, where 57.2% out of the 1568 sampled eggs were parasitized. Field and laboratory data suggest that Z. delicata could be a prospective biological control agent against other, exotic, proconiine sharpshooters including H. coagulata. However, the efficiency of Z. delicata is restricted to habitats dominated by grasses.

Molecular characterization of Gonatocerus tuberculifemur (Ogloblin) (Hymenoptera: Mymaridae), a prospective Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) biological control candidate agent from South America: divergent clades.

We genetically characterized the prospective South American egg parasitoid candidate, Gonatocerus tuberculifemur, of the glassy-winged sharpshooter (GWSS), Homalodisca vitripennis, for a neoclassical biological control program in California. Two molecular methods, inter-simple sequence repeat-polymerase chain reaction DNA fingerprinting and a phylogeographic approach inferred from the mitochondrial cytochrome oxidase subunit I gene (COI), were utilized. Five geographic populations from South America were analyzed; in addition, a phylogenetic analysis was performed with several named and one unnamed Gonatocerus species using the COI gene. DNA fingerprinting demonstrated a fixed geographic banding pattern difference in the population from San Rafael, Mendoza Province, Argentina. The COI analysis uncovered haplotype or geographic structure in G. tuberculifemur. A neighbour-joining distance (NJ) and a single most parsimonious tree (MP) clustered the populations into two well-supported distinct clades with strong bootstrap values (97-99% and 92-99%, respectively) with populations from San Rafael clustering into clade 2 and the rest of the populations clustering into clade 1. No haplotype sharing was observed between individuals from the two clades. Phylogenetic analyses performed by NJ and MP methods with 15 Gonatocerus species confirmed species boundaries and again uncovered two distinct clades in G. tuberculifemur with strong bootstrap support (95-100% and 68-100%, respectively). However, the NJ tree supported the morphologically defined relationships better than the MP tree. The molecular evidence in the present study is suggestive of a species level divergence. Because G. tuberculifemur is under consideration as a potential biological control agent for GWSS in California, understanding cryptic variation in this species is critical.

A new distribution and host record for Gonatocerus triguttatus in Florida, with notes on Acmopolynema sema (Hymenoptera: Mymaridae).

Triapitsyn et al. (1998) reported results of the 1997 survey of egg parasitoids of the glassywinged sharpshooter, Homalodisca coagulata (Say) (Homoptera: Cicadellidae), in northern Florida. As part of an on-going classical biological control program against H. coagulata in California, two of the authors conducted a survey of egg parasitoids of proconiine sharpshooters (Cicadellidae: Cicadellinae: Proconiini) throughout Florida in August 2001 (Triapitsyn & Hoddle 2001). Among several species in the families Mymaridae and Trichogrammatidae (both Hymenoptera) that were collected (Triapitsyn & Hoddle 2001), there were two mymarid species on which the previously unknown information is given below. All specimens resulting from this study were determined by S. V. Triapitsyn; the vouchers of parasitoid species were deposited in the Entomology Research Museum, University of California at Riverside, California [UCRC] and those of proconiine sharpshooter species were deposited in the California State Collection of Arthropods, California Department of Food and Agriculture, Sacramento, California; also examined was the collection of Mymaridae at the Florida State Collection of Arthropods in Gainesville, Florida [FSCA]. Gonatocerus triguttatus Girault, originally described from specimens reared from an egg mass of an unidentified leafhopper on orange, Citrus sinensis (L.) Osbeck, in Trinidad (Girault 1916), was reared recently in northeastern Mexico from egg masses of H. coagulata, Oncometopia clarior (Walker), and an unidentified Oncometopia species (Triapitsyn & Phillips 2000, Triapitsyn et al. 2002). Gonatocerus triguttatus is also known from eggs of H. coagulata in Texas (Jones 2001, Triapitsyn & Hoddle 2001). In Apopka, Florida, we reared two females of G. triguttatus from an egg mass of the blackwinged sharpshooter, Oncometopia nigricans (Walker), laid in a leaf of crape myrtle, Lagerstroemia indica L., in the parking lot of the University of Florida Mid-Florida Research and Education Center. From the same plant and several adjacent crape myrtle trees, we also collected an adult specimen and several nymphs of 0. nigricans, which is the prevalent proconiine sharpshooter species on woody plants in central and southern Florida, whereas relative abundance of H. coagulata decreases from north-central Florida southward (Timmer et al. 1982), although it is known in southern Florida as far as Homestead (Turner & Pollard 1959). Gonatocerus triguttatus has not been known previously from Florida and 0. nigricans is a new host record for this parasitoid. Before our discovery, the only known record of an egg parasitoid of 0. nigricans was by Turner & Pollard (1959) who reported a Gonatocerus sp. (as Lymaenon sp.) in Plant City, Florida, from eggs of Oncometopia undata (Fabricius), that is an obvious misidentification of 0. nigricans following Young (1968). Material Examined. USA, Florida, Orange Co., Apopka, 21-VIII-2001, M. S. Hoddle and S. V. Triapitsyn, 2 females (emerged in UCR quarantine 30-VIII-2001 from an egg mass of 0. nigricans on crape myrtle) [UCRC]. Notes on Aemopolynema sema Schauff. This species was described from a large series of type specimens reared from eggs of the johnsongrass sharpshooter, Homalodisca insolita (Walker), in Fort Valley, Georgia (Schauff 1981). We reared A. sema from egg masses of the same host, laid in Johnson grass, Sorghum halepense (L.) Persoon, collected at the grounds of the University of Florida Everglades Research and Education Center in Belle Glade, Florida, on 19-VIII-2001 and brought under permit into UCR quarantine. Numerous specimens of H. insolita were collected from the same plants on which the egg masses were found. Following emergence, which began within the sealed containers while we still were in Florida and continued en masse in UCR quarantine, female and male parasitoids were given time to mate and then were exposed to H. coagulata eggs laid in leaves of Euonymus japonica Thunberg on 24-VIII-2001. The first generation (n > 100), which consisted of both females and males (the sex ratio was 4.3:1, respectively), was successfully obtained on 10-IX-2001 and exposed to the host on 12-IX-2001. The second generation, which emerged on 29-IX-2001, however, consisted of males only (n > 400), thus our colony ofA. sema was discontinued thereafter. We suspect that this was in response to the fact that H. coagulata is not the natural host for this parasitoid, which prefers to attack egg masses of H. insolita, a species that feeds and lays eggs on grasses (Turner &

Parasitoids of obscure mealybug, Pseudococcus viburni (Hem.: Pseudococcidae) in California: establishment of Pseudaphycus flavidulus (Hym.: Encyrtidae) and discussion of related parasitoid species

Abstract To improve natural suppression of the obscure mealybug, Pseudococcus viburni (Signoret), the parasitoids Pseudaphycus flavidulus (Brèthes) and Leptomastix epona (Walker) (Hymenoptera: Encyrtidae) of Chilean origin were released in Californias Central Coast vineyards from 1997 to 1999. A survey for parasitoids of P. viburni was conducted in the Edna Valley appellation wine grape region from 2005 to 2007, 6–8 years after classical biological control releases were discontinued. Two survey methods were used. First, field collections of obscure mealybugs from commercial vineyard blocks (2005–2007) and, second, placement of “sentinel mealybugs” on potted (1 L) grape vines (2006 only). From both survey methods, P. flavidulus was recovered, albeit levels of parasitism were low (less than 0.6%). We also placed longtailed mealybug, Pseudococcus longispinus (Targioni Tozzetti), on potted plants concurrent with placement of sentinel obscure mealybugs in the vineyard in order to measure parasitoid activity on this closely-related mealybug species. No P. flavidulus were recovered from P. longispinus. Other encyrtid parasitoids reared from either P. viburni or P. longispinus were Anagyrus pseudococci (Girault), Leptomastix dactylopii Howard, Leptomastidea abnormis (Girault), Coccidoxenoides perminutus Girault, and Tetracnemoidea peregrina (Compere). A hyperparasitoid, Chaetocerus sp., was also reared. The data are discussed with respect to biological control of vineyard mealybugs and newly developed controls for the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae). Because Pseudaphycus species reared from mealybugs are superficially very similar a taxonomic key and discussion of host relationships for selected Pseudaphycus species are provided.

Egg Parasitoids of Proconiini (Hemiptera: Cicadellidae) in Northwestern Mexico, with Description of a New Species of Gonatocerus (Hymenoptera: Mymaridae)

Abstract Nine species of Mymaridae and Trichogrammatidae parasitic on eggs of Proconiini sharpshooters (Cicadellidae: Cicadellinae) were collected in northwestern Mexico in relation to neoclassical biological control efforts against glassy-winged sharpshooter, Homalodisca vitripennis (Germar), in California. Gonatocerus chula Triapitsyn and Bernal sp. n., which belongs to the ater species group of Gonatocerus Nees (Mymaridae), is described. Specimens of G. chula sp. n. were reared from eggs of the smoke-tree sharpshooter, Homalodisca liturata Ball, on jojoba [Simmondsia chinensis (Link) C. K. Schneider] leaves collected in central Sonora state, Mexico. Also given are new data on other egg parasitoids of Homalodisca spp. and Oncometopia spp. in Sinaloa and Sonora states, Mexico, including Gonatocerus atriclavus Girault, G. morrilli (Howard), and G. novifasciatus Girault, and the Trichogrammatidae Burksiella sp(p)., Ittys sp., Pseudoligosita sp., Ufens ceratus Owen, and U. principalis Owen. For the first time, a species of Ittys is recorded from eggs of Proconiini, and U. principalis from Mexico. Colonies of G. atriclavus, G. novifasciatus and Pseudoligosita sp. were successfully established in a quarantine laboratory at University of California, Riverside, on eggs of the glassy-winged sharpshooter. These three parasitoid species had never been reared under laboratory conditions. In addition, seven species of Proconiini were collected in central and northwestern Mexico: Cyrtodisca major (Signoret), Homalodisca insolita (Walker), H. liturata Ball, Oncometopia sp. cf. clarior (Walker), O. sp. cf. trilobata Melichar, O. (Similitopia) sp., and Phera centrolineata (Signoret). Oncometopia sp. cf. clarior, O. sp. cf. trilobata, and O. (Similitopia) sp. appeared to be undescribed species.

First Report of a Proconiine Sharpshooter, Anacuerna centrolinea (Hemiptera: Cicadellidae), in Chile, with Notes on Its Biology, Host Plants, and Egg Parasitoids

Abstract The first representative of the leafhopper tribe Proconiini (subfamily Cicadellinae), Anacuerna centrolinea (Melichar) is reported herein from the Tarapacá region in northern Chile. This species was discovered at high elevation (≈4,000 m) in the course of a survey conducted in South America by the USDA–ARS for the neoclassical biological control program against the glassy-winged sharpshooter, Homalodisca coagulata (Say) in California. New data are given on the biology and host plants of A. centrolinea. Information also is provided on its egg parasitoid, Gonatocerus tuberculifemur (Ogloblin) (Hymenoptera: Mymaridae) which also was a first record from Chile. This discovery encourages further exploration for leafhopper egg parasitoids in northern and central regions of Chile to identify new perspective biological control agents that are more adapted to Mediterranean climate (winters and wet summers), which are similar to California climate. In addition, it is possible that G. tuberculifemur may be a good candidate for the biological control of the recently discovered H. coagulata in Easter Island, Chile.

Marietta leopardina (Hymenoptera: Aphelinidae) and Aprostocetus (Aprostocetus) sp. (Hymenoptera: Eulophidae) are Obligate Hyperparasitoids of Tamarixia radiata (Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae)

Marietta leopardina and Aprostocteus (Aprostocetus) sp. that emerged from Diaphorina citri nymphs collected from the Pakistani Punjab and exposed in quarantine to D. citri nymphs parasitized by Tamarixia radiata or Diaphorencyrtus aligarhensis successfully emerged from both of these primary parasitoids. Marietta leopardina and A. (Aprostocetus) sp. did not reproduce on unparasitized D. citri nymphs. These exposure experiments confirmed that M. leopardina and A. (Aprostocetus) sp. are obligatory hyperparasitoids of T. radiata and D. aligarhensis in the Diaphorina-Tamarixia-Diaphorencyrtus system. Marietta leopardina y Aprostocteus (Aprostocetus) sp. emergidos de ninfas de Diaphorina citri recolectadas en Punjab de Pakistan fueron expuestos en cuarentena sobre ninfas de D. citri parasitadas por Tamarixia radiata o Diaphorencyrtus aligarhensis, logrando emerge con exito de estos dos parasitoides primarios. Marietta leopardina y A. (Aprostocetus) sp. no se reproducieron en ninfas de D. citri no parasitadas. Estos experimentos de exposicion confirmaron que M. leopardina y A. (Aprostocetus) sp. son hiperparasitoides obligatorios de T. radiata y D. aligarhensis en el sistema de Diaphorina-Tamarixia-Diaphorencyrtus.