E NTOMOLOGY

A. Protasov et al. (2008) Phytoparasitica 36(5):449-459

Occurrence of Two Local Megastigmus Species Parasitic on the Eucalyptus Gall Wasp Leptocybe invasa in Israel and Turkey
Alex Protasov,1 Miktat Do anlar,2 John La Salle3 and Zvi Mendel1, g
Two local Megastigmus species were found to be parasitoids on the invasive Eucalyptus gall wasp Leptocybe invasa Fisher & La Salle in Turkey and Israel. Megastigmus sp. from Israel is a larval and pupal parasitoid of L. invasa. Both species are biparental. Features showing morphological differences between them are presented. The biology, distribution and potential efciency as biological control agents are discussed. KEY WORDS: Adaptation; biological control; invasive species; longevity; seasonal occurrence.

INTRODUCTION The invasive Eucalyptus gall wasp Leptocybe invasa Fisher & La Salle (Hymenoptera; Eulophidae), in some cases erroneously identied as Aprostocetus sp., became established in the Mediterranean countries over the last decade (3,6,14,18). The cited studies have shed light on several aspects of the biology of this invasive gall wasp, but only Viggiani et al. (25) refer to parasitoids or predators associated with it in this area, citing the occurrence of Megastigmus sp. (Hymenoptera: Torymidae) parasitizing the galls of L. invasa in Italy. Subsequently, two Megastigmus species were reared by us from L. invasa galls in Israel and Turkey. Comparison of mounted specimens of the latter wasps with the Italian one suggested that the materials collected in Israel and Turkey belonged to different species (M. Do anlar, G. Viggiani, pers. comm.). g Megastigmus species have various feeding habits, but are mainly phytophagous in seeds or associated with galls (8). Although most of the gall associations are as parasitoids of the gall wasp, there have been some reports of Megastigmus species as inquilines or even as gall inducers (13). Megastigmus species form the major group of seed-eating insects recorded in Eucalyptus fruits (2). In Australia, among the nearly 120 species of Megastigmus Dalman whose biological habits are known, 36 species have been reared as presumptive parasitoids of a number of gall wasps on several plants (7). Parasitoids of the genus Megastigmus are also well known from cynipid gall wasps on oaks (5,10,12). In the present paper we report on the association between L. invasa and two Megastigmus species, one in Israel and the other in Turkey, and describe their occurrence in both countries. We also present information on the development and adult survival of the Israeli
Received April 6, 2008; accepted June 15, 2008; http://www.phytoparasitica.org posting Oct. 6, 2008. 1 Dept. of Entomology, ARO, The Volcani Center, Bet Dagan 50250, Israel. *Corresponding author [e-mail: zmendel@volcani.agri.gov.il]. 2 Mustafa Kemal Universitesi, Ziraat Fak ltesi, Bitki Koruma B l m , 31034 Antakya, Hatay, Turkey [e-mail: u ou u doganlar@mku.edu.tr]. 3 CSIRO Entomology, GPO Box 1700, Canberra, ACT, 2601, Australia [e-mail: john.lasalle@csiro.au].

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Megastigmus species. Moreover, we discuss the origin of these parasitoids in the light of their distribution and adult survival. MATERIALS AND METHODS Sampling areas and procedure Stands of Eucalyptus camaldulensis infested with L. invasa were sampled in 2006 and 2007 in three provinces of Turkey (Adana, Hatay and Osmaniye) located around Iskenderun Bay on the Mediterranean. Analogous samplings were conducted in Israel mainly in 2003 and 2004 and also, sporadically, between 2000 2002 and 20052007, in seven locations that represented all the major planting areas of the country. The sampling procedures in the two countries were similar. Twigs that harbored 4080 multicell galls of various ages were removed from the trees (fruits or owers were excluded) and put into sealed transparent polyethylene bags without ventilation. During a period of about 2 weeks the emerging wasps were collected and identied. Details of the sampling points and times of sampling in both countries are presented in Table 1. Longevity The longevity of Megastigmus sp.-I (Israel) was determined under eight feeding treatments: (i) no food; (ii) water; (iii) young healthy foliage of E. camaldulensis; (iv) honey solution, i.e., 1:1 solution in distilled water; (v) combination of treatments iii and iv; (vi) fresh E. camaldulensis owers; (vii) galled foliage and twigs of E. camaldulensis (Stage C, 75 days post-oviposition of L. invasa); and (viii) combination of treatments iv and vii. The wasps, 20 of each sex, were placed in 95-mm-diam petri dishes tted with a lter-paper disk. The water or the honey solutions were sprayed along a narrow strip on the cover of each petri dish, and the food supply, including water and leaf materials, was renewed daily. The wasps for testing were collected on the day of emergence, removed with a ne brush and placed in a petri dish, males and females separately. Wasp mortality was recorded daily. The test was conducted at 25 C and 7075% relative humidity. Survival data were analyzed with the Life Test Procedure software package of the SAS Institute (23). Empirical survival distributions were tted to the various treatments. The homogeneity of the survival distributions was tested with Log-Rank statistics. Parasitoid development Five groups of ve to ten 18-month-old saplings were exposed to one-day-old L. invasa in ventilated Plexiglas cages for 24 h. Ten gall wasps per sapling were introduced into each cage on a range of dates in order to produce a range of gall ages: (0) uninfested sapling, (A) 14 days (egg to hatching), (B) 50 days (young larvae), (C) 75 days (mature larvae), (D) 100 days (prepupae to pupae), and (E) 115 days (callow adult before emergence). Adult emergence occurred 122.5 3.6 days after the infestation, and ranged from 110 to 130 days. Two pairs of Megastigmus sp.-I were then introduced for 24 h into each cage. The test was conducted in a ventilated greenhouse with temperature ranging from 23 to 31 C and relative humidity from 40% to 75%. After 35 days the galling growths were removed and placed in transparent polyethylene bags in order to monitor the emergence of the wasps. Percentage mortality was calculated from the number of emerging parasitoids divided by the total number of emerging wasps (gall inducers + parasitoids) for each cage. RESULTS Taxonomic notes Megastigmus is a large and difcult genus, and the proper resolution of the identity of these two species (either as already named species or as new species) will
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require detailed revisional studies of the European fauna. For the purpose of this paper, we are supplying morphological characteristics which will allow the accurate determination of the two species associated with L. invasa in order to support efforts to monitor the spread and effectiveness of these wasps.

Figs. 1-4. Megastigmus sp. Turkey 1) Thorax dorsal view, 2) female forewing, 3) male forewing, 4) male gaster.

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452 TABLE 1. Sampling areas of the studied Megastigmus species in Turkey and Israel
Megastigmus Leptocybe invasa Number of sp. samplings Turkey 13 257 1 18 303 1 3 113 1 1 67 1 4 233 1 9 115 1 23 194 1 0 ** 1 0 ** 1 0 ** 1 0 ** 1 0 ** 1 0 ** 1 Israel 0 392 1 0 281 3 0 134 1 0 335 3 142 254 3 0 231 1 0 587 3 0 387 3 0 246 3 0 237 1 *27 km from Kadirli. **Wasps were not counted; at least several dozen emerged. Collection date Coordinates Collection site Country and area April 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 Nov. 07 June 06 July Sept. 03 June 06 July Sept. 03 July Sept. 03 April 05 May 05, June 06 May - June 05 June - July 05 July 06 36o 36o 36o 36o 37o 37o 37o 37o 37o 37o 37o 37o 37o 33o 32o 32o 33o 32o 32o 32o 32o 31o 31o 08N, 36o 04E 58N, 35o 29E 57N 35o 38E 59N 35o 40E 01N 35o 44 E 15N, 35o 39E 22N, 35o 51E 15N, 35o 39E 20N, 35o 55E 21N, 36o 03E 22N, 36o 05E 07N, 36o 12E 17N, 36o 21E 02N, 35o 58N, 35o 46N, 35o 04N, 35o 30N, 35o 26N, 34o 05N, 34o 03N, 34o 46N, 35o 19N, 34o 50E 48E 24E 35E 27E 54E 52E 50E 00E 40E Samanda g Incirlik Yakapnar Cakaldere Ceyhan Imamo lu g near Kozan* Sarcam City center Kadirli-Cukurk pr o u Kadirli-Aydnlar Kadirli Orhaniye D zici u Allone haBashan Keshet Golani Junction Hula Nir Dawid Hedera Forest Segula Tel Hashomer Eshtaol Gilat Hatay Adana Osmaniye Golan (center) Eastern Galilee Jordan Valley Bet Shean Valley Coastal Plain North Coastal Plain Center Coastal Plain Center Judean Foothills Western Negev

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TABLE 2. Number of Leptocybe invasa and Megastigmus sp.-I emerged in the laboratory per 100 galled twigs (>1000 galls) from Eucalyptus camaldulensis galling material collected during 8 months at Nir Dawid (Bet Shean Valley) in 2004 and comprising galls at various development stages
L. invasa Megastigmus sp.-I Jan 35 0 Feb 29 0 March 79 0 April 118 0 May 151 0 June 102 July 69 10 Aug 50 117 Sept 125 17 Oct 83 0 Nov 52 0 Dec 31 0

TABLE 3. Parasitism and development duration of Megastigmus sp.-I when exposed to Eucalyptus camaldulensis saplings bearing various gall stages of Leptacybe invasa
Galls of L. invasa subjected to attack by Megastigmus sp.-I Development stage (days Number of galls Number of after oviposition) immatures 0 0 0 A (14) 31* 31 B (50) 7 20 C (75) 19 32 D (100) 25 71 E ((115) 13 26 * Number of scars at the oviposition points. ** The parasitoid emerged from only one of the saplings. Emerging Megastigmus sp.-I Number Mean (SD) development time (days) 0 0 0 0 1 41** 11 44.0 1.7 20 42.0 2.2 2 43** Number Emerging L. invasa Mean (SD) development time (days) 0 118.61.9 121.31.5 122.73.5 125.03.2 124.03.3 % Mortality

0 26 16 17 51 22

0.0 0.0 5.0 34.4 28.2 7.7

Figs. 5-8. Megastigmus. Israel 5) Thorax dorsal view, 6) female forewing, 7) male forewing, 8) male gaster.

Both the Turkish and the Israeli Megastigmus are biparental. The features showing morphological differences between the two species are as follows. Distance between the tip of mesonotum and the rear end of the scutellum exceeds the width of the mesonotum (6.5:5) (Fig. 1); the female forewing has stigma almost three times as long as broad (Fig. 2); the male forewing has stigma 1.6x as long as broad (Fig. 3); the male gaster length is more than twice its breadth (Fig. 4) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Megastigmus sp.-T (Turkey)

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Fig. 9. Survival patterns of female (the upper graph) and male Megastigmus sp.-I at 25 C, as related to feed alternatives. Each treatment of each wasp sex involved 20 wasps. In parentheses are the values of Log-Rank statistics: values with a common letter do not differ statistically (P =0.05) according to a closed test procedure.

Distance between the tip of mesonotum and the rear end of the scutellum is shorter than the width of the mesonotum (5:6) (Fig. 5); the female forewing has stigma almost twice as long as broad (Fig. 6); the male forewing has almost circular stigma (Fig. 7); the male gaster is only slightly longer than its breadth (7:6) (Fig. 8) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Megastigmus sp.-I (Israel) In general, the parasitic species (as opposed to the phytophagous species) of Palearctic Megastigmus have their antennae inserted just above the level of the lower ocular line, and the thoracic dorsum with at least some metallic green, bluish or violet coloration (22). Both the studied species have their antennae inserted just above the level of the lower ocular line, which matches that of parasitic species; however, any metallic coloration on the thoracic dorsum is lacking. Thus, they do not t comfortably into the parasitoid/phytophagous

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groupings of Roques and Skrzypczynska (22). Habitat, hosts and seasonal occurrence The specimens of both Megastigmus species were obtained from galls of L. invasa induced on E. camaldulensis. Megastigmus sp.-T was found in several locations in Adana province and in the sampled locations in Hatay, but not in the sites sampled in Osmaniye (Table 1). In Turkey all the samples were collected in November, except for the Hatay area, where the sample was taken in April (Table 1). From all these sites small numbers of the Torymidae emerged (ranging from 1 to 23 individuals per sample) (cf. Table 1). Among the ten sampling sites in Israel, placed in some of the major Eucalyptus plantings of the country, Megastigmus sp.-I was found only in Nir Dawid, located in the Bet Shean Valley (Table 1). Since we initiated our study on the gall wasp, not even a single Megastigmus specimen was obtained in other areas. Samplings in Nir Dawid were conducted regularly during every warm season between 2000 and 2007, and specimens were always collected from samplings taken in the second half of the summer. Accurate counting of the wasps that emerged from galls sampled in 2004 suggested that the wasp could be detected on site in small numbers in July, reached its peak emergence in August, and disappeared from the samplings in October (Table 2). Longevity of Megastigmus sp.I The survival patterns of adult wasps differed significantly among treatments (Fig. 9). We were able to divide the females into two groups of survivors. When the wasps were not supplied with anything, or were supplied with water, young healthy foliage, or galled foliage alone or with honey solution (treatments i, ii, iii, vii and viii, respectively), estimated 50% female survival period was 3.0 days, with lower and upper 95% condence limits of 3 and 4 days. When the females received honey and water solution or owers, young healthy foliage + honey solution (treatments vi and v, respectively), 50% survival estimates ranged between 4.5 and 5.0 days, with lower and upper 95% condence limits of 4 and 7 days, respectively. Males could be divided into four groups of survivors (Fig. 9). The shortest life span was among those that were not supplied with anything (treatment i), whose survival lasted from 2.0 to 3.0 days. A second group, with longer survival, comprised those supplied with water, young healthy foliage, or galled foliage alone; their estimated survival ranged from 2.0 to 3.0 days, with lower and upper 95% condence limits being the same. The third group comprised those fed with owers, among whom male survival averaged 3.0 days, with lower and upper 95% condence limits of 2 and 4 days, respectively. Survival on owers was signicantly longer than in the no-feed treatment. The longest survivals were among males that were offered young leaves and honey solution, galled leaves and honey solution, or honey solution alone. Comparison between male and female survival in each feed treatment, separately, revealed that between treatments longevity differed signicantly between the sexes only in the case of galled leaves and honey solution (Chi-Square 14.1095; P>0.0002). Notes on the development of Megastigmus spp. Megastigmus sp.-I lays a single egg inside the gall, on the larva or pupa of L. invasa, and it develops as a solitary ectoparasitoid. In Adana province Megastigmus sp.-T can produce at least three generations during the period from May to November each year, but its effectiveness in controlling the gall wasp is very low. We could not determine whether the host was killed immediately or shortly after parasitization. As shown in Table 3, Megastigmus sp.-I developed on the larval and pupal stages, but among the 34 individuals that emerged, 31 were obtained from galls containing

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developed or mature larvae. The development took 4143 days in a greenhouse under a temperature regime of 2331C. Percentage mortality of the gall wasp was low: 5.0% and 7.7% for gall wasp stages B and E, respectively, rising to 28.2% and 34.4% in gall wasp stages D and C, respectively. The parasitoid did not develop on galls at stage A. In the cited laboratory conditions we were able to rear eight consecutive generations of Megastigmus sp.-I. In Adana province Megastigmus sp.-T can produce at least three generations during the period from May to November each year, but its effectiveness in controlling the gall wasp is very low. The sex ratio of both species is close to 1:1. DISCUSSION Our ndings suggest that Megastigmus sp.I is a larval and pupal parasitoid of L. invasa. Neither of the investigated Megastigmus forms from Turkey and Israel seems to be an efcient natural enemy of this gall wasp (cf. Tables 1 and 3). The nourishment tests showed that host feeding was impossible: when wasps were offered galls that were suitable for successful parasitism, female parasitoids that were engaged in parasitization and that were fed on honey solution lived for a shorter time than those that were supplied with honey solution alone. Females of Closterocerus chamaeleon (Girault), a uniparental parasitoid of Ophelimus maskelli (Ashmead) (17) and Selitrichodes sp. (Eulophidae), a biparental parasitoid of L. invasa (Kim, I.L., Mendel, Z., Protasov, A., Blumberg, D. and La Salle, J., in preparation), displayed the same survival pattern as Megastigmus when supplied with galled leaves and honey solution. The Megastigmus sp. I males survived equally long with galled leaves and honey solution and honey solution alone. Males and females of Megastigmus sp.I survived equally long when supplied with water and E. camaldulensis owers or no feed at all. The inability to benet from the owers supports our hypothesis that Megastigmus sp. I was not originally associated with Eucalyptus. Previous studies showed clearly that both Eucalyptus gall wasps, O. maskelli (16) and L. invasa (14), as well as their parasitoids C. chamaeleon (17), Stethynium ophelimi Huber (11) and the above mentioned Selitrichodes sp., all originated from Australia, and prolonged their survival by feeding on their hostplant owers. The question of the local host(s) of these Megastigmus species is still open. Eucalyptus camaldulensis is one of the most common tree species in the lower areas of the eastern Mediterranean: as planted forest stands, as groves growing under irrigation, as ornamental trees or as windbreaks around fruit tree plantations (7). The occurrence of both Megastigmus species on E. camaldulensis only in restricted areas in Israel and Turkey, even though their host is abundant in the entire area, suggests that both are local species that adapted to develop on L. invasa galls. However, assigning these species to the Palaearctic parasitic Megastigmus on the basis of morphological characteristics is problematic. Whereas the position of their antennae matches that of parasitic Megastigmus species of the Palaearctic, the typical metallic color of the latter is lacking in the presently studied species. However, Rizzo and Askew (20) recently showed that body pigmentation varies in many Chalcidoidea depending on both a latitudinal cline (darker in the North, lighter in the South) and host type, recording this kind of variation in Megastigmus dorsalis (Fabricius) and other Torymidae in Jordan. So, the lack of a metallic shade in the present study could be due to other factors in the studied species (20).
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One may raise the question of whether the studied Megastigmus species are indeed part of the local fauna or whether they spread from Australia together with or soon after the invading L. invasa. Nevertheless, our accumulated circumstantial evidence leads to the conclusion that the discussed Megastigmus spp. are not natural associates of L. invasa. This conclusion is supported by the following points. (i) In Israel the Megastigmus sp. was collected at only a single site, whereas its host occurs at very high density all over the country; also in Turkey the parasitoid was collected in only one area; (ii) The Megastigmus sp. never became established in several other areas of Israel, despite our repeated efforts to establish its population. (iii) The data from Turkey indicate clearly that the Megastigmus sp. was not reared from the L. invasa galls during the winter and spring, which suggests that the population of its native host is probably less abundant in the second half of the summer. (iv) All of the three Megastigmus spp. addressed in the present study are restricted to rather small areas, whereas if one of them were indeed a natural associate of the gall wasp, and spread together with it, one would expect that the pace of spread of the parasitoid would be similar to that of its host. (v) It is unrealistic to suggest that the three Megastigmus spp. arrived at the same time, in three different locations: the Bet Shean Valley in Israel, Antakya in Turkey, and near Naples in Italy. There are abundant examples of native parasitoids exploiting introduced exotic host species, e.g. the case of the chestnut gall wasp (1,4) and, conversely, of introduced exotic parasitoids adopting local alterative hosts, e.g. the case of the citrus leaf miner (19,21). Host switching for parasitoids of gall wasps is quite well known among parasitic Megastigmus species (e.g. 1,15,24); a switch from E. camaldulensis to an endemic South African tree was recorded for Megastigmus zebrinus Grissell (9). Megastigmus sp.I was released in Bet Dagan (Israel coastal plain) but did not establish itself (A. Protasov, unpublished data). Because of the overlapping generations of L. invasa (14), the gall wasp could easily emerge from foliage throughout the year in the laboratory. We suggest that the Megastigmus sp.I population survives on a local gall wasp population that develops on nearby host plants of the wild vegetation. For an as yet undetermined reason, it switches to L. invasa galls during midsummer. In the light of the limited seasonal occurrence of Megastigmus sp.I discovered in Nir Dawid, it seems that in the forest the parasitoids do not live on Eucalyptus from autumn to early summer. However, in the laboratory we were able to rear it from L. invasa galls for many generations.
ACKNOWLEDGMENTS We thank Dani Blumberg, Nita Saphir, Zion Madar, David Brand, Oded Bar Shalom, Ami Zehavi, Miriam Eliyahu, Yehuda Gat and Ido Gofer for their assistance in various stages of the study. REFERENCES 1. Aebi, A., Sch nrogge, K., Melika, G., Alma, A., Bosio, G. and Quacchia, A. et al. (2006) Parasitoid o recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus. in: Ozaki, K., Yukawa, J., Ohgushi, T. and Price, P.W. [Eds.] Galling Arthropods and Their Associates: Ecology and Evolution. Springer, Japan. pp. 103-121. 2. Andersen, A.N. and New, T.R. (1987) Insect inhabitants of fruits of Leptospermum, Eucalyptus and Casuarina in south-eastern Australia. Aust. J. Zool. 35:327-336. 3. Aytar, F. (2003) Natural biology, distribution and control method of Leptocybe invasa Fisher & La Salle (Hym., Eulophidae), eucalyptus gall wasp in Turkey. DOA Dergisi [J. Mountain & Mediterranean Forestry] 9:47-66 (Turkish, with English summary). 4. Cooper, W. R. and Rieske, L. K. (2007) Community associates of an exotic gallmaker, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), in eastern North America. Ann. Entomol. Soc. Am. 100:236-244.

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