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Note: First record of the eucalyptus gall wasp Ophelimus maskelli and its parasitoid, Closterocerus chamaeleon , in Turkey


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The Eucalyptus gall waspOphelimus maskelli (Ashmead) (Hymenoptera: Chalcidoidea: Eulophidae: Ophelimini) and its introduced parasitoidClosterocerus chamaeleon (Hymenoptera: Chalcidoidea: Eulophidae: Entedoninae) are recorded for the first time in the Mediterranean and Aegean Regions of Turkey. Some morphological characters of adult and larva ofO. maskelli and larva ofC. chamaeleon are described and illustrated. Distributions of the two wasps collected in Turkey are given. Results indicate that the biological control agent,C. chamaeleon, has spread over 1,300 km in the 16 months since its initial release.
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ENTOMOLOGY M. Doˇganlar and Z. Mendel (2007) Phytoparasitica 35(4):333-335
NOTE:First Record of the Eucalyptus Gall Wasp Ophelimus
maskelli and Its Parasitoid, Closterocerus chamaeleon, in
M. Doˇganlar1and Z. Mendel,2
The Eucalyptus gall wasp Ophelimus maskelli (Ashmead) (Hymenoptera: Chalcidoidea: Eu-
lophidae: Ophelimini) and its introduced parasitoid Closterocerus chamaeleon (Hymenoptera:
Chalcidoidea: Eulophidae: Entedoninae) are recorded for the first time in the Mediterranean
and Aegean Regions of Turkey. Some morphological characters of adult and larva of O.
maskelli and larva of C. chamaeleon are described and illustrated. Distributions of the two
wasps collected in Turkey are given. Results indicate that the biological control agent, C.
chamaeleon, has spread over 1,300 km in the 16 months since its initial release.
KEY WORDS: Biological control; Closterocerus chamaeleon; eucalyptus; Ophelimus maskelli.
The gall wasp Ophelimus maskelli (Ash-
mead) is a pest of eucalypts which has recently
invaded the Mediterranean Basin, where it was
originally reported under the name O. euca-
lypti (Gahan) by several groups of researchers
(1,3,5,8-10). However, at the present stage of
the research, it was shown by Protasov, Blum-
berg, Brand, La Salle and Mendel (submitted for
publication) that the correct name forthis species
in Israel is O. maskelli (Ashmead), based on
the taxonomic history, diagnostic characteristics,
biology and impact on host plants.
An integrated control program on gall-
inducing pests was initiated by M. Doˇganlar
and colleagues in 2005, after the discovery of
Leptocybe invasa Fisher and LaSalle (6) in Hatay
province, Turkey, by Doˇganlar (4), and in other
parts of the Mediterranean region by Aytar (2).
Projects were undertaken to discover natural en-
emies of L. invasa through collecting and cul-
turing samples under laboratory conditions, and
to determine resistant/tolerant varieties of Eu-
calyptus camaldulensis and E. grandis through
collecting seedlings from nature and testing their
tolerance to attack by L. invasa. Up to now
no natural enemies have been found, but some
resistant and tolerant Eucalyptus varieties have
been found. These studies are being continued.
In the second half of December 2006
and in January 2007 many specimens of E.
camaldulensis and E. nigra leaves galled by
O. maskelli were collected from the towns
of Kırıkhan, Kumlu, Antakya and Iskenderun
(Hatay province), Adana city center, the villages
of G¨unyurdu Arıklı and Yenice-Tarsus, the city
center of Tarsus (Mersin province); in Alanya-
Antalya and Muˇgla in July – August 2006; and
from Urla, Gaziemir, C¸ iˇgli, and Izmir city center
in February 2007. Pre-hatched adults of O.
maskelli were removed from the galls, and iden-
tified using the diagnostic characters provided by
Protasov et al. (7). In particular, the forewing
has only a single submarginal seta, the prestig-
mal, marginal and stigmal veins are distinctly
broadened and darkened, and the postmarginal
vein is longer than the marginal vein (Fig. 1A);
there are two funicular segments, both having
distinct linear sensila; the first one being about
Received Feb. 28, 2007; accepted May 8, 2007; posting July 29, 2007.
1Dept. of Plant Protection, Faculty of Agriculture, Mustafa Kemal University, 31034 Antakya, Hatay, Turkey
2Dept. of Entomology, ARO, The Volcani Center, Bet Dagan 50250, Israel. *Corresponding author [e-mail:].
Phytoparasitica 35:4, 2007 333
half the length of the second, but clearly larger
than the three anellar segments (Fig. 1B). Other
characteristics are as described by Protasov et al.
(7). Many of the galls harbor overwintering lar-
vae of O. maskelli which have plant material in
their mid-guts. They are very different from
the parasitoid larvae in having very long coni-
cal papillae and a wide opening of the stigma
(Fig. 1C), whereas the larvae of Closterocerus
chamaeleon have much smaller papillae and a
narrower opening of the stigma (Fig. 1D).
Several hundred females of C. chamaeleon
were reared from the galls of O. maskelli col-
lected from Kırıkhan and from Tarsus city cen-
ter since mid-December 2006; no males were
found. Dissection of the galls revealed that
the parasitoids overwinter as last-instar larvae
or pupae. However, they were able to develop
into adults when they were kept under laboratory
conditions at 20–25C and 70–80% r.h. The
population of C. chamaeleon in Hatay province
originated from individuals that were released in
several locations in Israel from September 2005
to March 2006 and dispersed northward. The
parasitoids released in Israel were collected from
E. camaldulensis trees growing on the banks
of the Murrumbidgee River in Wagga Wagga,
NSW, Australia, in 2005. In January 2007,
C. chamaeleon was found in galled E. camal-
dulensis leaves collected in the city of Izmir,
approximately 1,300 km from the release sites in
the central coastal plain of Israel (at Bet Dagan).
This provides evidence that the parasitoid has
already spread some 1,300 km from the release
sites in Israel in only 16 months. Such an
impressive spread for an introduced parasitoid
indicates that it may be capable of providing
substantial biological control in the region.
The work on life history and relationships of
the galler and the parasitoid, and the survey of
their distributions in Turkey, are continuing.
Fig. 1. Ophelimus maskelli female collected in Hatay, Turkey: female (A), fore wing (B), antenna,
cephalic substructure and spiracles of the larvae (C); and cephalic substructure and spiracles of the
larvae of Closterocerus chamaeleon (D).
334 M. Doˇganlar and Z. Mendel
We thank the staff of the Forestry Department of Hatay for their help in collecting the specimens in their
Eucalyptus-growing areas; and Dr. John La Salle for his help in identifying the species of Closterocerus
chamaeleon, and for his valuable comments on the manuscript.
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(Hym., Eulophidae), eucalyptus gall wasp in Turkey. DOA Dergisi (J. DOA) 9:47-66.
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Filippo Silvestri 59:93-98.
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invasa (Hymenoptera: Eulophidae) gen. & sp. nov., an invasive gall inducer on Eucalyptus. Aust. J. Entomol.
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taxonomy and impact on host plants of Ophelimus maskelli, an invasive gall inducer on Eucalyptus spp. in
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8. Pujade-Villar, J. and Riba-Flinch, J. M. (2004) Dos especies australianas de eulofidos, muy daninas para
Eucalyptus spp., introducidas en el nordeste Iberico (Hymenoptera: Eulophidae). [Two Australian eulophids
very harmful to Eucalyptus spp., introduced into the north-east of the Iberian Peninsula.] Boll. Soc. Entomol.
Aragonesa 35:299-301.
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(Gahan) (Hymenoptera: Eulophidae) in Campania. Boll. Zool. Agrar. Bachic. 33:79-82.
Phytoparasitica 35:4, 2007 335
... Their presence in urban and semi-urban habitats is common in Europe; parks and gardens have been found to hold the largest number of alien arthropods amongst invaded habitats (Lopez-Vaamonde et al. 2010). Closterocerus chamaeleon ( Figure 2C), a parasitoid of O. maskelli, is renowned for its high dispersal potential in many Mediterranean countries utilizing both wind currents and human-mediated transportations (Doğanlar and Mendel 2007;Branco et al. 2009;Lo Verde et al. 2010;Caleca et al. 2011). ...
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... Unintentional spread of some of the natural enemies recorded in this study was previously reported from other eucalypt growing regions of the world. For example, C. chamaeleon, since its intentional release in Israel in 2005 (Protasov et al. 2007), has spread to different eucalyptgrowing regions, including the Mediterranean region (Doganlar and Mendel 2007;Borrajo et al. 2008;Branco et al. 2009), Chile and Argentina (Aquino et al. 2014;Bush et al. 2016). Psyllaephagus bliteus was intentionally introduced in California, Mexico and Chile in 2000, 2002respectively (Daane et al. 2005Plascencia-González et al. 2005;Ide et al. 2006) and subsequently spread to Brazil, Colombia, several Mediterranean countries (Caleca et al. 2011;Pérez-Otero et al. 2011;Bella and Rapisarda 2013;Reguia and Peris-Filipo 2013;Karaca et al. 2015) and Portugal (Dhari et al. 2014). ...
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Eucalypt forestry in sub-Saharan Africa is challenged by non-native eucalypt-feeding insects. In recent studies, six invasive eucalypt insect pests, namely Blastopsylla occidentalis, Glycaspis brimblecombei, Gonipterus sp.n.2, Leptocybe invasa, Thaumastocoris peregrinus and Ophelimus maskelli were confirmed present in sub-Saharan Africa. We investigated the diversity and distribution of natural enemies of these pests in six countries in the region. Plant parts (leaves, petioles and stem) infested with the insect pests were sampled from multiple sites in each country. The emerged natural enemies were identified using morphological characteristics and DNA sequence data. Nine species of natural enemies were confirmed present in the surveyed countries, namely Anaphes nitens, Closterocerus chamaeleon, Megastigmus sp., M. pretorianensis, Psyllaephagus blastopsyllae, P. bliteus, Quadrastichus mendeli, Selitrichodes kryceri and S. neseri. No natural enemies were found in Ghana and Sierra Leone despite the presence of L. invasa in both of those countries. Interestingly, most of these natural enemies were unintentionally introduced into the surveyed countries. Results of this study showed that both insect pests and natural enemies introduced into one country are likely to affect many other countries in the region. These findings call for a more coordinated approach to the management of plantation pests in the region.
... References: Anonymous, 2006 (loc.cit. Branco et al., 2016);Flock, 1957;Bain, 1977;Beardsley & Perreira, 2000;Schauff & Garrison, 2000;Berry & Withers, 2002;Kim et al., 2005;Dȏganlar & Mendel, 2007;Kim & La Salle, 2008;Wingfield et al., 2008;La Salle et al., 2009;Branco et al., 2016;Mansfield, 2016;Dittrich-Schröder et al., 2018; (accessed January 2020); ...
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... (Doğanlar & Mendel, 2007) ، ‫وتونس‬ (Dhahri et al., 2010) ، ‫تغال‬ ‫البر‬ ‫و‬ (Branco et al., 2009) ...
... There was a subsequent dispersal to different regions of the world. Ophelimus maskelli, has been reported in Italy [17], Spain [18], France [19], Turkey [20], Portugal [21], Argentina (2013) [22], the United States of America (2014) [23], Israel, South Africa, New Zealand, Vietnam, and Indonesia [24]. O. eucalypti has been reported in New Zealand [25], Iran, Morocco, Kenya, Uganda [17,18,26], and Greece [27]. ...
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Ophelimus eucalypti and Ophelimus maskelli are gall wasps that are considered as a threat to the large Eucalyptus commercial plantations in Sumatra, Indonesia. However, they are partially suppressed by parasitoids including Closterocerus chamaeleon. The aim of this study was to evaluate the longevity and daily survival rate of O. eucalypti, O. maskelli and C. chamaeleon adults when receiving or not receiving food sources and also when reared in four different vial types under two environments (one environmentally-controlled and another ambient), in a laboratory in Riau, Sumatra. The rearing test of C. chamaeleon as a biocontrol agent would be used for augmentative releases. We also evaluated the duration of the stages and the complete lifespan (egg → larva → pupa → adult) of O. eucalypti in a greenhouse in Porsea, North Sumatra, Indonesia, where this species is aggressive. With few exceptions, the longevity and survival rate of O. eucalypti, O. maskelli and C. chamaeleon adults was similar between the two conditions. The longevity and survival of C. chamaeleon were much greater than those of its gall wasp hosts, and of O. eucalypti greater than that of O. maskelli. Overall, these parameters were greater for gall wasps and the parasitoid reared in the larger vial types. The food source provided to O. maskelli adults did not however benefit the longevity of this gall wasp in the best tube type. The lifespan of O. eucalypti (mean ± SD of the mean) was 44 ± 6 days in a greenhouse. The much greater longevity and survival rate of C. chamaeleon than those of its hosts are facts that trigger the success of this insect as a gall wasp parasitoid. The higher longevity and survival of O. eucalypti compared to O. maskelli contribute to the higher threat status of O. eucalypti to Eucalyptus. This article is protected by copyright. All rights reserved.
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Viene riportata, per la prima volta in Sicilia e in Calabria, la presenza su Eucalyptus spp. degli Hymenoptera Eulophidae galligeni Ophelimus prope eucalypti e Aprostocetus sp.; quest'ultimo è stato rinvenuto anche in Lazio, su alberature stradali della città di Roma. Entrambe le specie provengono dalla regione australiana e sono state recentemente segnalate per altre regioni italiane. In Sicilia Ophelimus prope eucalypti è ancora sporadico mentre Aprostocetus sp. risulta molto più diffuso. La galla di Ophelimus prope eucalypti è rotondeggiante, pustoliforme e localizzata solo sulla lamina fogliare; quella di Aprostocetus sp. è globosa e si rinviene sui germogli, rametti, piccioli fogliari e nella nervatura principale della foglia. Si segnala il ritrovamento di due maschi di Aprostocetus sp., mentre nessun parassitoide è emerso dalle galle di entrambi gli Eulofidi fitofagi. Sulle piante di Eucalyptus, che in Sicilia hanno in genere età comprese tra 30 e 50 anni, non pare che i due galligeni arrechino danni apprezzabili.
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Abstract Leptocybe invasa Fisher & LaSalle, a new genus and species of Eulophidae, displays thelytokous reproduction, forming typical bump-shaped galls on the leaf midribs, petioles and stems of new growth of several Eucalyptus species. Presently, this wasp occurs in large areas in the Middle East, the Mediterranean and Africa, and is a serious pest in young plantations. Heavy galling prevents further development of the infested growth. Leptocybe invasa is only known from females. Mean length of a gall containing a single wasp is 2.1 mm, leaves of intensively growing trees may carry over 50 galls per leaf. Mean development time from oviposition to emergence is 132.6 d in room temperature. In Israel the wasp produces two or three overlapping generations annually. Mean survival time for wasps fed with honey and water is 6.5 days. Ten species were found to be suitable hosts in Israel: E. botryoides, E. bridgesiana E. camaldulensis, E. globulus. E. gunii. E. grandis, E. robusta, E. saligna, E. tereticornis, and E. viminalis.
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Ophelimus maskelli (Ashmead) (Hymenoptera: Eulophidae), an invasive species in the Mediterranean area that occurs naturally onEucalyptus camaldulensis at Wagga Wagga in New South Wales, was studied in Israel on the same host plant. The most distinctive characteristic ofO. maskelli as compared with other congeners is the presence of only a single seta on the submarginal vein.O. maskelli shows a clear tendency to oviposit in developed, immature leaves, and it prefers to oviposit on an area of the leaf blade near the petiole. The female lays an average of 109 eggs when maintained on water alone. The egglaying distribution tended towards aggregation, and the same tendency has also been observed within and among trees. The wasp prefers to attack the lower canopy. The gall diameter ranged from 1.2 to 0.9 mm, and gall density from 11.5 to 36.0 galls cm−2, respectively. The typical color of the gall appeared as soon as third instar larva developed. Galls on shaded leaves remained green or greenish-yellow, whereas those that were exposed to the sun were reddish.O. maskelli produces three generations per year in Israel. High flight occurs among the spring generations, starting in early March. The wasps were attracted to green sticky plates much more than to the other tested colors. Heavy galling byO. maskelli results in premature shedding of the leaves, soon after the emergence of the wasps. Among the 84 eucalyptus species tested, the following 14 species were found to be suitable hosts:E. botryoides, E. bridgesiana, E. camaldulensis, E. cinerea, E. globulus, E. gunii, E. nicholii, E. pulverulenta, E. robusta, E. rudis, E. saligna, E. tereticornis andE. viminalis. This study focused on morphological and development characters that can clearly distinguishO. maskelli fromOphelimus eucalypti Gahan, and on examining the effect of crossing between eucalyptus species on the development possibilities of the wasps. Also considered were the effect of the food on adult survival, the competition between the eulophid gall makerLeptocybe invasa Fisher & LaSalle andO. maskelli, the heavy damage inflicted on eucalyptus, and the health problems and nuisance to people caused by the wasp near heavily infested trees during the mass emergence of adults.
The increase of insect pests inEucalyptus
  • G Viggiani
  • S Laudonia
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