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First record in Algeria of two eulophid wasps: Closterocerus chamaeleon (Girault) and its host, the Eucalyptus Gall Wasp Ophelimus maskelli (Ashmead)

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The endophagous parasitoid Closterocerus chamaeleon, released in Israel, Italy and Corsica, for classical biological control programs, and its host, the gall-maker Ophelimus maskelli, were recorded for the first time in Algeria, in a straight line 450 km far from the Sardinian release site and 700 km far from the closest Sicilian release site. Their presence is confirmed in Andalucia (Spain), about 2000 km far from release sites of Sicily and Campania. In about two years the parasitoid spread and established in many Mediterranean countries. RIASSUNTO Prima segnalazione in Algeria di due imenotteri eulofidi: Closterocerus chamaeleon (Girault) e il suo ospite, il galligeno dell'eucalipto Ophelimus maskelli (Ashmead). Il parassitoide endofago C. chamaeleon, introdotto in programmi di controllo biologico in Israele, Italia e Corsica nel 2005-2007, e il suo ospite O. maskelli, entrambi originari dell'Australia, sono stati ritrovati per la prima volta in Algeria, a Béjaïa, città distante in linea d'aria 450 km dal sito di rilascio in Sardegna e 700 km dal più vicino sito di rilascio in Sicilia. Si conferma la presenza dei due eulofidi in Andalusia (Spagna), a circa 2000 km dai siti di rilascio del parassitoide in Sicilia e Campania. In circa due anni il parassitoide si è diffuso ed acclimatato in molte aree del Mediterraneo.
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Naturalista sicil., S. IV, XXXIV (1-2), 2010, pp. 201-206
VIRGILIO CALECA
FIRST RECORD IN ALGERIA OF TWO EULOPHID WASPS:
CLOSTEROCERUS CHAMAELEON (GIRAULT) AND ITS HOST, THE
EUCALYPTUS GALL WASP OPHELIMUS MASKELLI (ASHMEAD)
(Hymenoptera Eulophidae)
SUMMARY
The endophagous parasitoid Closterocerus chamaeleon, released in Israel, Italy and Corsica, for
classical biological control programs, and its host, the gall-maker Ophelimus maskelli, were record-
ed for the first time in Algeria, in a straight line 450 km far from the Sardinian release site and 700
km far from the closest Sicilian release site. Their presence is confirmed in Andalucia (Spain), about
2000 km far from release sites of Sicily and Campania. In about two years the parasitoid spread and
established in many Mediterranean countries.
RIASSUNTO
Prima segnalazione in Algeria di due imenotteri eulofidi: Closterocerus chamaeleon (Girault) e
il suo ospite, il galligeno dell’eucalipto Ophelimus maskelli (Ashmead). Il parassitoide endofago C.
chamaeleon, introdotto in programmi di controllo biologico in Israele, Italia e Corsica nel 2005-2007,
e il suo ospite O. maskelli, entrambi originari dell’Australia, sono stati ritrovati per la prima volta in
Algeria, a Béjaïa, città distante in linea d’aria 450 km dal sito di rilascio in Sardegna e 700 km dal più
vicino sito di rilascio in Sicilia. Si conferma la presenza dei due eulofidi in Andalusia (Spagna), a circa
2000 km dai siti di rilascio del parassitoide in Sicilia e Campania. In circa due anni il parassitoide si
è diffuso ed acclimatato in molte aree del Mediterraneo.
INTRODUCTION
The eulophid gall wasp Ophelimus maskelli (Ashmead) (Hymenoptera
Eulophidae) living on Eucalyptus L’Heritier has been accidentally introduced
in the Mediterranean region; it was recorded in Italy, as Ophelimus eucalypti
(Gahan) (ARZONE & ALMA, 2000; VIGGIANI & NICOTINA 2001), as Ophelimus
prope eucalypti (Gahan) (BELLA & LOVERDE, 2002) and as Ophelimus sp.
(BAGNOLI & ROVERSI, 2004); in the meanwhile it was recorded in other
Mediterranean countries (Spain: SANCHEZ, 2003; Israel: MENDEL et al., 2005;
Greece: KAVALLIERATOS et al., 2006; France: EPPO, 2006; Turkey: DOGAN-
LAR &MENDEL, 2007; Portugal: BRANCO et al., 2009; Tunisia: DHAHRI et al.,
in press). Until now no paper records O. maskelli from Algeria, while anoth-
er eulophid gall-maker on Eucalyptus,Leptocybe invasa Fisher et LaSalle, was
here collected since 2002 (MENDEL et al., 2004).
O. maskelli causes galls on the leaf surface, showing a clear preference
for Eucalyptus camaldulensis Dehnh.; leaves bearing more than 50 galls live
considerably less than leaves without galls, dropping early (PROTASOV et al.,
2007a). Furthermore, the huge number of newly emerged wasps could induce
allergic reactions and other health problems (BAGNOLI &ROVERSI, 2004;
MENDEL et al., 2005; LAUDONIA et al., 2006; PROTASOV et al., 2007a).
In 2003 the Volcani Center of Bet Dagan (Israel) and the CSIRO of Can-
berra (Australia) began a biological control program to search natural enemies
of O. maskelli in Australia for their possible introduction. In 2005 Closterocerus
chamaeleon (Girault) (Hymenoptera Eulophidae), a uniparental parasitoid
species ovipositing in larvae, pupae and unemerged adults (VIGGIANI et al.,
2008), was introduced in Israel together with an oophagous parasitoid,
Stethynium ophelimi Huber (Hymenoptera Mymaridae) (MENDEL et al., 2007;
PROTASOV et al., 2007b). In 2006 Prof. Zvi Mendel (Volcani Center) kindly sent
leaves with galls parasitized by C. chamaeleon, and in April-May of the same
year the eulophid parasitoid was released in Campania (LAUDONIA et al., 2006)
and in five Sicilian sites (RIZZO et al., 2006); in December 2006 it was also
released in Calabria and Sardinia (CALECA et al., 2009). In few months C.
chamaeleon became established in all release sites, showing a remarkable dis-
persal rate (RIZZO et al., 2006, 2007; DEMARZO, 2007; SASSO et al., 2008; CALE-
CA et al., 2009), reaching Turkey from Israel (DOGANLAR &MENDEL, 2007).
Considering the quick spread of the parasitoid I tried to record whether
it also reached areas far from Sicilian release sites, through occasional col-
lecting of eucalyptus leaves in Algeria and Andalucia (Spain).
MATERIALS AND METHODS
At beginning of March 2008 I asked to Farid Aboud, Algerian PhD stu-
dent in the University of Palermo, about the possibility to collect some euca-
lyptus galled leaves in Algeria. On 17th March 2008 Aboud’s friend Salim
Ouchemoukh collected in the surroundings of the city of Béjaïa (Algeria,
202 V. CALECA
36°45’23”N, 05°04’00”E) about 200 leaves of E. camaldulensis bearing galls
caused by O. maskelli.
Additionally, on 10th May 2008 Prof. Maria Antonietta Germanà kindly
collected some galled leaves of E. camaldulensis, during a visit to Alcazar de
los Reyes Cristianos in Cordoba (Andalucia, Spain; 37°52’37.13”N,
04°46’56.92”W).
The collected material was maintained sealed to avoid any possible acci-
dental introduction of arthropods from those countries into Italy. At their
arrival in Palermo the leaves were placed in polyethylene transparent plastic
bags with a thin cotton cloth as cover to allow transpiration and to avoid an
excess of moisture; they were maintained at room temperature for one month
to allow the exit of gall makers and parasitoids. Afterwards, all galls were dis-
sected to identify adults not emerged, still inside the galls.
Parasitoids and gall makers were identified through specific characters
provided by PROTASOV et al. (2007a, 2007b).
RESULTS
Algeria
Galled leaves collected in Béjaïa were 196 and contained 1281 galls, with
6.5 ± 7.1 galls per leaf, whose 59% was already pierced by emerged wasps.
Because of the poor condition of leaves only 2 C. chamaeleon emerged,
but through the dissection of galls without exit holes 212 adults of O. maskel-
li and 4 adults of C. chamaeleon were recorded inside these leaves.
To my knowledge this is the first record in Algeria for both the parasitoid
and its gall-maker host.
Spain
Galled leaves collected in Cordoba were 7 and contained 647 galls, with
92.4 ± 161.6 galls per leaf, whose 86% was already pierced by emerged wasps.
From these leaves 3 adults of C. chamaeleon emerged; through the dis-
section of galls without exit holes other 11 adults of the parasitoid and 15
adults of O. maskelli were recorded inside the leaves.
These data confirm the establishment of C. chamaeleon recorded in
Andalucia by BORRAJO et al. (2008) in February 2008.
DISCUSSION
The record of the eulophid gall-maker O. maskelli is the first for Alge-
ria, but its arrival probably occurred some years before 2008.
203First record in Algeria of two eulophid wasps: Closterocerus chamaeleon...
Fig. 1 — Known distribution of C. chamaeleon in the Mediterranean region.
V. CALECA
204
The first record of the eulophid parasitoid C. chamaeleon in Algeria, in
a straight line 450 km far from the release site in Sardinia (CALECA et al., 2009)
and 700 km far from the closest Sicilian release site of Santa Ninfa (RIZZO et
al., 2006), is another evidence of the astonishing spread in the Mediterranean
region of this introduced parthenogenetic wasps. Its adult winter activity and
its long life as adult (RIZZO et al., 2006; PROTASOV et al., 2007b; SASSO et al.,
2008) facilitated its spread, probably also by means of transport accidentally
carrying some wasps. After its introduction in Israel ((MENDEL et al., 2007;
PROTASOV et al., 2007b), Italy (LAUDONIA et al., 2006; RIZZO et al., 2006;
CALECA et al., 2009) and Corsica (MENDEL,pers. comm.), C. chamaeleon is
now established in all release sites and reached Turkey (DOGANLAR &
MENDEL, 2007), several Italian regions (DEMARZO, 2007; BAGNOLI,pers.
comm., LOVERDE,pers. comm.), Spain (BORRAJO et al., 2008), Portugal
(BRANCO et al., 2009), Tunisia (LOVERDE et al., 2010) and Algeria (present
study) (Fig. 1); it is quite obvious to suppose its spread in all areas of the
Mediterranean region where O. maskelli occurs.
Acknowledgements — I wish to thank Salim Ouchemoukh and Farid Aboud for the collec-
tion of leaves in Béjaïa, Maria Antonietta Germanà for the collection of leaves in Cordoba, and
Bruno Massa for the critical revision of the manuscript.
First record in Algeria of two eulophid wasps: Closterocerus chamaeleon... 205
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Author’s address — V. CALECA, Dipartimento di Scienze Entomologiche, Fitopatologiche,
Microbiologiche agrarie e Zootecniche (SENFIMIZO), Università degli Studi di Palermo, viale delle
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206 V. CALECA
... Для Ближнего Востока O. maskelli впервые указан из Израиля в 2003 г. [33], в Турции выявлен в 2006 г. [18], в Иордании -в 2012 г. [21], в Сирии -в 2014 г. [37], в Ираке -в 2016 г. [25]. Для Африканского континента указан из Марокко по находкам, сделанным в 2002 г. [24], в Тунисе известен с 2006 г. [17], в Алжире -с 2008 г. [15], в Эфиопии -с 2017 г. [9]. Завезён в Южную Америку, где выявлен в Чили в 2003 г. и в Аргентине в 2013 г. [7], в 2014 г. был зарегистрирован в Северной Америке на территории США в Калифорнии [14]. ...
... При массовом развитии O. maskelli степень поражённости растений может достигать нескольких сотен галлов/лист. Например, в Испании степень поражённости E. camaldulensis достигала 647 галлов/лист, составляя в среднем 92,4 ±161,6 галла/лист [15], на Сицилии для этого же кормового растения было зарегистрировано развитие 158 галлов/лист [28], в Израиле -133,5 ±98,7 [33], в Алжире -6,5 ±7,1 [15]. ...
... При массовом развитии O. maskelli степень поражённости растений может достигать нескольких сотен галлов/лист. Например, в Испании степень поражённости E. camaldulensis достигала 647 галлов/лист, составляя в среднем 92,4 ±161,6 галла/лист [15], на Сицилии для этого же кормового растения было зарегистрировано развитие 158 галлов/лист [28], в Израиле -133,5 ±98,7 [33], в Алжире -6,5 ±7,1 [15]. ...
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... In the following thirty-years, three other Ophelimus species invaded different areas worldwide: O. maskelli Ashmead, and two undescribed species. Among these, O. maskelli is the most widely distributed (Mansfield, 2016), being present in the Mediterranean Basin and North America (Branco et al., 2009;Burks et al., 2015;Caleca, 2010;Dhahri et al., 2010;Protasov et al., 2007a). Eucalyptus camaldulensis and E. tereticornis, both belonging to section Exertaria, are their main host species Hill, 2004;Protasov et al., 2007a). ...
... This parasitoid was also released in Italy, imported from Israel (Caleca et al., 2009;Rizzo et al., 2006). It rapidly dispersed across the Mediterranean basin, including Portugal (Borrajo et al., 2008;Branco et al., 2009;Caleca, 2010;Doganlar and Mendel, 2007;Lo Verde et al., 2010), and established in the entire region, efficiently controlling O. maskelli (Branco et al., 2009;Caleca et al., 2011;Mendel et al., 2017). ...
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Ophelimus sp. (Hym: Eulophidae) is an Australian gall wasp newly found in Southern Europe forming galls on Eucalyptus globulus. A congeneric gall wasp O. maskelli, also established in the Mediterranean Basin, is currently controlled by the introduced parasitoid Closterocerus chamaeleon. To date, no parasitism was observed on Ophelimus sp. by C. chamaeleon. Here we analyze a possible escape from parasitism through an asynchronous life cycle in this host-parasitoid system. The ability of C. chamaeleon to oviposit and complete development on Ophelimus sp. was determined, both in laboratory and field experiments. Ophelimus sp. showed to be univoltine, with winter larval development and possible summer egg diapause, contrasting with the multivoltine behavior of O. maskelli, which completes 3–4 generations per year. Concomitantly, C. chamaeleon is normally collected in the field from May to October. In laboratory, under low temperatures (15 ± 1 °C), adults of the parasitoid could survive up to four months. Both old (86–89 days) and young (< 16 days) parasitoid females showed similar parasitism behavior. Naïve parasitoid females oviposited in both O. maskelli (on E. camaldulensis) and Ophelimus sp. (on E. globulus), with no apparent preference between the two host species. We observed parasitism, when we exposed adults of C. chamaeleon to bagged eucalypt leaves infested with Ophelimus sp. galls, in field conditions. Altogether, our results demonstrate that C. chamaeleon is able to oviposit and complete development in Ophelimus sp. However, in field conditions, the lack of parasitism is possibly due to life cycle asynchrony between the parasitoid and the gall wasp.
... Las especies asiáticas y americanas de Ulmus en ensayos de laboratorio han demostrado ser también susceptibles a este crisomélido como huésped potencial, siendo Ulmus wilsoniana L. la única opción para evitar el ataque en espacios verdes urbanos (Hall y Young, 1986;Hall y Townsend, 1987). De las dos especies de cochinillas encontradas, Kermes vermilio (antiguamente utilizada para la extracción de colorante natural) se alimenta sólo sobre encina (Quercus ilex L.) y coscoja (Quercus coccifera L.) (Pellizzari et al., 2012) (Valente y Hodkinson, 2009;Dhahri et al., 2010;Caleca, 2010). ...
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La entomofauna de los espacios verdes urbanos es poco conocida aun siendo reservorio de insectos plaga y beneficiosos. Este estudio tiene como principal objetivo catalogar los insectos plaga y sus potenciales enemigos naturales con el propósito de facilitar información para un correcto manejo integrado de este ecosistema ajardinado. Se realizaron muestreos durante 6 meses que dieron como resultado el registro de interacciones entre niveles tróficos así como la identificación de 69 especies, 53 insectos fitófagos potencialmente plaga o polinizadores pertenecientes a 7 órdenes y 28 familias (áfidos, trips, coleópteros, cochinillas, psílidos, aleuródidos, àpidos, minadoras de hojas y frutos… ), 2 especies de ácaros potencialemente plaga así como 14 enemigos naturales, depredadores o parasitoides, pertenecientes a 5 órdenes y 8 familias. Podemos concluir que la entomofauna fitófaga se encuentra bien controlada, en general, por sus enemigos naturales y que participan en una amplia red de interacciones tritróficas: planta-fitófago-enemigo natural cuyo conocimiento es crucial para el establecimiento de estrategias acertadas de control integrado de plagas en estos ecosistemas urbanos donde el uso de productos fitosanitarios está cada día más restringido.
... Currently, a few of these invasive gall wasp species are distributed worldwide. The red gum gall wasps Leptocybe invasa Fisher & La Salle and Ophelimus maskelli (Ashmead) (Hymenoptera Eulophidae) both became established in the Mediterranean Basin during the last 15 years (Caleca, 2010;Mendel et al., 2004;Protasov et al., 2007a;Nicotina, 2001) and are currently also present in North America, Asia and South Africa (Burks et al., 2015a,b;Hurley, 2014). Leptocybe invasa was first described in Israel in 2000 (Mendel et al., 2004). ...
... En situation de forte attaque, la croissance des plants est compromise (Mendel et al. 2004). Une autre espèce, Ophelimus maskelli Ashmead 1900 (Hymenoptera : Eulophidae), a été découverte pour la première fois en Italie en 1999 (Arzone & Alma 2000) et elle a également rapidement colonisé plusieurs pays méditerranéens (Branco et al. 2006;Doğanlar & Mendel 2007;Protasov et al. 2007;Caleca 2010 (Valente & Hodkinson 2009). Certains auteurs rapportent que les dégâts causés par cette espèce s'avèrent plus dramatiques que ceux des autres gallicoles, avec des défoliations totales des arbres, comme cela a été observé en Amérique du Nord (Brennan & Gill 1999). ...
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Eco-ethology of new invasive pest species on eucalyptus plantation of Morocco. In the last decade, three invasive insect pests have been discovered in the Moroccan eucalyptus stands (Gharb region). Leptocybe invasa Fisher & La Salle 2004 (Hymenoptera: Eulophidae) has been detected in 2002, while the two others, Ctenarytaina eucalypti (Maskell 1890) and Glycaspis brimblecombei Moore 1964 (Hemiptera: Psyllidae), have been observed in 2008 and 2009, respectively. Only one parasitoid of L. invasa, Megastigmus sp. (Chalcidoidea: Torymidae), was identifi ed in 2009. The dynamics of L. invasa and its field infestation rate were followed since 2008, in eucalyptus plantation in the Gharb Region. Some bio-ecological parameters and control strategies of these new pests are reviewed and discussed.
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Gall pests have caused seriously damage to eucalyptus in recent years in China. In this study, we collected and identified the invaded eucalyptus gall wasp Ophelimus maskelli and its parasitoid Closterocerus chamaeleon for the first time in China. O. maskelli induced two types of gall shape, i.e., blister- and neoplastic-shaped galls. The blister-shaped galls were most likely induced on leaves rather on petioles and stems, while the neoplastic-shaped galls were more frequently found on petioles rather than on leaves and stems. We find that of the four solar orientations, O. maskelli significantly preferred to colonize Eucalyptus trees in the sunnier areas in south over that in west and north with significantly lower gall infestation rate detected in east. The parasitism rate of C. chamaeleon increased from 23.4% in February to 97.4% in March 2023 when the population of O. maskelli galls was low (236.8–251.4 galls/20 branches); however, when gall population increased to a high level (≈ 450 galls/20 branches), the parasitism rate significantly decreased to 26.5% in April, although it raised to 62.6% again in May. Our findings deliver insigne into development of biological control programs of O. maskelli using C. chamaeleon .
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Des galles foliaires causant de graves dégâts ont été observées sur Eucalyptus camaldulensis dans la région du Gharb-Maâmora au cours de l'année 2002. Celles-ci sont causées par Ophelimus maskelli (Ashmead) (Hymenoptera: Eulophidae) signalé pour la première fois au Maroc. Depuis, cet organisme nuisible s'est propagé à d'autres peuplements d'eucalyptus à l’échelle nationale. Au cours des investigations menées sur le terrain, les auteurs ont observé que les degrés d'infestation d'Eucalyptus camaldulensis diffèrent d'une région à l'autre et ont été classés sur une échelle à 3 niveaux : faible, modéré ou élevé. L’étude du cycle biologique de l'insecte sur le terrain et en laboratoire a révélé la présence de deux générations par an. Ce travail a permis de constater que Closterocerus chamaeleon (Hymenoptera: Eulophidae), parasitoïde utilisé avec succès dans d'autres pays de la region OEPP comme agent de lutte biologique, est présent au Maroc. Le taux de parasitisme observé s'est avéré très élevé ce qui pourrait expliquer le peu de dégâts actuellement causés par l'organisme nuisible gallicole O. maskelli sur l'Eucalyptus camaldulensis au Maroc.
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SUMMARY Closterocerus chamaeleon (Girault) (Hymenoptera Eulophidae), parasitoid of the Eucalyptus gall wasp Ophelimus maskelli (Ashmead) (Hymenoptera Eulophidae) has been recorded for the first time in Tunisia in July 2007. This record suggests that 14 months after its release in Sicily, in May 2006, it has spread over Sicily Channel. RIASSUNTO Ritrovamento in Tunisia di Closterocerus chamaeleon (Girault) (Hymenoptera Eulophidae), parassitoide dell’eulofide galligeno dell’eucalipto Ophelimus maskelli (Ashmead) (Hymenoptera Eulophidae). Viene segnalata per la prima volta la presenza di Closterocerus chamaeleon (Girault) (Hymenoptera Eulophidae), parassitoide dell’eulofide galligeno dell’eucalipto Ophelimus maskelli (Ashmead) (Hymenoptera Eulophidae). Il parassitoide era stato introdotto in Sicilia nel maggio 2006, diffondendosi rapidamente in tutta l’isola nei successivi 18 mesi. Il suo ritrovamento in Tuni- sia indica che 14 mesi dopo il rilascio nell’isola C. chamaeleon aveva già superato il Canale di Sicilia, raggiungendo le coste del Nord Africa.
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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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Dhahri, S., Ben Jamaa, M. L., and Lo Verde, G. 2010. First record of Leptocybe invasa and Ophelimus maskelli eucalyptus gall wasps in Tunisia. Tunisian Journal of Plant Protection 5: 231- 236. Two Australian gall wasps were detected for the first time in Tunisia on the foliage of Eucalyptus camaldulensis trees. Leptocybe invasa was detected in 2004, while Ophelimus maskelli in 2006. L. invasa makes galls on petioles, leaf midribs and young branches whereas O. maskelli induces galls on limbs. Vigilance is recommended when seedlings are carried to plantation.