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Presence of the Eucalyptus gall wasp Ophelimus maskelli
and its parasitoid Closterocerus chamaeleon in Portugal:
First record, geographic distribution and host preference
Manuela Branco & Conceição Boavida &
Nicolas Durand & José Carlos Franco & Zvi Mendel
Received: 18 December 2007 /Accepted: 6 October 2008 /Published online: 7 January 2009
Springer Science + Business Media B.V. 2008
Abstract The Eucalyptus gall wasp Ophelimus
maskelli (Hymenoptera: Eulophidae) and its par-
asitoid Closterocerus chamaeleon (Hymenoptera:
Eulophidae) were observed for the first time in
Portugal, in 2006 and 2007, respectively. Data on
the distribution of O. maskelli in Portugal, differences
in the susceptibility of two host species, Eucalyptus
globulus and Eucalyptus camaldulensis, and parasitism
by C. chamaeleon are given.
Keywords Eucalyptus camaldulensis
Ophelimus maskelli (Ashmead) (Hymeno ptera: Eulo-
phidae) is a gall wasp causing damage on Eucalyptus
species. It induces numerous small pimple-like, nearly
round galls visible on both sides of the leaf (Protasov
et al. 2007b). In Israel its population produces three
generations per year, between spring and the end of
fall, the duration of the entire gall development being
80–90 days (Protasov et al. 2007b). In Europe, the wasp
was first recorded, in Italy in 2000, misidentified as O.
eucaly pti (Arzone and Alma 2000; Viggiani and
Nicotina 2001). Later, it was detected in the south of
Spain in 2003 (Sánchez 2003), in the northeast of
Spain in 2004 (Pujade-Villar and Riba-Flinch 2004),
and in the south of France in 2005 (European and
Mediterranean Plant Protection Organization 2006). No
signs of its presence were observed during intensive
surveys carried out in 2003 and 2004 in Portugal in
order to detect Eucalyptus gall wasps (Branco et al.
2006) when the only wasp species found was
Leptocybe invasa Fisher & LaSalle (Hymenoptera:
Eulophidae). Ophelimus maskelli was first detected in
April 2006, near Lisbon, on Eucalyptus camaldulensis
(M. Branco, unpublished data).
Eucalyptus globulus and E. camaldulensis are the
major Eucalyptus species in the Iberian Peninsula;
other species are seldom found. The main Eucalyptus
forests are based on E. globulus. Eucalyptus camal-
dulensis is mostly used in leisure, roadside and urban
areas. Due to the importance of these two Eucalyptus
Phytoparasitica (2009) 37:51–54
J. C. Franco
Centro de Estudos Florestais, Instituto Superior
Agronomia, Universidade Técnica de Lisboa,
Tapada da Ajuda,
1349-017 Lisbon, Portugal
Instituto Nacional de Recursos Biológicos,
Ministério da Agricultura,
Desenvolvimento Rural e Pescas,
Edifício 1, Tapada da Ajuda,
1349-017 Lisbon, Portugal
Department of Entomology, ARO, The Volcani Center,
Bet Dagan 50250, Israel
M. Branco (*)
Departamento de Engenharia Florestal,
Instituto Superior Agronomia,
Universidade Técnica de Lisboa,
Tapada da Ajuda,
1349-017 Lisbon, Portugal
species, a monitoring program was designed to survey
the distribution of O. maskelli in Portugal, and to
confirm the susceptibility of E. globulus and E.
camaldulensis to this wasp, as reported by Protasov
et al. (2007a) in Israel. Unexpectedly, during this
survey, the parasitoid Closterocerus chamaelon Girault
(Hymenoptera: Eulophidae) was found among the
wasps emerging from O. maskelli -infested leaves
parasitoid was identified according to Protasov et al.
(2007a). This species was first collected in Australia
(Mendel et al. 2007;Protasovetal.2007a), and
imported and released in Israel, in 2005 and 2006
(Mendel et al. 2007; Protasov et al. 2007a), and to Italy
in 2006 (Laudonia et al. 2006), for biological control
of O. maskelli.
In this paper, the geographical distribution of O.
maskelli is reported together with the spontaneous
occurrence of C. chamaeleon in Portugal. Information
on differences in host plant susceptibility and prelim-
inary results on parasitoid activity are presented.
In spring 2007, a coun trywide survey of E.
globulus and E. camaldulensis trees was carried out
on 23 locations to detect the presence of O. maskelli.
At each location five to ten trees were inspected by
observing at least five branches on each and the
presence of the typical galls induced by the wasp was
In September 2007, O. maskelli-infested leaves were
collected on two occasions in an E. camaldulensis
coppice, in Lisbon, in order to develop a rearing
procedure in the laboratory. The leaves were chosen
among those having fully developed galls and left in
containers for one month, before counting the emerged
In October/November 2007, samples were collected
from infested trees of both E. globulus and E.
camaldulensis, in two locations, Lisbon and Peninsula
of Setúbal, about 60 km south of Lisbon, to assess
differences in susceptibility between host plant species.
Seven E. camaldulensis and eight E. globulus trees
were randomly sampled from the same stand in each
location. Six 40–50-cm-long branches were randomly
collected per sampled tree, using telescopic pruning
scissors, and placed in separate labeled plastic bags.
Each sample was observed in the laboratory to
determine its infestation level using the following
notation: class 0—leaves with no O. maskelli galls;
class 1—leaves with one to 40 galls/leaf; class
—leaves with more than 40 galls/leaf. An ANOVA
was used to test the effects of Eucalyptus species on
the percentage of leaves on each infestation class
applied by General Linear Model procedure (SPSS
version 15 software). Arcsine transformation was used
to stabilize variance. Separate analyses were performed
for each infestation class. Species effects were tested
by simple contrast.
The susceptibility of the two Eucalyptus species to
O. maskelli was evaluated also based on gall size. A
sample of 30 galls per each tree species was collected
from different leaves and their diameter was mea-
sured. Differences between plant species were com-
pared by using a t-test on untransformed data.
Fig. 1 Distribution of Ophelimus maskelli in Portugal in 2007,
based on the presence of typical leaf galls in two Eucalyptus
species: (closed stars) E. camaldulensis with galls; (open stars)
E. camaldulensis with no signs of galls; (closed dots) E.
globulus with galls; (open dots) E. globulus with no signs of
52 Phytoparasitica (2009) 37:51–54
The emergences of O. maskelli and its parasitoid
C. chamaeleon were assessed in infested leaf samples
of E. camaldulensis collected in the middle part of the
same branches used to assess the infestation level s of
O. maskelli in the two locations referred to before
(October/November 2007). No samples were collect-
ed from E. globulus because of its very low level of
infestation by O. maskelli. In the laboratory the leaves
were examined and the number of galls without wasp
emergence holes was counted per leaf and considered
as the number of suitable galls available for para-
sitisation by C. chamaeleon close to the sampling
date. Galls with emergence hole were not considered
since it was not possible to know whether it was the
galler or the parasitoid that emerged from them. The
samples were kept in containers in the laboratory, at
room conditions for one month and the emerged
wasps were collected and counted every week.
The survey conducted in Portugal in 2007 show ed
that O. maskelli was present in 12 out of 23 sites,
mainly in two areas, the South, near the border with
Spain, and the Centre, near Lisbon (Fig. 1). During
this field survey, the gall wasp was mainly observed
in E. camaldulensis (Fig. 1). In agreement, the
percentage of infested leaves (classes 1 and 2) in E.
camaldulensis was significantly higher (F
p<0.001 and F
=103.5; p<0.001, respectively)
than in E. globulus (Fig. 2) while the percentage of
leaves with no galls was significantly higher (F
146.6, p<0.001) in E. globulus (about 70%), compared
to E. camaldulensis (about 20%). Gall mean diameter
(±SE) was significantly smaller in E. globulus (0.88±
0.037 mm), and most of these galls showed no wasp
emergence, in comparison with E. camaldulensis
(1.42±0.051 mm; t=8.58; df=58; p<0.001).
Closterocerus chamaeleon was found in Portugal
for the first time in the beginning of September 2007
in leaf samples infested with O. maskelli galls
collected from E. camaldulensis showing 51.5–
63.5% of parasitism (Table 1). The mean number of
galls/leaf (±SE) was 155.3±14.9. Later, in October/
November 2007, almost only the parasitoid wasps
emerged from the galls collected in the survey and
both O. maskelli and C. chamaeleon emerged in very
few numbers from the samples (Table 1).
According to the sur vey reported previously
(Branco et al. 2006), O. maskelli invaded Portugal
between 2004 and 2006, probably from the south of
Spain, where it was observed in 2003 (Sánchez 2003).
However, no previous reports exist confirming the
presence of C. chamaeleon in the western Medi terra-
nean Region and Napoli (in Italy), about 2,700 km
from Lisbon, seems to be the nearest area where this
parasitoid had been released (Laudonia et al. 2006).
Closterocerus chamaeleon has several biological
traits that favor population increase and spread to
new zones, such as thelytoky, high fecundity, short
generation time, and in particular the relatively high
Fig. 2 Percentage of galled leaves of Eucalyptus camaldulensis
and Eucalyptus globulus by Ophelimus maskelli according to
three classes of leaf gall density: 0—no galls, 1—fewer than 40
galls per leaf, 2—more than 40 galls per leaf. Bars capped
with the same letter in each class are not significantly
different (P <0.001)
Table 1 Cumulative emergences of Ophelimus maskelli and its parasitoid, Closterocerus chamaeleon, from leaves of Eucalyptus
camaldulensis collected in 2007 in Lisbon and Peninsula of Setubal, Portugal
Date and location Number
O. maskelli C. chamaeleon Percent galls with emergence
of C. chamaeleon
September, Lisbon 10 1,104 398 701 63.5
16 2,588 1,245 1,333 51.5
October, Lisbon 28 4,349 0 1,838 42.3
November, Setubal 40 8,453 55 810 9.6
Phytoparasitica (2009) 37:51–54 53
adult longevity coupled with its very small size, which
favors dispersal by wind (Protasov et al. 2007a). In
Israel, the parasitoid spread 120 km in one year
(Mendel et al. 2007; Protasov et al. 2007a). In Turkey,
a population of C. chamaeleon found in January 2007
is thought to have originated from individuals dispersed
from the population released in Israel, approximately
1,500 km away (Doganlar and Mendel 2007). The
greatest dispersal distances traveled by released para-
sitoids have been reported a s 150 km per year
(Godfray 1993). However, spread rates may be much
higher, reaching 100 to 300 km per day, when transport
by prevailing winds occu rs (Farrow 1981). Hence it
might be possible that this parasitoid is established
in southwestern Mediterranean taking advantage of
the high population densities of its host on E.
camaldulensis in the area.
Although E. globulus is a suitable host-plant species
for O. maskelli as indicated by Protasov et al. (2007b),
the present results provide evidence that its suscepti-
bility is much lower compared to E. camaldulensis.
This is to be predicted by differences in gall density
and gall size, which were both significantly lower in E.
globulus. In particular, gall size is an important
predictor of galler survival and therefore of its fitness
(Stone and Schönrogge 2003). According to the
present finding, host-plant genotype may have a
significant impact on gall size for this galler–host plant
system. The data also predict significant differences in
gall density between trees within species, evidencing
intraspecific variability to O. maskelli within these two
Closterocerus chamaeleon was reared from all leaf
samples infested with O. maskelli. The mean percent-
age of parasitoid emergences from O. maskelli galls in
collected leaf samples varied between 63.5% in
September and 9.6% in November. This value refers
to emergences observed during one month and may
reflect successful parasitization that occurred just
before the collection of samples. In the beginning of
September, when C. chamaeleon was first collected,
the host-to-parasitoid ratio was close to 1:1. Later on,
this ratio decreased markedly in favor of the parasit-
oid, since very few emergences of the gall wasp
occurred. This pattern indicates that the parasitoid may
remain active in the field for longer periods than the
host species. Host and parasitoid phenologies need to
be investigated throughout the year, in order to
understand the distributions observed in field samples.
Acknowledgments Thanks are due to João Barrento, Ana
Raquel Reis and Helena Santos for their help in the field
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