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Dispersal rate and parasitism by Closterocerus chamaeleon (Girault) after its release in Sicily to control Ophelimus maskelli (Ashmead) (Hymenoptera, Eulophidae)


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Spread of the exotic parasitoid Closterocerus chamaeleon (Girault) and its parasitism on the Eucalyptus gall wasp Ophelimus maskelli (Ashmead) (Hymenoptera, Eulophidae) were studied in Sicily after C. chamaeleon introduction in May 2006. Parasitoid spread was evaluated by sampling sites at increasing distances from the five release sites. C. chamaeleon quickly established and spread; within 5months, it caused 62% parasitism at release sites and 38% parasitism at sites 2km from release sites. One year after its introduction (spring 2007), C. chamaeleon was detected more than 50km distant from release sites. By winter 2007–08, the parasitoid was recovered throughout Sicily and in many surrounding islets, with parasitism rates always >65% and usually at 100%. The dispersal rate was 0.15km/month in the 2months after release. It increased to 0.6km/month in the next 3months, reaching 7.5km/month 5–7months after release and 20km/month in the following 11months, when the entire island was colonized. The pattern of spread followed the spread latency model of biological invasions; the spread latency period was very short because of the parasitoid’s biological characteristics and a favourable environment. Parasitism trends differed between suburban and afforested sites, showing a longer spread latency period in the afforested sites due to the greater extent of potentially colonisable area. The parasitoid’s use of continuous and long-distance dispersal mechanisms enabled it to rapidly colonize even very distant regions and enhances its effectiveness as a biological control agent.
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Dispersal rate and parasitism by Closterocerus chamaeleon (Girault)
after its release in Sicily to control Ophelimus maskelli (Ashmead)
(Hymenoptera, Eulophidae)
Virgilio Caleca
, Gabriella Lo Verde, Maria Concetta Rizzo, Roberto Rizzo
Department of Entomological, Phytopathological, Microbiological and Animal Sciences (S.En.Fi.Mi.Zo.), Entomology, Acarology and Zoology Section, Agriculture
Faculty, University of Palermo, viale delle scienze, 90128 Palermo, Italy
article info
Article history:
Received 13 July 2010
Accepted 21 December 2010
Available online 30 December 2010
Closterocerus chamaeleon
Ophelimus maskelli
Eucalyptus gall wasp
Parasitoid introduction
Dispersal strategy
Parasitism level
Spread of the exotic parasitoid Closterocerus chamaeleon (Girault) and its parasitism on the Eucalyptus gall
wasp Ophelimus maskelli (Ashmead) (Hymenoptera, Eulophidae) were studied in Sicily after C. chamae-
leon introduction in May 2006. Parasitoid spread was evaluated by sampling sites at increasing distances
from the five release sites. C. chamaeleon quickly established and spread; within 5 months, it caused 62%
parasitism at release sites and 38% parasitism at sites 2 km from release sites. One year after its introduc-
tion (spring 2007), C. chamaeleon was detected more than 50 km distant from release sites. By winter
2007–08, the parasitoid was recovered throughout Sicily and in many surrounding islets, with parasitism
rates always >65% and usually at 100%. The dispersal rate was 0.15 km/month in the 2 months after
release. It increased to 0.6 km/month in the next 3 months, reaching 7.5 km/month 5–7 months after
release and 20 km/month in the following 11 months, when the entire island was colonized. The pattern
of spread followed the spread latency model of biological invasions; the spread latency period was very
short because of the parasitoid’s biological characteristics and a favourable environment. Parasitism
trends differed between suburban and afforested sites, showing a longer spread latency period in the
afforested sites due to the greater extent of potentially colonisable area. The parasitoid’s use of continu-
ous and long-distance dispersal mechanisms enabled it to rapidly colonize even very distant regions and
enhances its effectiveness as a biological control agent.
!2010 Elsevier Inc. All rights reserved.
1. Introduction
Because of their adaptability to dry climates and rapid growth
rates, Eucalyptus spp. are among the most common plantation
trees in the Mediterranean Basin (FAO, 1979). Eucalypts were
introduced into Italy in the 19th century and were primarily used
as a source of essential oils (Moggi and Giordano, 1957). In the
20th century and especially in the 1950s, 1960s, and 1970s, euca-
lypts were extensively planted in Sicily, usually in large forest
plantations, to provide wood for paper mills or to prevent soil
erosion. Eucalypts are also commonly planted along roads
(Barbera et al.,2001). Sicilian Eucalyptus plantations currently
occupy 35,664 ha (Saporito, 2004) and mostly contain Eucalyptus
camaldulensis Dehnh., Eucalyptus globulus Labill., and to a lesser
degree, Eucalyptus occidentalis Endl. and Eucalyptus gomphocephala
DC. (La Mantia et al., 2000; Saporito, 2004). Interest in using
eucalypts to produce plant biomass for energetic exploitation
has increased recently; both existing plantations and short
rotations are being considered as sources of plant biomass
(Facciotto and Mughini, 2003).
Over the last 50 years, many exotic, herbivorous insects that
feed on Eucalyptus have been accidentally introduced into Italy,
sometimes increasing to large numbers and causing substantial
damage. Among these pests, two Australian eulophid gall wasps,
Leptocybe invasa Fisher and La Salle and Ophelimus maskelli
(Ashmead) (Eulophidae), have been recorded in Italy since 2000
(Arzone and Alma, 2000; Viggiani and Nicotina 2001; Bella and
Lo Verde, 2002; Bagnoli and Roversi, 2004) and have also spread
to other Mediterranean countries including Spain (Sánchez,
2003), Israel (Mendel et al., 2004, 2005), Turkey (Dog
˘anlar, 2005;
˘anlar and Mendel, 2007), Portugal (Branco et al., 2006), Greece
(Kavallieratos et al., 2006), France (EPPO, 2006), Tunisia (Dhahri
et al., 2010), and Algeria (Mendel et al., 2004; Caleca, 2010). The
current paper focuses on biological control of O. maskelli.
O. maskelli produces blister-like galls on the leaf surface and
prefers to oviposit on leaves that are 35–40 days old. Leaves with-
out galls live for about 243 days, whereas leaves with more than 50
galls live only about 70 days (Protasov et al., 2007a). Infested
leaves wither and drop, and a general decay occurs on nursery
plants (Lo Verde et al., 2009). Moreover, high numbers of flying,
1049-9644/$ - see front matter !2010 Elsevier Inc. All rights reserved.
Corresponding author. Fax: +39 091 6515331.
E-mail address: (V. Caleca).
Biological Control 57 (2011) 66–73
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newly emerged wasps can cause allergic reactions and other health
problems in humans (Bagnoli and Roversi, 2004; Mendel et al.,
2005; Laudonia et al., 2006).
O. maskelli completes more than one generation per year in Italy
(Bagnoli and Roversi, 2004; Laudonia, 2005; Lo Verde et al., 2009)
and completes three generations per year in Israel (Protasov et al.,
2007a). Larvae overwinter in galls and develop only slowly in win-
ter (Viggiani and Nicotina, 2001; Protasov et al., 2007a). In nurseries
where eucalypts are propagated, clays and systemic chemicals may
prevent initiation of galls and thus protect young plants from dam-
age caused by O. maskelli (Mendel et al., 2005; Lo Verde et al., 2009).
In 2003, a classical biological control program was jointly
undertaken by the Volcani Center of Bet Dagan (Israel) and the
CSIRO of Canberra (Australia), and the initial research concerned
the search for and evaluation of natural enemies of O. maskelli in
Australia. In 2005, the uniparental endophagous parasitoid species
Closterocerus chamaeleon (Girault) (Hymenoptera, Eulophidae) was
introduced into Israel together with Stethynium ophelimi Huber
(Hymenoptera Mymaridae) (Mendel et al., 2007; Protasov et al.,
2007b; Viggiani et al., 2008). In April 2006, Prof. Zvi Mendel of
the Volcani Center sent the authors Eucalyptus leaves bearing galls
parasitized by C. chamaeleon. In May 2006, C. chamaeleon was re-
leased at five Sicilian sites (Rizzo et al., 2006). C. chamaeleon was
also introduced in Campania in April–May 2006 (Laudonia et al.,
2006; Sasso et al., 2008), in Calabria and Sardinia in December
2006 (Caleca et al., 2009). The present paper describes the release
and the subsequent spread of C. chamaeleon and its rate of parasit-
ism in Sicily. Data from preliminary reports (Rizzo et al., 2006,
2007; Caleca et al., 2009) are included in this publication.
2. Materials and methods
2.1. Laboratory rearing
In April 2006, about 500 E. camaldulensis leaves bearing galls of
O. maskelli parasitized by C. chamaeleon were sent to the authors by
the Volcani Center in Israel and were examined with a stereomi-
croscope to ensure that no other arthropods were present. The
leaves were then placed in polyethylene bags (about 50 leaves
per bag) with blotting paper at room temperature (Rizzo et al.,
2006). Bags were examined daily for emergence of C. chamaeleon
adults. Some of the adults that emerged were used for a no-choice
alternative host test (to be described in a future report), and other
adults were placed on seedlings of E. camaldulensis with unparasit-
ized galled leaves. Each seedling was isolated by an aphid-proof
net bag. Once the high specificity of C. chamaeleon was ascertained
by the no-choice parasitism tests (unpublished data), the adults
that emerged from galls in these bags were collected daily and
used for field releases, as described in the next section.
2.2. Release of C. chamaeleon
In the spring of 2006 the gall wasp O. maskelli was widespread
in E. camaldulensis trees of Sicily; anyway the presence of leaves
bearing O. maskelli galls was ascertained in all release sites prior
to releasing C. chamaeleon. The parasitoid was released at the fol-
lowing five sites (Fig. 1):
1. Luparello, Palermo (38"07
N, 13"18
E; 100 m a.s.l.).
This site contained 20 E. camaldulensis trees growing along a
small road in the suburbs of Palermo.
2. Via Basile, Palermo (38"05
N, 13"20
E; 75 m a.s.l.).
This site contained 30 E. camaldulensis trees growing along a
road in the suburbs, 1.7 km from the Agriculture Faculty of
the University of Palermo.
3. Raffo Rosso, Palermo (38"10
N, 13"15
E; 450 m a.s.l.).
This site was an afforested area (122 ha) with conifers and E.
camaldulensis (about 20%), 2.5 km from the city.
4. Monte Finestrelle, Santa Ninfa (Trapani) (37"48
N, 12"54
E; 580 m a.s.l.). This site was a large afforested area (350 ha)
with conifers and Eucalyptus spp. (about 10%).
5. Mustigarufi, Caltanissetta (37"32
N, 13"55
E; 500 m
a.s.l.). This site was a large area (3252 ha) planted with E. cam-
aldulensis, E. occidentalis, and E. globulus, in the centre of Sicily.
The first two suburban release sites consist of small patches in
which E. camaldulensis trees are few in number (20 and 30, respec-
tively); in the surrounding areas, where the secondary sites were
located (see below), the eucalipt trees are mainly present in road
tree lines or in small patches, and not uniformly shared out. On
the contrary, the three afforested sites consist of large or very
large areas (122, 350 and 3252 ha respectively), including conifers
(Raffo Rosso and Monte Finestrelle) or other eucalypt species
(Mustigarufi); the extent of these release sites resulted so large
that the secondary sites (see below) were chosen inside the same
afforested areas.
From the 6 May to 17 May 2006, 400–600 adult C. chamaeleon
were released at each site. The adults were released on five adja-
cent trees at each site. In addition, 10–15 leaves bearing parasit-
ized galls were pinned to the green leaves of the same trees to
allow the gradual emergence of the parasitoid. To ensure that par-
asitism could occur in the field, about 100 C. chamaeleon adults
were released inside an aphid-proof net bag (70 !130 cm) that en-
closed a branch with galled leaves. There was one bag per release
site, and the determination of parasitism in the bags and at the re-
lease sites is described in the following Section 2.4.
2.3. Sampling of release sites
Because C. chamaeleon required 3 weeks to complete one gener-
ation in the laboratory (Rizzo et al., 2006; Protasov et al., 2007a),
the first sampling was carried out about 20 days after the release.
At least 100 galled leaves were collected from the five release trees
and 100 leaves from nearby trees at each release site. At the same
time, all leaves and insects found inside the net bag were collected,
and the net bag was removed. Materials were transferred to the
laboratory and treated as described earlier for the leaves received
from Israel. Emerged gall wasps and parasitoids were collected dai-
ly and counted. Data regarding the presence of the parasitoid in-
side the net bags were recorded only at the first sampling and
were not cumulated with those coming from the open air.
2.4. Sampling to determine spread from release sites
Parasitoid spread was evaluated after the parasitoid was re-
corded for the first time (whether from the leaves in the open air
or inside the net bags) at each release site. Spread was determined
by sampling five ‘‘secondary sites’’ for each site. Each of them was
about 1–2 km away from the release site; 100 leaves with galls
were collected from each secondary site, transferred to the labora-
tory, and examined for parasitoid emergence as described earlier.
Once the parasitoid had emerged from every secondary site, four
additional samplings sites were added per each release site; these
‘‘tertiary sites’’ were located 12–20 km from and to the east, west,
north, and south of the release site. If sample areas of the tertiary
sites associated with different release sites overlapped, as they did
in the three suburban sites, these samplings were considered to be
in common. Every time the parasitoid was recorded in each of
these tertiary sites, four more ‘‘quaternary samplings sites’’
(located 21–50 km from the release site) were added as above to
enlarge the sampling area around each release site; with the
V. Caleca et al. / Biological Control 57 (2011) 66–73 67
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addition of the quaternary sites, the five sampling areas merged.
Since in April 2007 the parasitoid was established in all release
sites and also in most of secondary and tertiary sites, its subse-
quent spread over the whole region, from November 2007 until
April 2009, was monitored by collecting samples (at least 100
galled leaves per sample) mostly in the eastern part of Sicily or
at high altitude sites (over 800 m a.s.l.) and on some islets sur-
rounding Sicily. In total, 119 samples at 60 sites were collected
in all Sicilian provinces. The distance between a new site and the
release sites was calculated in a straight line on a topographic map.
The percentage parasitism was calculated as: A/(A+B)!100,
where Ais the number of C. chamaeleon and Bis the number of
O. maskelli that emerged from sampled leaves.
3. Results and discussion
In total, 109,447 O. maskelli and 68,524 C. chamaeleon were ob-
tained from the 119 field samples. In Figs. 1–6 it is possible to fol-
low the spread of the parasitoid and the growth of its parasitism
Release sites
Parasitization level
Parasitoid not recorded
10 km
1 – June ‘06: 20 days
after the release
Fig. 1. Map of Sicily showing release sites and parasitism level recorded 20 days after the release of Closterocerus chamaeleon.
Secondary sites
Release sites
10 km
Parasitization level
Parasitoid not recorded
2 – July 06: 2 months
after the release
Fig. 2. Parasitism level recorded in release and secondary sites 2 months after the release of C. chamaeleon.
68 V. Caleca et al. / Biological Control 57 (2011) 66–73
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level in Sicily and its surrounding islets. In four of the five release
sites, C. chamaeleon was recovered 20 days after its introduction
(Fig. 1). By October 2006, within 5 months of release, the parasitoid
was recorded in all release sites, it had spread up to 2 km from the
release sites and had caused 62% parasitism at the release sites and
38% parasitism at the secondary sites (Fig. 3,Table 1). From Octo-
ber 2006 onward, parasitism was nearly 100% (95–100%) at all
coastal Palermo sites (Figs. 3–5). In December 2006, C. chamaeleon
was detected in 8 out of 11 tertiary sites, up to 17 km from release
sites, with an average parasitism of 63% in the 8 positive sites
(Fig. 4,Table 1). In spring 2007, 1 year after the release, the parasit-
oid had dispersed more than 50 km from release sites, while at the
beginning of winter 2007–08, the parasitoid was recovered
throughout Sicily and also in many surrounding islets (Fig. 5,
Table 1). Since then, parasitism has remained over 65% in all
seasons and sites, mostly reaching 100% (Fig. 6,Table 1). Thus, both
the data for spread and parasitism rate indicate that C. chamaeleon
was well established within 18 months of release. It is also
10 km
Secondary sites
Release sites
Parasitization level
> 90%
Parasitoid not recorded
3 – October 06: 5 months
after the release
Fig. 3. Parasitism level recorded in release and secondary sites 5 months after the release of C. chamaeleon.
10 km
Other sample sites
Release sites
Parasitization level
> 90%
Parasitoid not recorded
4 – Winter ’06-’07: 7-9
months after the release
Fig. 4. Parasitism level recorded in release, secondary and tertiary sites 7–9 months after the release of C. chamaeleon.
V. Caleca et al. / Biological Control 57 (2011) 66–73 69
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interesting that in the first year after the release, both the parasit-
ism rate and the dispersal rate increased slowly at first but then in-
creased rapidly (Figs. 1–7,Table 1).
The recorded maximum C. chamaeleon dispersal rate (calculated
as maximum distance from release site/time of first recovery after
parasitoid release) was 0.15 km/month in the first 2 months after
release and 0.6 km/month in the next 3 months (Fig. 7). The max-
imum dispersal rate had increased to 7.5 km/month 7 months after
release and to 20 km/month 18 months after release. By the 18th
month, the parasitoid had colonized the entire island (Figs. 6 and
7). The dispersal rate is most likely underestimate from autumn
2006 onwards because C. chamaeleon was recovered at the first
sampling in most of the new sample sites, which made it difficult
to assess when it had arrived at those sites (Figs. 4 and 5,Table 1).
Parasitoid dispersal mechanisms are still poorly understood
(Langhof et al., 2005), and the few valuable studies are typically
based on mark-release-recapture experiments (Wanner et al.,
2007; Grillenberger et al., 2009). Exotic parasitoid introductions
10 km
Other sample sites
Release sites
Parasitization level
> 90%
Parasitoid not recorded
5 – Spring-summer 07:
1 year after the release
Fig. 5. Parasitism level recorded in release, secondary, tertiary and quaternary sites 1 year after the release of C. chamaeleon.
10 km
Sites with parasitisation level > 90%
Release sites
Sites with parasitisation level 60-89%
6 – November 07- April 09:
18-35 months after the
Fig. 6. Parasitism level recorded in sample sites 18–35 months after the release of C. chamaeleon.
70 V. Caleca et al. / Biological Control 57 (2011) 66–73
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constitute interesting case studies in which spreading models can
be investigated and tested (Liebhold and Tobin, 2008; Gichini et al.,
The C. chamaeleon case study provides some insights into the
dispersal rate and ecology of exotic parasitoids. Indeed, the initial
increase in dispersal and parasitism rates was slow but constant,
indicating a continuous spreading mechanism that depended on
the parasitoid’s short-distance dispersal capacity (sensu Liebhold
and Tobin, 2008) and population growth rate. In addition, the
introduced populations of C. chamaeleon were evidently not nega-
tively affected by the initially small numbers (i.e., by the Allee ef-
fect); the Allee effect has been observed in other exotic parasitoid
introductions (Gichini et al., 2008).
In our case, the pattern of parasitoid spread fit the spread latency
model of biological invasions, in which a time lag or latency period
typically occurs between the arrival of a non-native species and the
growth of its population to detectable levels (Liebhold and Tobin,
2008). Both the biological features of the parasitoid and environ-
mental factors allowed a very short spread latency period, with
clear differences between suburban and afforested release sites
and their secondary sites that were 2 km away. In suburban release
sites, parasitism rates increased rapidly, leading to the rapid colo-
nisation of small Eucalyptus patches, so that plots of percentage of
parasitism on time were very similar in release and related second-
ary sites (Fig. 8). In the three afforested areas, increases in parasit-
ism at the secondary sites tended to lag behind increases at the
release sites, indicating a longer spread latency period in afforested
areas than in suburban area, probably due both to the greater ex-
tent of potentially colonisable area and to the cooler climate
(Fig. 8).
Although large Eucalyptus plantations are isolated and uncom-
mon in Sicily, small patches of Eucalyptus spp., mixed reafforested
areas, and roads lined with mostly E. camaldulensis are widespread
and represent dispersal corridors that facilitate the continuous par-
asitoid spread; here it was similar to that documented in Sardinia
and Calabria, i.e., the parasitoid was widely recovered in all three
regions 18 months after its introduction (Caleca et al., 2009). The
recovery of C. chamaeleon in Basilicata and Apulia (De Marzo,
2007) may be a consequence of releases made in two adjacent re-
gions, Campania and Calabria.
Maximum distance from release sites (km)
Months after parasitoid release
Maximum distance from release sites (km)
Dispersal rate (km/month)
Dispersal rate (km/month)
Fig. 7. Dispersal rate of Closterocerus chamaeleon in Sicily after its release.
Table 1
Seasonal average parasitism (%) of Ophelimus maskelli by Closterocerus chamaeleon at the release sites and at other sites from May 2006 to April 2009. For other sites, distance from
the closest release site is indicated.
Sites June
Release sites n = 5 0.6 10 62 93 77
(0–1.4) (0–47) (10–100) (77–100) (40–99)
n=5 n=5 n=5 n=5 n=5
Secondary sites
(up to 2 km) n=5
0 38 52 42
(0.04–96) (0–99) (1.1–99)
n=5 n=5 n=5 n=5
Tertiary sites
(from 12 to 20 km)
n= 13
46 29 100 96 –
(0–100) (0.1–100) (100–100) (93–100)
n= 11 n= 12 n=3 n=2
Quaternary sites
(from 21 to 50 km)
n= 20
– – 0 8 34 99 76 100
(0.01–18) (1–67) (94–100) (67–97)
n=2 n=9 n=2 n=6 n=5 n=2
Sites beyond 50 km n= 17 0,2 96 72 86
(0–1) (67–100) (71–73)
n=4 n= 13 n=2 n=1
All sites n= 60 0.6 5 50 54 29 34 97 79 100 86
(0–1.4) (0–47) (0.04–100) (0–100) (0–100) (1–67) (67–100) (67–100)
n=5 n= 10 n= 10 n= 23 n= 35 n=2 n= 22 n=9 n=2 n=1
Top line = average; in brackets = extreme values; n= sample sites; – = no collected data.
V. Caleca et al. / Biological Control 57 (2011) 66–73 71
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On the other hand, the recovery of C. chamaeleon on small islets
that surround Sicily, as documented in the current paper and in a
preliminary report (Caleca et al., 2009), demonstrates that this par-
asitoid has the capacity for long-distance dispersal, which would
be due to passive transport due both to the wind, facilitated by
its small size, its ability to survive for long periods (Protasov
et al., 2007b), its winter activity (Rizzo et al., 2006), and by the hu-
man movements along the regional territory, enabled by its protec-
tion in accidentally transported galled leaves.
Evidence of long-distance dispersal by C. chamaeleon is also
provided by data following its accidental introduction in 2007 in
Turkey (Doganlar and Mendel, 2007); Portugal (Branco et al., 2009);
Tuscany (Bagnoli, pers. comm.); Liguria and Lazio (Lo Verde, pers.
comm.); and Tunisia (Lo Verde et al., 2010). In 2008, the parasitoid
was also detected in Spain (Borrajo et al., 2008), Lombardy (Lo
Verde, pers. comm.), and Algeria (Caleca, 2010). Both long-distance
and continuous dispersal mechanisms have also been observed for
other Eulophid exotic parasitoids that have spread throughout new
territories after their release or accidental introduction (Mineo
et al., 1998; Massa et al., 2001; Rizzo et al., 2007; Gichini et al.,
As demonstrated in Israel and Campania (Protasov et al., 2007b;
Sasso et al., 2008), C. chamaeleon greatly reduces O. maskelli popu-
lations. Its efficacy as a biological control agent is enhanced by the
following characteristics: telitokous parthenogenesis, preimaginal
development (3 weeks) shorter than that of its host (at least
3 months), adult winter activity (Rizzo et al., 2006; Protasov
et al., 2007b; Sasso et al., 2008), and host specificity (Protasov
et al., 2007b; authors’ unpublished data).
We are grateful to Zvi Mendel and the Volcani Center (Israel)
for providing the parasitoids for releases; to John La Salle for his
information on the parasitoid; and to Graziella Vicari, Francesco
Tortorici, Matteo Maltese, Bruno Massa, Tommaso La Mantia,
Giuseppe Di Giorgio, Letizia Perremuto, and Antonella Blanda
for their help in collecting and analysing samples. Technical
editing and revising was provided by Bruce Jaffee. This research
was funded by Università degli Studi di Palermo (Progetti di
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
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0 50 100 150 200 250 300 350
% Parasitism
Days after release
suburban release sites afforested release sites
suburban secondary sites afforested secondary sites
tendency line of suburban release sites tendency line of afforested release sites
tendency line of suburban secondary sites tendency line of afforested secondary sites
Fig. 8. Plots of parasitism (percentage of Ophelimus maskelli parasitized by Closterocerus chamaeleon) in suburban and afforested release sites and their respective secondary
sites, which were 1–2 km from the release sites.
72 V. Caleca et al. / Biological Control 57 (2011) 66–73
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... 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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A five-month survey on Eucalyptus spp., one of the most commonly planted trees in Cyprus, was undertaken in Limassol and Akrotiri in urban, rural and protected habitats. Two alien gall-inducing Eucalyptus wasps: Leptocybe invasa Fisher and La Salle, 2004 and Ophelimus maskelli (Ashmead, 1900) (Hymenoptera: Eulophidae) were recorded for the first time from Cyprus. In addition, three new alien parasitoids: Stethynium ophelimi (Huber, 2006) (Hymenoptera: Mymaridae), Closterocerus chamaeleon (Girault, 1922) (Hymenoptera: Eulophidae) and Megastigmus lawsoni Doğanlar and Hassan, 2010 (Hymenoptera: Torymidae), were reared from O. maskelli and L. invasa galls. The distribution, introduction and management actions for Eucalyptus spp. and their alien Chalcidoidea associates are discussed.
... The greater longevity of C. chamaeleon than of its hosts explains its widespread distribution and greater capacity as a biocontrol agent of both O. eucalypti and O. maskelli in terms of foraging capacity and parasitism rate (Branco et al., 2009;Caleca et al., 2011). This parasitoid is recorded to have parasitised up to 100% of the galls induced by O. maskelli in Sumatra and led to a satisfactory capacity of the leaves to recover after the adult parasitoid emerged from its host . ...
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.
... The Australian parasitoids Quadrastichus mendeli Kim & La Salle and Selitrichodes kryceri Kim & La Salle (Hymenoptera: Eulophidae) have been released to control L. invasa in Israel (Kim et al. 2008). The Australian parasitoid Closterocerus chamaeleon (Girault) (Hymenoptera: Eulophidae) has been used to effectively control O. maskelli in some areas of the Mediterranean Basin (Burks et al. 2015;Caleca et al. 2011;Mendel et al. 2007;Protasov et al. 2007;Rizzo et al. 2006). Closterocerus chamaeleon has already exhibited strong potential for independent expansion to populations of O. maskelli in distant areas, such as Portugal (Branco et al. 2009), and there is the possibility that it will spread to Gibraltar, which may help mitigate any potential impacts of this pest. ...
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Four invasive eucalypt-feeding insects, native to Australia, are recorded from Gibraltar for the first time: the gall-forming wasps Ophelimus maskelli (Ashmead) and Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae), the lerp-forming psyllid Glycaspis brimblecombei Moore (Hemiptera: Aphalaridae), and the bronze bug Thaumastocoris peregrinus Carpintero & Dellapé (Hemiptera: Thaumastocoridae), whilst the status of two Eucalyptus longhorned borers, Phoracantha recurva Newman and P. semipunctata (Fabricius) (Coleoptera: Cerambycidae), is summarised. The former five species have been found on the red-gum tree Eucalyptus camaldulensis Dehnh., growing in the urban environment in Gibraltar. The potential impact of these invasive species is discussed.
... Minute parasitoids often disperse small distances unless carried by prevailing winds, which makes proximity of floral resources critical for wasps whose activity coincides with host life stages in crops. Parasitoid dispersal can be measured directly through mark-recapture efforts that involve fluorescent dyes [33], albumin-based compounds that are evaluated, with ELISA protein markers [34], or release and recovery through sentinel eggs or sticky cards [29,35] or on the natural host [36]. Low recovery rates are a detriment of mark-recapture studies. ...
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The herbivorous brown marmorated stink bug, Halyomorpha halys, has spread globally, and one of its key parasitoids, Trissolcus japonicus, has recently been detected in the pest's introduced range. For an exotic natural enemy to impact its targeted host in a novel environment, it must disperse, locate hosts, and potentially be redistributed to susceptible sites. Through intentionally releasing T. japonicus across four Oregon eco-regions, we investigated an introduced parasitoid's dispersal capacity in urban sites and in two perennial crops, hazelnut and raspberry. In a second paired field and laboratory study, we investigated T. japonicus survival in different plant materials. Within three days of release, adult T. japonicus located host egg masses at 45% of sites and, one year later, were detected at 40% of release sites. Areas where released wasps survived winter were mostly urban or semi-natural. In commercial crop release experiments, we recovered the highest percentage of wasps in raspberry within 5 m of the release site but found no statistical difference in dispersal distance with some wasps dispersing up to 50 m. Adult parasitoids survived up to 16 weeks outdoors in the winter, with greater survival over time in bark compared to leaf litter. Wasp survival remained above 50% over the course of a simulated winter environment without precipitation. Our work affirms the continuation of H. halys parasitism by T. japonicus in novel environments and provides insight into the high population sizes necessary to survive winter and locate host egg masses the following season.
... This parasitoid was introduced from Australia to be used in classical biological control programs of O. maskelli in Israel (2005)(2006) and Italy (2006). In both countries, the control results were successful (Laudonia et al., 2006;Protasov et al., 2007b;Mendel et al., 2007;Caleca et al., 2011;Mendel et al., 2017;Suma et al., 2018). In this context and due the significant economic burden E. globulus represent for the Chilean forest industry, we aimed to determine the presence of Ophelimus migdanorum in plantations of E. globulus located between the Maule, Biobío and La Araucanía Regions, Chile. ...
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Wasps that belong to the genus Ophelimus develop galls on Eucalyptus spp., and E. globulus is considered among the most susceptible species. In 2003, a new species of Ophelimus was detected in Chile. This species forms galls on E. globulus and E. camaldulensis, and it was recently considered as Ophelimus migdanorum nov sp. The present study was carried out 16 yr after its detection and it was aimed to determine the presence of Ophelimus in plantations of E. globulus located in Maule, Biobío and La Araucanía Regions, which represent 76% of the area covered with this species in the country. Between August and September 2017, a total of 165 sampling forest farms were established in stands of E. globulus, located in these regions of the country. In each farm, twigs were collected that represented formation of galls and maintained in laboratory conditions until the emergence of adults. These were identified according to their external morphological characteristics. The presence of O. migdanorum and Closterocerus chamaeleon was determined. Both species emerged together in all the regions considered in the study, 92.1% and 46.7% of the evaluated forest farms, respectively. Then Ophelimus migdanorum is widely distributed in Maule, Biobío and La Araucanía Regions, in Chile.
... 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). ...
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.
... Finally, in relation to the two Eucalyptus gall wasps, recent studies carried out after the release of the parasitoid C. chamaeleon in Sicily showed its high efficacy in reducing O. maskelli populations. Its establishment, spreading speed and the observed discontinuous pattern of dispersal showed the occurrence of both long and short distance dispersal mechanisms (CALECA et al., 2011b). ...
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A review is reported in the present paper on invasive alien insects introduced in Sicily on Eucalyptus trees, together with unpublished results from recent surveys. As to the latter ones, observations were conducted especially on Thaumastocoris peregrinus (Carpintero & Dellapé) (Hemiptera, Thaumastocoridae), the most recently introduced species. Overall, eight alien insect pests have been accidentally introduced in the island on Eucalyptus, belonging to the orders Hemiptera (Aphalaridae, 2 spp.; Thaumastocoridae, 1 sp.), Coleoptera (Cerambycidae, 2 spp.; Curculionidae, 1 sp.) and Hymenoptera (Eulophidae, 2 spp.). Two encyrtid parasitoids, Avetianella longoi Siscaro and Psyllaephagus bli-teus Riek, obtained from Phoracantha spp. and Glycaspis brimblecombei Moore respectively, and Closterocerus chamaeleon (Girault) (Hymenoptera, Eulophidae) attacking Ophelimus maskelli (Ashmead), are also reported. Details on current distribution, host plants, morphological and biological remarks are given for each species.
... After the first record of P. bliteus in Sicily, its spread all over the region occurred in a short time, showing the high dispersal capacity. Similarly, Closterocerus chamaeleon (Girault), a parasitoid released in Sicily to control the euca- lypt gall wasp Ophelimus maskelli (Ashmead) (Hyme - noptera, Eulophidae) (RIZZO et al., 2015), rapidly spread through short and long distance dispersal mechanism, being widely distributed in the region after 18 months from its release in 2006 (CALECA et al., 2011b). ...
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Rapisarda C.-Environmental factors impact and incidence of parasitism of Psyllaephagus bliteus Riek (Hymenoptera Encyrtidae) on populations of Glycaspis brimblecombei Moore (Hemiptera Aphalaridae) in Mediterranean climatic areas. The red gum lerp psyllid, Glycaspis brimblecombei Moore (Hemiptera, Aphalaridae), is an Australian native sap-sucking insect pest of eucalypts that has been first reported for the West Palaearctic Region in 2008 and, in 2010, it has been found also in Italy. Subsequently its primary parasitoid, Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae), was also detected within the main European and North African infested areas, where no release of the parasitoid was ever performed. This study, carried out in 30 Eucalyptus camaldulensis plantations located along the coast, on the hills and the mountains in Mediterranean climatic areas of Sicily (Italy), aimed to determine the influence of environmental parameters on the incidence of both, the psyllid infestation level and the parasitization activity. P. bliteus reached highest average levels in summer samplings and resulted widespread in Sicily at all detected altitudes without statistically significant differences. P. bliteus parasitization is the main factor lowering G. brimblecombei infestation; this result, together with the accidental and contemporaneous arrival of the host and its parasitoid, could explain the absence of high damage level on eucalypts in Sicily. The most significant metric factors positively influencing G. brimblecombei infestation are the percentage of daily hours above 80% of relative humidity and the average maximum temperature, obviously related to other, but less significant climatic factors. The altitude affects both infestation and parasitization, but single sites could explain significantly more, so that the local conditions where the samplings were carried out have to be considered as the main responsibles for the variability in the obtained results. In any sampled Sicilian site, from sea level to 540 m a.s.l., both the psyllid and its parasitoids show a good adaptation to climatic conditions, confirming that areas fitting for E. camaldulensis growth fit also for P. bliteus activity, and proving that Mediterranean climate, differently from some inland areas of California, does not obstacle its parasitic activity.
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p> Eucalyptus spp. are commonly cultivated in the forest industry sector as the raw material for the pulp and paper industry. One of the problems in Eucalyptus plantations is leaf galls caused by insects. Leaf galls can cause leaf damage and inhibit plant growth. The objective of this study was to identify insects associated with leaf galls on eucalyptus plants. Leaves with gall symptoms were collected in the Tele sector located between Humbang Hasundutan and Samosir Regencies, North Sumatra Province. Identification was based on morphological characters of the antenna, dorsal mesosoma, fore wings, and hind legs. Results showed that there were seven insect species associated with leaf galls on Eucalyptus, i.e. Ophelimus eucalypti (Gahan) (Eulophidae) pest gall on eucalyptus leaf, Eurytoma sp. Illiger (Eurytomidae), Aprostocetus sp. Westwood, Quadrastichus mendeli Kim & La Salle, Chrysonotomyia germanica (Erdös), and Closterocerus chamaeleon (Girault) (Eulophidae) acts as a parasitoid and Diplesiostigma bisetosum Boucek (Tetracampidae).</p
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We report here for the first time the presence of Ophelimus mediterraneus sp. n. in Mediterranean Europe. This species appears to be closely related to Ophelimus maskelli, a well-known invasive pest of Eucalyptus. Based on molecular (Cytochrome Oxydase I, 28S), morphological (Multivariate Ratio Analysis) and bio-ecological investigations, our study gives unambiguous relevant criteria that allow the discrimination between these 2 species. A full description of O. mediterraneus sp. n. is also provided. The geographic distribution of O. mediterraneus sp. n. as well as its impact on Eucalyptus species needs to be more widely assessed since its presence may have been confused with O. maskelli in their sympatric introduced areas. Further Investigations of potential parasitoids in the native area may thus be welcomed to evaluate classical biological control achievability.
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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.