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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
Keywords:
Closterocerus chamaeleon
Ophelimus maskelli
Eucalyptus gall wasp
Parasitoid introduction
Dispersal strategy
Parasitism level
abstract
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;
Dog
˘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.
doi:10.1016/j.biocontrol.2010.12.006
⇑
Corresponding author. Fax: +39 091 6515331.
E-mail address: caleca@unipa.it (V. Caleca).
Biological Control 57 (2011) 66–73
Contents lists available at ScienceDirect
Biological Control
journal homepage: www.elsevier.com/locate/ybcon
Author's personal copy
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
0
04
00
N, 13"18
0
11
00
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
0
41.7
00
N, 13"20
0
18
00
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
0
45
00
N, 13"15
0
38
00
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
0
25
00
N, 12"54
0
38
00
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
0
55
00
N, 13"55
0
25
00
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
0.1-15%
10 km
12
3
4
5
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
16-59%
Parasitoid not recorded
0.1-15%
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%
60-89%
16-59%
Parasitoid not recorded
0.1-15%
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%
60-89%
16-59%
Parasitoid not recorded
0.1-15%
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%
60-89%
16-59%
Parasitoid not recorded
0.1-15%
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
release
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.,
2008).
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.
0
5
10
15
20
25
0
20
40
60
80
100
120
140
160
180
200
23456789101112131415161718
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
2006
July
2006
Autumn
2006
Winter
2006–07
Spring
2007
Summer
2007
Autumn–Winter
2007–08
Spring
2008
Summer–Autumn
2008
Spring
2009
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.,
2008).
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).
Acknowledgments
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
Ateneo).
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.biocontrol.2010.12.006.
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0
20
40
60
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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.
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