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2013 IEEE Symposium on Humanities, Science and Engineering Research (SHUSER)

Assessment on the Diversity of Parasitoids of


Bagworms (Lepidoptera: Psychidae) in
FELDA Gunung Besout 6, Sungkai, Perak

*Mohd Hanysyam, M.N., *Fauziah, I., **Siti Khairiyah, M.H., *Fairuz, K., *Mohd Rasdi, Z.,
**Nurul Zfarina, M.Z., *Ismail R. and *Norazliza, R.
*Faculty of Plantation and Agrotechnology, Universiti Teknologi MARA, 40450 Shah Alam, Selangor
**Faculty of Applied Sciences, Universiti Teknologi MARA, 40450 Shah Alam, Selangor
E-mail (corresponding authors): matlabu5741@yahoo.com; sitikhairiyah@salam.uitm.edu.my; fairuzdk@salam.uitm.edu.my

Abstract--- Species abundance, diversity, richness, evenness and Bagworm, particularly Metisa plana Walker, is one of the
similarities of parasitoids of bagworms were evaluated at three important leaf-eating pests of oil palm in Malaysia and
different localities in an oil palm plantation at FELDA Gunung Indonesia. This species of bagworm is capable of being
Besout 6 in Sungkai, Perak. All the three study areas were present as outbreak and a damage of 50% would cause high
situated approximately 500m between each other and included yield losses up to 40-47% or 10 t/ha over two years after a
the margin and interior part of the oil palm area, and also serious infestation [4] - [9]. Crop losses due to the extent of
around the beneficial plants area, which particularly Antigonon defoliation by a serious bagworm attack, are still inevitable
leptopus. The abundance, diversity and similarity of insects were and a moderate defoliation of about 10%-30% may cause a
varied at all three study sites, which demonstrated the effect of crop loss of about 33%-40% in two years time [8],[10].
level of disturbances, vegetation diversity and food sources
availability. Samplings were conducted for six months starting Parasitoids are an important group of natural enemies that
from August 2011 until January 2012 using Malaise traps. A total survive on nectar of beneficial plants as source of food [9],
of 59 parasitoids, belonging to two orders and seven families were while their life cycles are dependent on their preferred hosts
collected from the trap around margin area, whereas a total of 67 [11]. Bagworm-parasitoid interactions are highly influenced
insects belonging to two orders and seven families were collected by presence of beneficial plants surrounding the plantation
from the trap around the interior area and a total of 68 insects areas [9] and the availability of bagworms as host [12].
belonging to two orders and six families were collected from the
trap around the beneficial plants area. The beneficial plant site In oil palm area of FELDA Gunung Besout 6, chemical
has the highest Shannon-Weiner Diversity Index, followed by the insecticides spraying such as trichlorfon, diflubenzuron,
interior and the margin site. However, there were no significant cypermethrin or monocrotophos and methamidophos
differences between the three habitats (p>0.05) through ANOVA injections have been utilized for bagworms control. Such
analysis. Results of this study showed that even though the level controls using these chemicals are effective for the beginning
of diversity of parasitoids in the oil palm area of FELDA Gunung of the pest generation as the larvae at the early stage are more
Besout 6 was relatively low, there are still some extensive susceptible than the next stage [13]. However, the usage of
measurement could be carried out for their augmentation and these wide spectrum insecticides are usually would create a
conservation. Factors like food resources, disturbances and long term residue. The residue not only being recognized as
anthropogenic effect are still play the main role in conserving the
the main factor of the recurrent bagworms attack but also is
biodiversity and ecosystem in certain area. Hence, the
designation of oil palm landscape should be functioned in
able to extinguish the non-target insect species, especially the
healthier and more sustainable way in order to provide a wide natural enemies.
range of ecosystem services and the conservation of biodiversity. The presence of natural enemies in the study area, such as
parasitoids, is doubtful since there were poorly propagated of
Keywords-component: diversity, abundance, parasitoids, bagworms, the beneficial plants. The only species that available was
oil palm, FELDA Gunung Besout 6 Antigonon leptopus and it was just a few patches around the
area. This study was intended to gather information on the
I. INTRODUCTION availability of parasitoid species that associated with
bagworms at three different localities in the oil palm area.
The Malaysian palm oil industry continues to dominate the
global supply of the world’s palm oil [1]. Today, the palm oil II. MATERIALS AND METHODS
sector account for nearly seven per cent of Malaysia’s Gross A. Study site
Domestic Product (GDP) and provides more than 1.4 million This research was conducted from August 2011 until
jobs. Not surprisingly, in 2011, the total oil palm planted area January 2012, at FELDA Gunung Besout 6, an oil palm
in the whole country has reached 5.0 million hectares, a plantation in Perak (located 68 km from Sungkai), where the
massive increase of 3.0% against 4.85 million hectares bagworm infestation had occurred for several times and was
recorded the previous year [2]. It also covered approximately allowed to persist without any chemical intervention. This
73% of the total agricultural land and made the oil palm a very plantation has a total area of 652.19 ha. The study site was
promising raw material for renewable energy generation [3].

978-1-4799-0443-3/13/$31.00 ©2013 IEEE 130


2013 IEEE Symposium on Humanities, Science and Engineering Research (SHUSER)

constituted almost 80 oil palm trees. The trees were planted in two orders. There were Hymneoptera and Diptera, which
1989 and have been yielded at least four times since then. represented by only one family, Tachinidae. The species
composition and number of individual parasitoid species
B. Sampling methods collected from the different study sites is shown in Table 1.
The study was carried out at three localities, at about 500
m distance from each other. Each locality represented three A total of 59 insects belonging to 13 species of
types of habitat, where insect sampling was conducted: the oil Hymenopterans parasitoids and one family of Dipterans
palm margin area; the oil palms interior at a distance of about parasitoids were collected from margin area in the oil palm
250 m from the margin; and the beneficial plants patches plantation. The most abundant family is observed at this site
(particularly Antigonon leptopus). was Tachinidae (20 individuals or 33.9% of the parasitoids
collected). Eulophidae constituted 32.2% of the total
Insect sampling was carried out using Malaise traps at parasitoids observed at the margin site and was represented by
every locality in the study area [14]. At all localities, Malaise five species. Pediobius anomalus and Tetrastichus sp. were
trapping was carried out once a month. The collecting jars the most abundant species of Eulophidae, followed by
were filled with 70% alcohol and kept open for at least seven Pediobius imbrues, Pediobius elasmi and Sympiesis sp. In
to ten days, then cleared from the collected individuals. addition, 16.95% of the total parasitoids collected belonged to
Sampling was carried out over a total period of six months, Braconidae, with only Dolichogenidea metesae were found.
yielding total of 18 samples altogether. Ichneumonidae constituted 11.86% from the total of
From each of the samples, all the insects were pooled parasitoids recorded and represented by three species,
together in yellow pan and initially sorted according to their Paraphylax varius, Goryphus bunoh and Spinaria spinator.
physical attributes based on major order. There were seven Only one individual or 1.7% of the total parasitoids were
orders altogether and being stored in vials separately based on collected from three other Hymenopteran families. There were
their original location of trap. Each specimen were then, Ceraphonidae (represented by Aphanogmus thylax),
pinned, and, once dried, these will be kept indefinitely. Eupelmidae (represented by Euplemus catoxanthae) and
Specimens that were too small to pin were mounted on points, Eurytomidae (represented by Eurytoma sp.).
on tiny minuten pins. Large and showy insects were mounted A total of 67 insects belonging to 11 species of
in various types of glass-topped display boxes. Hymenopterans parasitoids and one family of Dipterans
Pinning is the best way to preserve hard-bodied insects parasitoids were collected from the interior area of oil palm.
[15]. The specimens were pinned with a special type of steel Eulophidae was the most abundant family collected with 33
pin, well known as insect pin. Insect pin sizes range from 00 individuals, constituted almost 50% of the total parasitoids,
to 7, but number 2 and 3 are best for general use. Pinning with Tetrastichus sp. were being the most abundant species
block were used to obtain uniformity. For moths and among all parasitoids found (25.37% of total parasitoids),
butterflies, spreading board was used to spread their wings for followed by Pediobius imbrues, Pediobius anomalus,
easy studied. Insects too small to pin were mounted on a card Pediobius elasmi and Sympiesis sp. Dipteran family,
or point. Points are elongated, triangular pieces of light Tachinidae recorded at least 16% of total parasitoids, followed
cardboard or heavy paper, about 8 or 10mm long and 3 or by Braconidae with 14.93% (represented by Dolichogenidea
4mm wide at the base. metesae), Ichneumonidae, 13.43% (represented by two
species, Goryphus bunoh and Paraphylax varius) and
Identification of all species of insects was implemented Ceraphonidea (Aphanogmus thylax) with almost 3%.
with the help of Entomologist and Science Officers from Euplemidae (Euplemus catoxanthae) and Eurytomidae
Strategic Resources Research Centre, MARDI, the Centre of (Eurytoma sp.) have only one individual found, which
Insect Systematic, Faculty of Science and Technology, UKM constituted 1.5% of the total parasitoids collected.
Bangi, and also from Department of Biology, Faculty of
Applied Sciences, UiTM Shah Alam. A total of 68 insects belonging to 13 species of
Hymenopterans parasitoids and Dipterans parasitoids were
C. Data analysis collected from the beneficial plant area in the oil palm
A biological community usually has a large number of plantation. Eulophidae was the dominant family collected
species with relatively small abundances [16]. When a random (five species, 38 individuals), constituted 55.88% of the total
sample of individuals is selected and each individual is individuals collected. Tetrastichus sp. (Eulophidae) still was
classified according to species identity, some rare species may the most abundant species found which constituted 23.53% of
not be discovered. This study insect diversity was considered the total parasitoids found, followed by Pediobius imbrues,
based on the number of species within the sites. The diversity Pediobius elasmi, Pediobius anomalus and Sympiesis sp.
was calculated using the Shannon-Wiener Index [17]. Tachinidae recorded at least almost 18% of total parasitoids,
To determine the percent on the insect species similarity, followed by Ichneumonidae, with 13.24% (represented by four
the Jaccard’s Coefficient Index were being used for comparing species, Paraphylax varius, Spinaria spinator, Goryphus
the similarity and diversity of the insect sample sets [18]. All bunoh and Busymania oxymora), Braconidae, with 8.82%
of the data obtained were encoded and processed by (represented by two species, Dolichogenidea metesae and
employing Microsoft Office Excel 2007 and the statistical Apanteles aluella), Eurytomidae, constituted 2.94% (one
analyses were performed using the Paleontological Statistics species recorded, Eurytoma sp.) and Ceraphonidae, with only
(PAST) software programme [14]. one individual recorded, Aphanogmus thylax.
Throughout the recent study, a total of 194 individuals of
D. RESULTS AND DISCUSSION
parasitoids under two orders of Hymenoptera and Diptera
A. Abundance of all insects in three different habitats were collected. Figure 1 showed the percentage of individual
A total 194 individuals of parasitoids that mainly of parasitoids collected from all three study site in the oil palm
associated with bagworms collected were belonging to only area.

131
2013 IEEE Symposium on Humanities, Science and Engineering Research (SHUSER)

Eupelmidae recorded the highest percentage with 47.42% interior and the beneficial plant area, consists of more than
(92 individuals), followed by Dipteran family, Tachinidae 20% of total parasitoids. This species of parasitoid can be
with 22.17% (43 individuals), Braconidae (13.4%, 26 found on bagworm, Metisa plana as a primary parasitoid and
individuals), Ichneumonidae (11.86%, 23 individuals), as a hyperparasitoid on Mahasena corbetti [19]. Most
Cerophonidae and Eurytomidae (both constituted 2.06%, four Tetratichus sp. is gregarious larval-pupal endoparasitoid and
individuals), and Eupelmidae with only 1.03% (two koinobiont [20] – [23], which it allows the host to continue its
individuals). development while feeding upon it.
Tetratichus sp. from family Eulophidae recorded the
highest number in individuals collected in two sites, the

TABLE I. NUMBER OF INDIVIDUALS OF PARASITOIDS COLLECTED FROM T HREE DIFFERENT SITES IN T HE OIL PALM AREA
Species Family Order Margin Interior Beneficial plant Total
Aphanogmus thylax Ceraphonidae Hymenoptera 1 2 1 4
Eupelmus catoxanthae Eupelmidae Hymenoptera 1 1 - 2
Eurytoma sp. Eurytomidae Hymenoptera 1 1 2 4
Pediobius anomalus Eulophidae Hymenoptera 6 4 4 14
Pediobius elasmi Eulophidae Hymenoptera 2 3 6 11
Pediobius imbrues Eulophidae Hymenoptera 3 6 9 20
Sympiesis sp. Eulophidae Hymenoptera 2 3 3 8
Tetrastichus sp. Eulophidae Hymenoptera 6 17 16 39
Dolichogenidea metesae Braconidae Hymenoptera 10 10 5 25
Apanteles aluella Braconidae Hymenoptera - - 1 1
Goryphus bunoh Ichneumonidae Hymenoptera 2 5 2 7
Paraphylax varius Ichneumonidae Hymenoptera 4 4 3 11
Busymania oxymora Ichneumonidae Hymenoptera - - 1 1
Spinaria spinator Ichneumonidae Hymenoptera 1 - 3 4
Tachinidae Diptera 20 11 12 43
Total individuals 59 67 68 194
Total families 7 7 6

There were other four parasitoid species belonging to As for Ichneumonidae, there were four species recorded,
Eulophidae family, namely Pediobius imbrues, which namely Paraphylax varius with 5.67% of total parasitoids,
constituted 10.31% of total parasitoids, Pediobius anomalus Goryphus bunoh (3.61%), Spinaria spinator (2.06%) and
(7.23%), Pediobius elasmi (5.67%) and Sympiesis (4.12%). Busymania oxymora (0.52%). Paraphylax varius was found as
Pediobius imbrues is mainly found as a primary and a hyperparasitoid for Dolichogenidea metesae on Metisa plana
hyperparasitoid for bagworm, Metisa plana [19]. This species and some species of nettle caterpillars (Norman et al., 1998).
has broad range of 18 other hosts and acted as an obligate and Goryphus bunoh was found as a primary parasitoid for both
facultative hyperparasitoids for other Hymenopteran Metisa plana and Mahasena corbetti but can be a
parasitoids [4]. It is also recorded as the most dominant hyperparasitoid for nettle caterpillar species, Setora nitens
parasitoids found with parasitized bagworms [12]. Due to this (Lepidoptera: Cochlidiidae). Another two species of bagworm
fact, it showed that its effectiveness as primary parasitoid was moths that related to Goryphus bunoh as its host are Amatissa
not affected by its hyperparasitic behaviour. sp. and Dappula sp. (Lepidoptera: Psychidae). Spinaria
spinator was only found on nettle caterpillar, Setora nitens, as
Pediobius anomalus is basically behaving as both primary a primary parasitoid.
and hyperparasitoid for two major bagworms, Metisa plana
and Pteroma pendula [19]. Pediobius elasmi can be found on
other bagworm species, Mahasena corbetti, as primary and
hyperparasitoid. As for Sympiesis sp., it can be found on
Metisa plana and Mahasena corbetti as a primary parasitoid.
Pediobius elasmi and Pediobius imbrues also can be found as
hyperparasitoid for two other moth pests, namely Artona
catoxantha (Lepidoptera: Zygaenidae) and Parasa lepida
(Lepidoptera: Limacodidae) [19].
Family Braconidae was represented by only two species,
namely Dolichogenidea metesae and Apanteles aluella.
Dolichogenidea metesae was far more abundant in number of
individuals than Apanteles aluella in all three sites, consists of
12.89% of total parasitoids collected. Dolichogenidea metesae
can be found as primary parasitoid for bagworm. However, its
parasitizing activities can be interrupted by Pediobius
Figure 1. The percentage of total parasitoids collected from all three
imbrues, which acted as hyperparasitoid [12]. Apanteles localities in the oil palm area
alluella, which only one individual found in the beneficial
plant area, was recorded as primary parasitoid for Darna trima Of all the parasitoid species collected from the three
(Lepidoptera: Limacodidae), another moth pest species [19]. localities, there were three families owned only one parasitoid

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2013 IEEE Symposium on Humanities, Science and Engineering Research (SHUSER)

species recorded. Those families were Ceraphonidae, significant role in supporting the sustenance of parasitoids in
Eurytomidae and Eupelmidae. Aphanogmus thylax from the oil palm area [9]. This study proved that the practices of
Cerphonidae consist of 2.06 % or four individuals collected establishing the beneficial plants in the oil palm area by the
from all three sites. This species can be found on Metisa plana management were able to utilize the parasitoids as the natural
and Mahasena corbetti as a hyperparasitoid [19]. Eurytoma enemies of bagworm pests. However, the H’ value is still
sp. from Eurytomidae also recorded four individuals considered low. It suggested that the establishing the
altogether and can be found on Metisa plana, Mahasena beneficial plants in the study area need to be implemented
corbetti and other lepidopterans as a hyperparasitoid as well. extensively.
However, most species of the large and widespread parasitoid
At the interior site, the H’ value (2.183) was also
genus Eurytoma prefer to attack gall wasps Cynipidae
(Hymenoptera) and two other Diptera families, namely influenced by the E’ value (0.74) and the R’ value (2.616),
where the diversity of the parasitoids was a little bit less
Tephritidae (fruite flies) and Cecidomyidae (gall midges or
gnats) [24]. As for Eupelmus catoxanthae, only two diverse compared to the beneficial plant area. All area in the
interior site was covered with oil palm trees and most palms
individuals collected from both matgin and interior sites. This
species can be found on Metisa plana and Mahasena corbetti were uniform in age and size. Hence, this area may not be able
to contribute on the sustenance of the parasitoids due to the
as primary and hyperparasitoid. Other hosts are including
moth pest species Artona catoxantha and Parasa lepida. lack of beneficial plants as food sources. However, it may
serve as a support for biological interaction with bagworm
Tachinidae, the only dipterans parasitoid family recorded pests as hosts for their reproduction and larval development.
comprises 22.17%, making them second most number
As for the margin site, the H’ value (2.087) was the lowest
collected in all three sites, after Hymenopterans family,
Eulophidae. Tachinidae is included more than 8,500 among all three study sites. Nevertheless, the diversity index,
H’ value, were still influenced by both E’ (0.62) and R’
described species worldwide and all of them are parasitoids of
insects or ohter arthropods, and rank second only to the (2.943) values. Margin sites were situated at the edge of the oil
parasitic Hymenoptera in diversity and ecological importance palm plantation area. This area was adjacent with the main
as insect parasitoids [25]. Therefore, this group has been road, management building, factories, stores, houses and
recognized to be very valuable to humans, because the larval others. Hence, it received the most disturbances and
stages are parasites of other insects and many species aid in anthropogenic effects directly as compared to other two sites.
The lack of beneficial plants and oil palm trees also
keeping pest species in balance [15]. Tachnids attack many
different groups on insects and although most of them are contributed the low level of diversity and species richness in
restricted to certain hosts, a few can develop in a wide variety the area.
of hosts. All tachinid species recorded that associated with In general, all of these sites in the oil palm plantation were
bagworms can be found on Mahasena corbetti and acted as a dealing directly with a lot of factors like the high temperature,
primary parasitoid [19]. low humidity and direct disturbances affect, which lead to the
loss of diversity of fauna in the oil palm plantation [26]. These
B. Diversity of all insects in the three different localities
factors were observed and detected in every part of the oil
The richness of parasitoid species and the abundance in
palm studied area. In this case, homogeneous environment,
three localities based on diversity and evenness are presented
where type of vegetation, rainfall counts, level of humidity
in Table 2. The H’, E’ and R’ values were varied between
and temperature, and soil structure are almost identical in the
three different localities in the oil palm area, even though their
whole area, is expected to exist. Homogenisation of
values are relatively low due to small number of population.
landscapes due to agricultural intensification is widely
The highest parasitoid diversity was found in the beneficial
recognised as the principal cause of declining farmland
plant area, which has a Shannon-Wiener index diversity of
wildlife populations [27].
2.294. The next highest level of diversity was found in the
moderately disturbed habitat, the interior site, which had a Shannon-Wiener diversity index was then analyzed by
diversity index of 2.183. Finally, the lowest amount of using one-way ANOVA in order to compare the significant
diversity was observed in the margin site, which had a high differences between the three localities. The result showed that
level of disturbance and a diversity of 2.087. Evenness also there were no significant differences between the three
tracked habitat and disturbance, but with the greatest value habitats with p>0.05. Therefore, there were no significant
being associated with the interior site, followed by the values in terms of species distribution in all three sites.
beneficial plant site and the margin site.

TABLE II. SHANNON-WIENER DIVERSITY INDEX (H’), C. Similarity of all parasitoids in three different localities in
EVENNESS INDEX (E’) AND MARGALEF RICHNESS I NDEX (R’) FOR ALL the oil palm area
PARASITOIDS COLLECTED AT THE T HREE LOCALITIES IN THE OIL PALM Percent of parasitoid species similarities (Jaccard’s
AREA
Coefficient Index) among the three localities which is shown
Evenness, Margalef, in Table 3 and Figure 2 were relatively high (more than 70%).
Taxa. S’ Individuals Shannon, H’
E’ R’
The similarity value was 80% (Jaccard’s Coefficient Index =
Margin 13 59 2.087 0.620 2.943
0.8), 92.3% and 73% between beneficial plant and margin,
Interior 12 67 2.183 0.740 2.616 interior and margin, and beneficial plant area and interior
B/plant 14 68 2.294 0.708 3.081 respectively.

The higher value of H’ at the beneficial plant site is TABLE III. THE J ACCARD’S COEFFICIENT INDEX (SIMILARITY
influenced by the value of (E’ = 0.708) and value of (R’ = INDEX) FOR ALL PARASITOIDS IN THREE DIFFERENT
3.081). The high value of diversity in the study site is expected LOCALITIES IN THE OIL PALM AREA
due to the consisted of plant species that play a very

133
2013 IEEE Symposium on Humanities, Science and Engineering Research (SHUSER)

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Hamid, assistant manager, for the permission and supports Entomology 6(1), pp. 55-62.
during the field work. Special thanks also to Mr. Jayprakash [19] Norman, K., Mohd Basri, W. and Zulkefli, M. (1998). Handbook of
Pertabai from MARDI and Mr. Roslan Abd. Aziz from UKM, Common Parasitoids and Predators Associated with Bagworms and
for their assistances in identified the insect species. Thanks to Nettle Caterpillars in Oil Palm Plantations. Institut Penyelidikan Minyak
all academic and admin staffs at FPA and FSG for their Kelapa Sawit Malaysia (PORIM), p. 29.
supports and cooperation. This project was totally funded by [20] Mohamed, S.A., Wharton, R.A., von Mérey, G. and Schulthess, F.
(2006). Acceptance and suitability of different host stages of Ceratits
Excellence Funds, Universiti Teknologi MARA, 600- capitata (Wiedemann) (Diptera: Tephritidae) and seven other tephritid
RMI/ST/DANA 5/3/Dst (476/2011).

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fruit fly species to Tetrasthicus giffardii Silvestri (Hymenoptera: [24] Mena-Correa, J., Sivinski, J., Anzures-Dadda, A., Ramírez-Romero, R.,
Eulophidae). Biological Control 39, pp. 262-271. Gates, M. and Aluja, M. (2010). Consideration of Eurytoma sivinskii
[21] Liu, H., Bauer, L.S., Miller, D.L., Zhao, T., Gao, R., Song, L., Luan, Q., Gates and Grissell, a eurytomid (Hyemnoptera) with unusual foraging
Jin, R. and Gao, C. (2007). Seasonal abundance of Agrilus planipennis behaviors, as a bilogical control agent of tephritid (Diptera) fruit flies.
(Coleoptera: Buprestidae) and its natural enemies Oobius agrili Biological Control 53, pp. 9-17.
(Hymenoptera: Encyrtidae) and Tetrastichus planipennisi [25] Jang, S.A. and Park, C.G. (2010). Gymnosoma rotundatum (Diptera:
(Hymenoptera: Eulophidae) in China. Biological Control 42, pp. 61-71. Tachinidae) attracted to the aggregation pheromone of Plautia stali
[22] Abell, K.J., Duan, J.J., Bauer, L., Lelito, J.P. and Van Driesche, R.G. (Hemiptera: Pentatomidae). Journal of Asia-Pacific Entomology 13, pp.
(2012). The effect of bark thickness on host partitioning between 73-75.
Tetrastichus planipennisi (Hymen: Eulophidae) and Atanycolus spp. [26] Ewers, R.M., Fayle, T.M., Foster, W.A., Snaddon, J.L. and Turner, E.C.
(Hymen: Braconidae), two parasitoids of emerald ash borer (Coleop: (2011). The impact of oil palm expansion on environmental change:
Buprestidae). Biological Control 63, 320-325. Putting conservation research in context. Environmental Impact on
[23] Yang, S. Duan, J.J., Lelito, J. and Van Driesche, R. (2012). Biofuels 1, pp. 579-586.
Multiparasitism by Tetrastichus planipennisi (Hymenoptera: [27] Reid, N., McDonald, R.A. and Montgomery, W.I. (2010).
Eulophidae) and Spathius agrili (Hymenoptera: Braconidae): Homogeneous habitat can meet the discrete and varied resource
Implication for biological control of the emerald ash borer (Coleoptera: requirements of hares but may set an ecological trap. Biological
Buprestidae). Biological Control. Conservation 143, pp. 1701-1706.

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