First Report on the Occurrence of the Braconid parasitoid Opius monilicornis on the Chickpea Leaf Miner Liriomyza cicerina in Tunisia

Abstract

Surveys were conducted during 2016 and 2017 in chickpea crops to document the parasitoid species of the chickpea leaf miner (Liriomyza cicerina) in Beja and Kef sites (north-west of Tunisia). One braconid wasp species namely Opius monilicornis was recorded for the first time as parasitoid on L. cicerina larvae. Larvae parasitism was observed from the end of March onwards and reached its peak during April coinciding with the second annual generation of the pest. Parasitism was noticed only on the second and third instars leaf miner larvae. The parasitoid abundance was higher in Beja site compared to Kef. In winter chickpea crops, parasitism rates during 2016 and 2017 ranged from 11.44 to 17.95% while in spring they fluctuated from 11.96 to 19.77%.

Full text

Tunisian Journal of Plant Protection 93 Vol. 13, No 1, 2018
First Report on the Occurrence of the Braconid parasitoid
Opius monilicornis on the Chickpea Leaf Miner Liriomyza
cicerina in Tunisia
Abir Soltani, Faculté des Sciences de Bizerte, 7021 Zarzouna Bizerte, Université de
Carthage, Tunisia, Ahmet Beyareslan, Department of Biology, Faculty of Arts and
Sciences, Bitlis Eren University, 1300 Bitlis, Turkey, Soumaya Haouel-Hamdi, Laboratoire
de Biotechnologie Appliquée à l’Agriculture, Institut National de la Recherche Agronomique
de Tunisie, Université de Carthage, Tunisia, Arbia Bousselmi, Faculté des Sciences de
Bizerte, 7021 Zarzouna Bizerte, Université de Carthage, Tunisia, Moez Amri, International
Center for Agricultural Research in the Dry Areas, Rabat, Morocco, and Jouda Mediouni-
Ben Jemâa, Laboratoire de Biotechnologie Appliquée à l’Agriculture, Institut National de la
Recherche Agronomique de Tunisie, Université de Carthage, Tunisia
__________________________________________________________________________
ABSTRACT
Soltani, A., Beyareslan, A., Haouel-Hamdi, S., Bousselmi, A., Amri, M., and Mediouni-
Ben Jemâa, J. 2018. First report on the occurrence of the braconid parasitoid Opius
monilicornis on the chickpea leaf miner Liriomyza cicerina in Tunisia. Tunisian Journal
of Plant Protection 13 (1): 93-100.
Surveys were conducted during 2016 and 2017 in chickpea crops to document the parasitoid species of
the chickpea leaf miner (Liriomyza cicerina) in Beja and Kef sites (north-west of Tunisia). One
braconid wasp species namely Opius monilicornis was recorded for the first time as parasitoid on L.
cicerina larvae. Larvae parasitism was observed from the end of March onwards and reached its peak
during April coinciding with the second annual generation of the pest. Parasitism was noticed only on
the second and third instars leaf miner larvae. The parasitoid abundance was higher in Beja site
compared to Kef. In winter chickpea crops, parasitism rates during 2016 and 2017 ranged from 11.44
to 17.95% while in spring they fluctuated from 11.96 to 19.77%.
Keywords: Braconidae, chickpea, leaf miner, Opius monilicornis, parasitism
__________________________________________________________________________
Leaf miner flies are a highly
diverse group of exclusively
phytophagous species and occur
worldwide (Shahreki et al. 2012). The
genus Liriomyza comprises numerous
species that are economically important
pests of many agricultural crops including
Corresponding author: Jouda Mediouni Ben Jemâa
Email address: joudamediouni1969@gmail.com
Accepted for publication 16 January 2018
chickpea (Naresh and Malik 1986).
Liriomyza cicerina is the most important
pest that causes significant damages on
chickpea crops in West Asia and North
Africa and the Mediterranean region
(Cardona 1983; Çikman and Civelek
2006; El-Bouhssini et al. 2008; Soltani et
al. 2016). Damages are caused by larvae
consuming the mesophyll of leaves and
the formation of holes and galleries with
different shapes in the leaf tissue which
reduce the photosynthetic capacity of
infested leaves (Çikman 2006).

Tunisian Journal of Plant Protection 94 Vol. 13, No 1, 2018
In Tunisia, chickpea is ranked as
the second major cultivated food legume
crop after faba bean (Ouji et al. 2016).
Fewer insecticidal treatments were
undertaken in chickpea crops. Thus, as
reported by Minkenberg and van Lenteren
(1986), in such agricultural systems using
infrequent pesticide applications, partial
to complete control of agromyzid leaf
miners is often the result of the abundant
parasite fauna action. Consequently, in
this work, we undertake a first survey to
identify natural occurring parasitoids on
L. cicerina larvae. In these regards,
Heimpel and Meloche (2001) reported
that a number of parasitoids of leaf
miners have been recorded throughout the
world. In addition, more than 140 species
of parasitoids as natural enemies of
Liriomyza have been reported (Liu et al.
2009). Braconid species (Hymenoptera:
Braconidae) are among natural enemy’s
assemblages of agromyzid leaf miners
(Gratton and Welter 2001). Among
braconids, Opius monilicornis is a
primary parasitoid on agromyzid leaf
miners including L. cicerina (Çikma et al.
2008).
This paper reports first
investigations on L. cicerina parasitoid
species from the Braconidae family.
Herein, we report the key morphological
characters of Opiu smonilicornis and we
present its parasitism rates in two regions
of north-west Tunisia (Kef and Beja).
MATERIALS AND METHODS
Study sites.
The study was carried out over a
2-year period (2016 and 2017) in
chickpea fields from two sites located in
north-west of Tunisia: Beja
(36°44'56.83''N 9°12'50.24''E) and Kef
(36°07'13.96"N 8°43'21.39"E). The sites
belonged respectively to sub-humid and
semi-arid bioclimatic stages. For this
study, the sampling was made from Beja
1 and Amdoun varieties (winter and
spring varieties, respectively).
Sampling.
Sampling was carried out during
the period from March to May each year.
Thirty chickpea leaves (≈ 360-450
leaflets) harboring insect mines were
weekly sampled from the two sites Beja
and Kef. Samples were kept in a
transparent plastic boxes closed with
cotton ball and covered with muslin at
25± 2ºC, 70±5% RH and 14:10 h (L:D)
photoperiod until the emergence of adults
of both the pest and the parasitoids. After
emergence, both pest and parasitoids
specimens were conserved in 70%
ethanol and stored at -4°C until
identification.
Identification.
The emerged braconids were
identified by Professor Ahmet Beyarslan
(Department of Biology, Faculty of Arts
and Sciences, Bitlis Eren University,
Bitlis, Turkey). Specimens were
morphologically identified based on
taxonomic identification keys (Fischer
1972, 1977, 1986, 1987).
Assessment of parasitism rate.
For O. monilicornis, parasitism
rate was determined according to Russell
(1987) formula as following:
Rate of parasitism (%) =
   
      
× 100
Statistical analysis.
All statistical analyses of
individual number of parasitoids O.
monilicornis were performed using the
"SPSS statistical software version 20.0.
Armonk, NY: IBM Crop". Differences in
values of each year or season-sown crops
and sites were tested by one-way
ANOVA followed by Duncan test. All
values given were the means of three

Tunisian Journal of Plant Protection 95 Vol. 13, No 1, 2018
replications and were expressed as the
mean ± standard deviation. Significant
differences are reported as P
< 0.05.
RESULTS
Parasitoid identification.
Opius monilicornis belongs to the
order of Hymenoptera, super family
Chalcidoidea, family Braconidae and
subfamily Opiinae. This species has been
reported as a parasitoid of L. cicerina in
Syria (El-Bouhssini et al. 2008), Turkey
(Çikman et al. 2006), Iran, Jordan,
Morocco, Moldova, Spain, and Algeria
(Ghahari et al. 2010; Khajeh et al.2014).
O. monilicornis had long antennae
as body, 16- or 17-flagellomeres (Fig
1.1). The basal flagellomeres are 1.8
times as long as wide, middle
flagellomeres and the rest not more than
1.5 times as long as wide; most
flagellomeres clearly separated from each
other, like a string of pearls, 2 or 3
sensillae visible in lateral view, the
numerous hairs shorter than the
flagellomeres wide (Fig 1.2).
The mesosoma is one-third times
as long as high, upper side rather flat. The
mesoscutumis about as wide as long,
lateral lobes weakly rounded, declivity
straight, dorsal fovea punctiform, notauli
only anteriorly indicated; sides on
posterior half margined. Only a few hairs
occurred on the declivity and along the
imaginary course of the notauli (Fig 1.3).
The scutellum is longer than wide, axillae
are absent. The rest of the mesosoma is
smooth (Fig 1.4). Propodeumis fused with
the metapleuron, no suture between them,
lateral spiracles are present. All furrows
of the side are smooth (Fig 1.5). Hind
femur is 5 times as long as wide, also the
other ones are short and thick (Fig 1.1).
For wings, pterostigma is
cuneiform; radiusis arising from basal
third. First section of radius is one-third
as long as pterostigma wide, while second
section of radius is about half as long as
cubital vein; the third section of radius, is
2 times as long as second section of
radius, curved inwards, radial cell ending
before tip of wing, second radial cell
narrowed distal, discoideus hardly long
than nervusrecurrens, nervus almost
interstitial, brachial cell closed,
nervusparallelus arising from the middle
of the distal side of brachial cell (Fig 1.7).
For, the metasoma, first tergite 1.5 times
as long as hind wide, parallel-sided
behind, a little narrowed in front, smooth
and shining, dorsal carinae developed on
basal third (Fig 1.6). Ovipositor sheaths
hidden or clearly visible, the rest of
metasoma without sculpture, the
projecting part a third as long as the
metasoma, the hypopygium retracted (Fig
1.8).
Hosts and distribution.
This species has been reported as a
parasitoid of L. cicerinain Turkey
(Çikman et al. 2008). It was also reported
from L. congesta, L. pusilla, Ophiomyza
sp., Phytomyza atricornis, Asphondylia
verbasci (Fischer and Koponen 1999).
This parasitoid occurred in Syria, Jordan,
Turkey (Çikman et al. 2008), Iran
(Ghahari et al. 2012), Morocco (Lahmer
and Zeouienne1987), and Algeria (Papp
1982).
Parasitism rate.
Results regarding the parasitism
rates of the braconid O. monilicornis
during 2016 and 2017 were reported in
Fig. 2. Results revealed that this species
was very abundant in both sites (Beja and
kef). The correspondent parasitism rates
during 2016 were 23.2% in Beja and
21.05% in Kef for winter variety, while
for the spring one parasitism rates were
18.5%, in Beja and 17.3% in Kef. During
2017, an increase in parasitism rates was
observed during June. Indeed, the peaks

Tunisian Journal of Plant Protection 96 Vol. 13, No 1, 2018
of parasitism rates were 35.8% for winter
variety and 35.11% for spring variety in
Beja. Regarding Kef site, parasitism rates
were 21.4% for winter variety against
28% for spring variety.
Fig. 1. (1) Opius monilicornis (adult ♂) (1) Antenna, (2) Mesoscutum (3)
Mesosoma (4) Scutellum (5) Hind Femur (6) Lateral view of metasoma, and (7)
Wings (8) Ovipositor.

Tunisian Journal of Plant Protection 97 Vol. 13, No 1, 2018
Fig. 2. Evolution of parasitism rates (%) Opius monilicornis during 2016 and 2017 in Beja and Kef sites.
Fig. 3 reported the emergence of
O. monilicornis according to season-sown
crops and sites. Results showed that the
distribution depends on crops (winter or
spring chickpea) and year. Statistical
analysis showed the presence of high
significant differences between the two
sites (F = 37.91, P
< 0.01). Additionally,
statistical analysis revealed that in Beja
site, O. monilicornis presented significant
differences between winter and spring
chickpea varieties for 2017, while no
significant differences between winter
and spring crops were observed for 2016.
The braconid O. monilicornis
represented 44.09 and 43.2% of the total
emerged insects in Beja and Kef,
respectively, during 2016 and 52.5 and
44.9% during 2017. Furthermore, results
indicated that Beja site differed from Kef
by the number of individual parasitoids
during both years for winter and spring
varieties.
0
10
20
30
40
50
2017
Winter variety
Spring variety
2017
Winter variety
Spring va riety
0
10
20
30
40
50
15
March
05
April
16
April
01
May
16
May
01
June
16
June
2016
Winter variety
Spring va riety
15
March
05
April
16
April
01
May
16
May
01
June
16
June
2016
Winter variety
Spring va riety
Beja Kef
Parasitism rates (%)
Parasitism rates (%)

Tunisian Journal of Plant Protection 98 Vol. 13, No 1, 2018
Fig. 3. Distribution of Opius monilicornis according to cropping season and years in Beja and Kef sites.
Different letters indicated significant differences (P < 0.05) for each year among winter and spring chickpea
varieties (lowercase letters); and among years for each winter or spring crops (uppercase letters). Each value is
the mean ± SD of three replicates.
DISCUSSION
Agromyzid leaf miners are known
to have rich natural enemy communities
(Gençer, 2004). Numerous studies have
been reported on the natural enemies of
the Agromyzidae including L. cicerina in
various countries (Asadi et al. 2006;
Baideng 2016; Fathipour et al. 2006;
Heinz and Parrella 1990; Lahmar and
Zeouienne 1990; Sivapragasam et al.
1999). However, no previous studies were
conducted on the natural enemies of the
chickpea leaf miner in Tunisia. Thus, the
present work carried out the first
investigations on parasitoids occurring on
L. cicerina in chickpea fields in Tunisia.
This study reported the first occurrence of
the braconid wasp O. monilicornis with
an interesting parasitism rate of 19.77%
in Beja during 2017. According to
previous records, this parasitoid belongs
to the superfamily of Ichneumonidea
(Murphy and LaSalle 1999). Previous
investigations on L. cicerina parasitoid
fauna revealed that O. monilicornis is one
of the parasitoid complex of chickpea leaf
miner. In this regards, Çikman et al.
(2008) reported that in Sanhurfa region in
Turkey, the braconid O. monilicornis was
one of the L. cicerina parasitoid fauna.
Earlier, Hincal et al. (1996) and Gençer
(2004) reported respectively O.
monilicornis as parasitoid attacking L.
cicerina in Izmir, Denizil, Uşakand
Ankara province (Turkey). Besides, our
results agreed with those obtained in
Syria which revealed that the parasitoid
O. monilicornis was found to be the most
effective against the chickpea leaf miner,
compared with Diglyphusisaea, as the
parasitism reached about 70% (El-
Bouhssini et al. 2008). In Morocco,
Lahmar and Zeouienne (1990) identified
O. monilicornis as the only parasitoid of
L. cicerina achieving a parasitism rate of
20.35%. Such activity seems to be
important compared to results
accomplished in Turkey where O.
monilicornis occurred with a low
parasitism rate of 3.27% (Çikman et al.
2008). The relatively higher parasitism
rate can suggest that this parasitoid is an
important mortality factor in the
dynamics of leaf miner populations. For
this reason, it can be considered as a
potential biocontrol agent against this
pest.
ACKNOWLEDGEMENTS
Authors thank the Regional Field Crop
Research Center of Beja (CRRGC) and the Regional
Station of the National Agricultural Research
Institute of Tunisia (INRAT) in Kef for fields work.
Moreover, we would like to express our gratitude to
Mr. David Mercati, Department of Life Sciences
University of Siena, Italy for his assistance in the
photographic work.
a, A a, A
a, B
b, B
0
20
40
60
80
100
Winter Sp ring Winter Spring
2016
2017
Beja
a, A a, A a, A a ,A
0
20
40
60
80
100
Winter Sp ring Winter Spring
2016 2017
Kef
Number of individuals
Number of individuals

Tunisian Journal of Plant Protection 99 Vol. 13, No 1, 2018
__________________________________________________________________________
RESUME
Soltani A., Beyareslan A., Haouel-Hamdi S., Bousselmi A., Amri M. et Mediouni-Ben
Jemâa J. 2018. Premier signalement du parasitoïde Braconidae Opius monilicornis sur
la mineuse du pois chiche Liriomyza cicerina en Tunisie. Tunisian Journal of Plant
Protection 13 (1): 93-100.
Des prospections ont été menées en 2016 et 2017 dans les cultures de pois chiche pour étudier les
parasitoïdes de la mineuse (Liriomyza cicerina) du pois chiche dans les sites de Béja et du Kef (Nord-
Ouest de la Tunisie). Une espèce de Braconidae Opius monilicornis a été enregistrée pour la première
fois comme parasitoïde sur les larves de L. cicerina. Le parasitisme des larves a été observé à partir de
la fin du mois de mars et a atteint son pic en avril, coïncidant avec la deuxième génération annuelle du
ravageur. Le parasitisme n'a été observé que sur les larves des deuxième et troisième stades.
L'abondance du parasitoïde était plus élevée dans le site de Béja que dans celui du Kef. Dans les
cultures de pois chiche d'hiver, les taux de parasitisme durant 2016 et 2017 ont varié de 11,44 à 17,95%
tandis que dans celles de printemps, ils ont fluctué de 11,96 à 19,77%.
Mots clés: Braconidae, mineuse des feuilles, Opius monilicornis, parasitisme, pois chiche
__________________________________________________________________________
ﺺﺨﻠﻣ
ﻲﻧﺎﻁﻠﺳ، ﺭﻳﺑﻋ ﺩﻣﺣﺃﻭ ﻥﻼﺳﺭﻳﺑ ﺔﻳﻣﺳﻭ ﻝﺍﻭﺣ -ﻱﺩﻣﺣ ﺔﻳﺑﺭﻋﻭ ﻲﻣﻟﺎﺳﻭﺑ ﺯﻌﻣﻭ ﻱﺭﻣﻋ ﺓﺩﻭﺟﻭ ﻲﻧﻭﻳﺩﻣ-ﻥﺑ ﺔﻋﺎﻣﺟ.
.2018 ﺍ ﻦﻋ ﻝﻭﻷﺍ ﺮﻳﺮﻘﺘﻟﺩﻮﺟﻭ ﻞﻴﻔﻁ ﻱﺪﻧﻮﻛﺍﺮﺑ Opius monilicornis ﻰﻠﻋﻟﺍ ﺺﻤﺤﻟﺍ ﻕﺍﺭﻭﺃ ﺔﻘﻓﺎﻧ ﺓﺮﺸﺤ
Liriomyza cicerina
ﻲﻓ ﺱﻧﻭﺗ. 13 (1): 93-100. Tunisian Journal of Plant Protection
ﺕﻳﺭﺟﺃ ﺔﺳﺍﺭﺩ ﺔﻳﺋﺎﺻﻘﺗﺳﺍ ﻲﺗﻧﺳ 2016 ﻭ2017 ﻲﻓ ﻉﺭﺍﺯﻣ ﺹﻣﺣﻟﺍ ﻝﻭﺣ ﺕﺎﻳﻠﻳﻔﻁ ﻟﺍﺓﺭﺷﺣ ﺔﻘﻓﺎﻧ ﻕﺍﺭﻭﺃ ﺹﻣﺣﻟﺍ
(Liriomyza cicerina) ﻲﻓ ﻲﻌﻗﻭﻣ ﺔﺟﺎﺑ ﻑﺎﻛﻟﺍﻭ )ﻝﺎﻣﺷﻟﺍ ﻲﺑﺭﻐﻟﺍ ﺱﻧﻭﺗﻟ.( ﺩﻗﻭ ﻡﺗ ﻝﻳﺟﺳﺗ ﻉﻭﻧ ﻥﻣ ﻱﺩﻧﻭﻛﺍﺭﺑﻟﺍ
)Braconidae( )Opius monilicornis ﺕﺎﻗﺮﻳ ﻰﻠﻋ ﻞﻴﻔﻄﻛ ﺓﺮﻣ ﻝﻭﻷ ( L. cicerina ﻆﺣﻮﻟ ﺪﻗﻭ . ﻞﻔﻄﺗﻦﻣ ﺕﺎﻗﺮﻴﻟﺍ
ﺱﺭﺎﻣ ﺔﻳﺎﻬﻧﻢﺛ ﺮﻬﺷ ﻝﻼﺧ ﻪﺗﻭﺭﺫ ﻎﻠﺑﺃ ﺕﺎﻗﺮﻳ ﻰﻠﻋ ﻂﻘﻓ ﻞﻔﻄﺘﻟﺍ ﻆﺣﻮﻟ ﺪﻗﻭ .ﺔﻓﻶﻟ ﻲﻧﺎﺜﻟﺍ ﻱﻮﻨﺴﻟﺍ ﻞﻴﺠﻟﺍ ﻊﻣ ﻦﻣﺍﺰﺘﻟﺎﺑ ﻞﻳﺮﻓ
ﺑ ﺔﻧﺭﺎﻘﻣ ﺔﺟﺎﺑ ﻊﻗﻮﻣ ﻲﻓ ﻰﻠﻋﺃ ﻞﻴﻔﻄﻟﺍ ﺓﺮﻓﻭ ﺖﻧﺎﻛﻭ .ﺔﻠﺋﺎﻌﻟﺍ ﺓﺮﺸﺤﻠﻟ ﺚﻟﺎﺜﻟﺍﻭ ﻲﻧﺎﺜﻟﺍ ﺭﻮّﻄﻟﺍ ﻊﻗﻮﻤ ﺕﻻﺪﻌﻣ ﺖﺣﻭﺍﺮﺗﻭ .ﻑﺎﻜﻟﺍ
ﻱﻮﺘﺸﻟﺍ ﺺﻤﺤﻟﺍ ﻉﺭﺍﺰﻣ ﻲﻓ ﻞﻔﻄﺘﻟﺍ ﻝﻼﺧ2016 ﻭ2017 ﻦﻣ11,44 ﻰﻟﺇ17,95% ﻦﻣﻭ11,96 ﻰﻟﺇ19,77% ﻲﻓ
ﻉﺭﺍﺯﻣ ﺹﻣﺣﻟﺍ ﻲﻌﻳﺑﺭﻟﺍ.
ﺔﻴﺣﺎﺘﻔﻣ ﺕﺎﻤﻠﻛ
: ،ﻞﻔﻄﺗ،ﻕﺍﺭﻭﻷﺍ ﺔﻘﻓﺎﻧ ،ﺺﻤﺣ Braconidae ،Opius monilicornis
__________________________________________________________________________
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