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First record of the feather-legged fly Trichopoda pennipes (Fabricius, 1781) (Diptera Tachinidae) a parasitoid of the southern green stink bug Nezara viridula (Linnaeus, 1758) (Hemiptera Pentatomidae) in Algeria

Authors:
INTRODUCTION
The parasitoid tachinid species Trichopoda pen-
nipes (Fabricius, 1781) (Diptera Tachinidae) is na-
tive to the Nearctic region (Salerno et al., 2002).
This species is an imaginal and infrequently a
nymphal parasitoid of many different bugs (Harris
& Todd, 1981; Ruberson et al., 2010). In its natural
geographic area, its host range includes several
species of various Heteroptera families as Alydi-
dae, Coreidae, Pentatomidae, and Pyrrhocoridae
(Francati et al., 2019). Besides, the introduction
of Nezara viridula (Linnaeus, 1758) (Hemiptera
Pentatomidae) into the North of America in 1700,
make it as an additional host of T. pennipes (Jones,
1988). Trichopoda pennipes is commonly known
as the feather-legged fly because of the feathers
existing on the posterior legs (Worthley, 1924).
This fly is an endoparasitoid of the southern green
stink bug Nezara viridula adults and final instars
(Todd, 1989). It was introduced from the USA into
Australia to control bugs, especially Nezara
viridula (Waterhouse, 1998). In Europe, this ta-
chinid fly was accidentally introduced to Italy and
it was detected for the first time in 1988 near Rome
(Colazza et al., 1996). It was recorded in several
other Mediterranean countries like southern France
(Tschorsnig et al., 2000), Spain (Peris, 1998;
First record of the feather-legged fly Trichopoda pennipes
(Fabricius, 1781)
(Diptera Tachinidae) a parasitoid of the
southern green stink bug Nezara viridula
(Linnaeus, 1758)
(Hemiptera Pentatomidae) in Algeria
Ahlem Meriem*, Lina Aitaider, Bahia Doumandji-Mitiche & Abderrahmane Chebli
Lab. protection des végétaux en milieux agricoles et naturels contre les déprédateurs des cultures. Département de
Zoologie Agricole et Forestière. ENSA, El Harrach, ES1603, Algeria; e-mail: l.aitaider@edu.ensa.dz,
b.doumandji@ensa.dz, a.chebli@edu.ensa.dz
*Corresponding author, e-mail: a.meriem@edu.ensa.dz; meriemahlem94@gmail.com
Biodiversity Journal, 2021, 12 (3): 561
566 https://doi.org/10.31396/Biodiv.Jour.2021.12.3.561.566
Between 2018 and 2019 we conducted a comprehensive study on the southern green stink bug
Nezara viridula (Linnaeus, 1758) (Hemiptera Pentatomidae) for the first time in Algeria. On
August 2019 specimens of the feather-legged fly Trichopoda pennipes (Fabricius, 1781)
(Diptera Tachinidae) were detected for the first time from reared parasitized adults of Nezara
viridula (L.) (Hemiptera: Pentatomidae) which were sampled from tomato crop in an
agricultural region called Ouled Hadedj in the eastern part of Mitidja in Algeria. Trichopoda
pennipes is an endoparasitoid of the stink bug Nezara viridula. This study provides the first
record of this Nearctic tachinid fly and its genus in Algeria which can also be a very useful
addition for biodiversity and for the geographical distribution of this species. Morphological
description of the detected parasitoid species and Colored photographs of the parasitoid and
parasitized host are provided.
Biological control, biodiversity, distribution, parasitism, tomato crop, Mitidja.
Received 25.02.2020; accepted 30.04.2021; published online 24.07.2021
KEY WORDS
ABSTRACT
AHLEM MERIEM ET ALII
562
Tschorsnig et al., 2000), Slovenia (De Groot et al.,
2007), Netherlands (Zeegers, 2010), Albania
(Tschorsnig et al., 2012), Hungary (Sándor, 2014)
and Portugal (Pétremand et al., 2015). In 2006 ex-
actly in Switzerland, T. pennipes was identified for
the first time in Ticino (Obrecht, 2014; Pétremand
et al., 2015). It was introduced and well established
in Hawaii for the biological control of Nezara
viridula (Davis, 1964; Michael, 1981). In Egypt, the
species was detected for the first time from para-
sitized adults and nymphs of the southern green
stink bug Nezara viridula (El-Hawagry et al., 2020).
The fly has generally 2 to 3 generations per year.
The female can lay one or more whitish plano-con-
vex, non-incubated eggs upon the body of the adult
and occasionally on final nymphal instar of the bug.
The majority of eggs are placed on the sides of the
thorax (Worthley, 1924; Salerno et al., 2002). After
hatching, the larvae of Trichopoda pennipes bore
the tegument of the host and enter inside and feed
on its fluids for about 2 weeks. Then just one mature
larva leaves the bug’s body through its anal extremity
and form puparia, subsequently the bug dies (Worth-
ley, 1924). Pupation lasts between 2 to 4 weeks
(Cargnus et al., 2011) then the emerged adults of T.
pennipes feed on nectar (Worthley, 1924). In Algeria,
Trichopoda pennipes and its host Nezara viridula
have not been studied before. In this study we present
the first record of the feather-legged fly T. pennipes.
The study includes its morphology and biology.
MATERIAL AND METHODS
Study area
This study was carried out on 1 August 2019 in
Ouled Hadedj in the eastern part of Mitidja in Algeria
(36º4537, 23N, 3º2820, 52E) (Fig. 1) as a part of
a complete comprehensive survey of the pest Nezara
viridula which was conducted between 2018 and
2019. The bugs were collected from tomato crop by
hand sampling which was a very useful technique
to facilitate and to make sure the recovery of the in-
dividuals alive. To study the behaviour of the bug,
the individuals (adults and nymphs) were put for
rearing in a plastic box (30 cm, 20 cm, 12 cm) in
which we added Solanaceae plants as tomato and
green pepper to ensure the life continuity of the bugs
and they were transferred to an insectarium which
is a room of constant temperature about 25°C in the
Department of Zoology in the Superior National
Agronomic School, Algeri.
There were 60 individuals of the southern green
stink bug Nezara viridula, which were collected
to be reared. The rearing of these bugs enabled us
to observe that most of them were parasitized
(about 40 parasitized individuals). They appeared
carrying yellowish white tiny eggs on several parts
of the body like head, thorax and scutelum from
anterior and posterior sides (Fig. 2). The majority
die before the emergence of the parasitoid, only 8
parasitized individuals remained, seven of them
were adults and the eighth one was a final nymphal
instar. We isolated each one of these 8 parasitized
bugs separately in Petri dishes numbered from 1
to 8, fed them with tiny slices of green pepper and
tomato. Seven mature maggots of Trichopoda pen-
nipes had emerged from the seven parasitized adults
of Nezara viridula. The parasitized final nymphal
instar died during the ecdysis. From the seven pu-
paria formed there were just 4 adults of T. pennipes
have been emerged. This study was based on 4
adult individuals (3 males and 1 female) of T. pen-
nipes. The first of these individuals were a male
found in 17 August 2019 in the Petri dish. Two an-
other males were found in another two Petri dishes
in 26 August 2019, after one day in 27 August
2019 a female of T. pennipes were found in another
Petri dish. Both of the parasitoid and its host were
identified and confirmed in the laboratory of zool-
ogy department in the Higher National Agronomic
School (ENSA), Algiers. The identification was
made by a specialist under a binocular magnifying
glass using dry specimens and relying on searching
Figure 1. Location of the study region: Ouled Hadadj
in the eastern part of Mitidja in Algeria.
in several references and articles such as Worthley
(1924), O’Hara (2013), Tschorsnig (2017). The
typical host of the tachinid fly is the cosmopolitan
pentatomid Nezara viridula which was confirmed
relying on the insects’ collection of the depart-
ment’s insectarium.
RESULTS
Observation on Parasitoidsm
We noticed that the parasitized bugs have a dif-
ferent behavior compared with the non-parasitized
ones; the parasitized bugs were found very slow
and stopped feeding on the green pepper and tomato
slices. A parasitized adult of N. viridula in Petri
dish number 1 was a female carrying four eggs,
two were fixed on its thorax edges and two on the
prosternum. On 2 August 2019, a maggot left the
bug’s body from the abdominal extremity and after
about one hour formed its puparium, immediately
after the parasitized female died. A male of T. pen-
nipes (Fig. 3) emerged from the puparium 15 days
later. On 5 August 2019, and exactly in Petri dish
number 4 a second maggot left the male bug’s body
and it was a really thin maggot, it formed its pu-
parium but it didn’t produce any fly. Later on 10
First record of Trichopoda pennipes a parasitoid of Nezara viridula in Algeria 563
Figure 2. Specimens of Nezara viridula collected carrying yellowish white tiny eggs
of Trichopoda pennipes on several parts of the body.
Figure 3. Specimens of Trichopoda pennipes emerged from the parasitized bugs Nezara viridula. Male
of Trichopoda pennipes (to the left). Female of Trichopoda pennipes (to the right).
August 2019, other 3 maggots left the bodies of 3
female bugs in Petri dishes number 7, 5 and 2 re-
spectively. Sixteen days later, we found two male
of the feather-legged fly emerged in Petri dishes
number 7 and 2. One day later a female of T. pen-
nipes emerged from the puparium in Petri dish
number 5 and it was the only female (Fig. 3). The
last two parasitized bugs in Petri dishes number 3
and 6 died soon after the maggot exit on 17 and 22
August 2019 respectively and didn’t produce any
fly. About The parasitized final nymphal instar died
in Petri dish 8 during the ecdysis before the maggot
exit. We observed that its exoskeleton was carrying
an egg on the corner between the head and the tho-
rax (Fig. 4).
Morphological description of Trichopoda
pennipes detected in Algeria
Four adults of T. pennipes have been emerged
from their puparia, 3 males and one female. In gen-
eral, the males’ size is about 7 mm and for the fe-
male is 10 mm; they have a remarkable colored ap-
pearance. The color golden-yellow is centered as
stripes on the head and the thorax. The abdomen is
orange and the wings are brown. They also have a
special identification feature which is the feathers
on the posterior leg exactly in the tibia which appear
obviously (Fig. 5).
The difference between the two sexes is not dif-
ficult. We distinguished male and female by their
specific coloration. Generally, the three males have
a yellowish-orange appearance. Two large shining
yellow-golden lines around the eyes in the head,
the thorax has three thick vertical black strips sur-
rounded by a bright yellow-golden color in the rest
of the thorax surface, the abdomen is dark in the
top, and then it goes to orange in the middle. The
wing is characterized by a color gradation. At the
edge of the wing of the male, there is a light brown
large strip, which goes to dark black in the center.
The female appearance is darker than the males. It
has a black abdomen, a black thorax and black
wings with a grey-brown top border.
AHLEM MERIEM ET ALII
564
Figure 4. Egg of T. pennipes in the exoskeleton
of the final nymphal instar of N. viridula.
Figure 5. Feathered leg.
DISCUSSION
It is difficult to know how and when and from
where exactly this parasitoid arrived to Algeria, as
this is the first time to study the southern green
stink bug N. viridula in Algeria. T. pennipes may
have reached Algeria from other nearby Mediter-
ranean countries like Spain, Italy and France, where
it abundantly exists. The use of the tachinid fly as a
biocontrol agent is very important to control N.
viridula as some attempts of its introduction were
successful in Hawaii and California (Davis, 1964;
Pickett et al., 1996). Salerno et al. (2002) observed
a maximum rate of parasitism of nearly 25 % of N.
viridula populations by T. pennipes in various crops
distributed in two areas of central Italy. A 100%
rate of parasitism of N. viridula has been reported
in Hawaii (Davis, 1964; Michael, 1981). However,
some experiments of the T. pennipes introduction
and establishments have failed in Australia between
1940 and 1950 (Michael, 1981) and recently in
1990 (Waterhouse, 1998). Michael (1981) supposed
that the failure of the fly’s establishment after its
introduction and efforts of rearing back to the in-
sufficient number of this parasitoid.
CONCLUSIONS
The rearing of the southern green stink bug N.
viridula from tomato crop in the region of Ouled
Hadedj in the eastern part of Mitidja, Algeria which
has been done for a comprehensive study of this
pest detect the presence of some parasitized indi-
viduals. The isolation and the monitoring of these
parasitized bugs revealed the first record of the par-
asitoid T. pennipes which can be a very useful ad-
dition for the biodiversity of the country and for
the distribution of this tachinid. The parasitoid can
be tested as a biological control agent to solve the
wide fast reproduction and spread of the southern
green stink bug.
ACKNOWLEDGEMENTS
We are very grateful to Mr. Doumandji Salaheddine,
Professor at the department of Zoology in the
Higher National Agronomic School (ENSA, El Har-
rach/Algiers, Algeria) for his help in the identifica-
tion and the confirmation of the species and also
Professor Tschorsnig Hans-Peter, an entomologist
that specializes in caterpillar flies at the Natural
History Museum in Stuttgart, Germany for the con-
firmation of the genus of the species and for giving
us the information about the geographic distribution
of it. We would also like to extend our special thanks
to Mr. Hamitouch Mohamed, agricultural engineer
from the department of agricultural hydraulics/Ge-
nie rural in the Higher National Agronomic School
(ENSA, El Harrach/Algiers, Algeria) for his help
in achieving the map of the study site.
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First record of the feather-legged fly Trichopoda pennipes (Diptera Tachinidae)
a parasitoid of the southern green stink bug Nezara viridula (Hemiptera Pentatomidae) in Algeria
7
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