Parasitoids of the Almond Bark Beetle Scolytus amygdali in Tunisia

Parasitoids of the Almond Bark Beetle Scolytus amygdali in
Tunisia
Asma Zeiri, Département de Biologie, Faculté des Sciences Bizerte, Université de
Carthage, 7021, Zarzouna, Bizerte, Tunisia, Mohamed Braham, Laboratoire
d’Entomologie, Centre Régional des Recherches en Horticulture et Agriculture
Biologique, Université de Sousse, 4042 Chott-Mariem, Sousse, Tunisia, and
Mohamad Braham, Institut de l’Olivier, Unité Spécialisée de Sousse, 4061 Ibn
Khaldoun, Sousse, Tunisia.
__________________________________________________________________________
ABSTRACT
Zeiri, A., Braham, M., and Braham, M. 2013. Parasitoids of the almond bark beetle
Scolytus amygdali in Tunisia. Tunisian Journal of Plant Protection 8: 45-56.
Since 2009, the biology and the life cycle of Scolytus amygdali have been studied in Tunisia. Branches
of infested almond, plum, apricot, and peach trees were taken to the laboratory and put in plastic boxes.
Adults of S. amygdali and their natural enemies have been collected. Among the parasitoids found on
S. amygdali, we identified three species belonging to the family Pteromalidae, namely Cerocephala
eccoptogastri with average coefficient of dominance of 53.26%, Cheiropachus quadrum with 14.88%
and Rhaphitelus maculatus with 10.44%. The Eupelmidae parasitoid Eusandalum merceti was
collected in October 2009 and this is the first record of this parasitoid in Tunisia. It was found to be an
ectoparasitoid of the mature larvae and pupae of S. amygdali. Larvae of S. amygdali were also attacked
by an Acari species: Pyemotes sp. Several bioassays were conducted in Petri dishes to evaluate the
damage caused by this mite on the studied beetle. Results showed that it attacks all the developmental
stages of S. amygdali and also the associated hymenopteran parasitoids.
Keywords: Cerocephala eccoptogastri, Cheiropachus quadrum, Eusandalum merceti, parasitoids,
Pyemotes sp., Pteromalidae, Rhaphitelus maculates, Scolytus amygdali, Tunisia
__________________________________________________________________________
Bark beetles are the most
destructive insect pests in coniferous and
fruit trees in both temperate and tropical
climates (30). The almond bark beetle,
Scolytus amygdali, is an important pest
that belongs to the Scolytidae family (4,
14). In Tunisia, it was reported on fruit
trees (1, 17, 38, 39, 40) and was also
studied in Morocco (7, 9), Egypt (37)
and Italy (33). The Hymenoptera are
among the most important natural
enemies of bark beetles. According to
Balachowsky (5), their role is much
stronger than the other natural enemies.
For Ruguloscolytus rugulosus (35) and
Phloeotribus scaraboides (8), the rate of
parasitism by Hymenoptera can be
considered as primordial limiting factor.
Several Pteromalidae were reported on S.
amygdali (7, 10, 30, 34, 40). Mendel (30)
mentioned some Pteromalidae species on
other Scolytidae infesting fruit and forest
trees such as S. multistriatus, Rugulosus
mediterraneus. On P. scarabaeoides,
Corresponding Author: Asma Zeiri
Email: [email protected]
Accepted for publication 13 June 2013
Tunisian Journal of Plant Protection
45
Vol. 8, No. 1, 2013
some Pteromalidae were reared by
Benazoun (8), Gonzalez and Campos (21,
22), Russo (33) and Campos and Lozano
(15). They were also reared from other
Scolytidae like Leperisinus varius (28) on
olive, Hylesinus fraxini (31), S. nitidus
(14) and elm bark beetles in Serbia (36).
Parasitoids belonging to Eupelmidae
family were the most recorded on
Scolytidae. Only few species were
reported in Tunisia according to the
Universal Chalcidoidae Database (32). S.
amygdali is also threatened by other
natural enemies including mites (7, 10).
Some species of the genus Pyemotes are
natural enemies of forest insects or stored
product insects. This genus is divided into
two species: P. scolyti and P. ventricosus
(18). Species of the scolyti group are
phoretic on bark beetles (Scolytidae); they
feed only on bark beetle brood or on
immature beetles in the subcortical
habitats; none feeds on adults (18). They
are relatively "venom less" and the host
remains alive for about a day after the
initial attack (18). Doberski (20) analyzed
the mite populations present in elm logs
infested by S. scolytus in England and
reported the infrequent appearance of P.
scolyti. Species of the ventricosus group
are not known to be phoretic (27). At
least some species of mites possess
venom; they inject it into prey, which
causes paralysis and eventual death (27).
The host range includes a variety of hosts.
The aim of this work is to identify
associated parasitoids of the almond bark
beetle and their incidence.
and apricot. Five branches of almond,
peach, apricot, and plum (1-2 cm in
diameter, 30-50 cm in length) infested
with S. amygdali were weekly cut from
trees. The cuttings were transported to the
laboratory for further investigations.
Adults’ rearing.
Starting from December 2009,
branches were cut in pieces of between 15
and 25 cm length and put in plastic
emergence boxes (21 × 21 × 9 cm). Each
box contains 5 cuttings. The rearing of
the insect was performed at 25°C and
16L/8D photoperiod. Emerged S.
amygdali individuals and parasitoids were
daily collected until emergence stopping.
Natural enemies were immediately
collected and the ratio of dominance of a
parasitoid species (RD) was calculated
[RD (%) = Number of each species/Total
number of parasitoids) × 100]. Branches
were also weekly opened and mortality
causes were noted for natural enemies
under the bark. Parasitoids were
examined
under
microscope
for
morphological analysis and photographed
with a Canon Power Shot S50 camera
attached to a stereomicroscope LEICA
(DMLB2), a MZ 12.5 Binocular and a
SEM (Quanta 200 FEI).
Identification of mortality causes.
The emerged parasitoids were
sorted according to their morphological
feature under binocular microscope.
Samples stored in a solution of alcohol
70° were sent to Dr. Gray Gibson and Dr
Mircea-Dan Mitroiu for identification.
Infested animal material with Acari was
observed under stereomicroscope LEICA
(DMLB2) for identification.
MATERIALS AND METHODS
Experimental sites.
The experiments were conducted
in two orchards of fruit trees in the
center-east of Tunisia, delegation of
Jemmal and Souassi. In these orchards,
the almond was the most predominant in
addition to few trees of pear, plum, peach,
Tunisian Journal of Plant Protection
Effect of Acari on bark beetles
population and its parasitoids.
Four Petri dishes were placed in
the same rearing conditions in the
46
Vol. 8, No. 1, 2013
laboratory. Each Petri dish contained
infested larvae with Acari and 20 larvae,
20 nymphae, 20 adults or 20 Raphitellus
maculatus. After 24 h, each Petri dish was
opened under binocular and mortality was
noted.
Pteromalidae (Chalcidoidea). This
species of Pteromalidae Hymenopteran
parasitoids were recorded on S. amygdali
from infested trees and rearing boxes.
Among them, Pteromalidae parasitoids
collected were:
Cerocephala eccoptogastri. This
parasitoid (Fig. 1) was collected from
infested peach tree branches in Jammel
during November 2009 and almond in
Esswassi during Mai 2010 (Table 1).
RESULTS
Hymenopteran parasitoids families of
Scolytus amygdali.
Fig. 1. Cerocephala eccoptogastri, a: Female dorsal view, b: Female ventral view, c: Male dorsal view.
The morphological description
was given by Hedqvist (24). The Fig. 2
shows the Cerocephala collected and
observed under ESM. The antenna of the
female is 9 segmented; the male one is 10
segmented. The head presents an
interantennal crest slightly acute in
profile; upper facial processes forming
distinct pointed teeth. In the thorax, the
pronotum is long. The medial segment is
long, reticulately rugose. Submarginal
vein has a tuft of terminally long hair.
Abdomen has a distinct petiole.
Fig. 2. Details of Cerocephala eccoptogastri (Not to the
same scale). IC: Interantennal crest, Prn: Pronotum.
Tunisian Journal of Plant Protection
47
Vol. 8, No. 1, 2013
It was the main parasitoid recorded
in both sites representing a ratio of
dominance of 53.26% in November 2009
(Table 1). This wasp parasitizes old
larvae and pupae of the beetle.
Rhaphitelus maculatus. This
parasitoid (Fig. 3) was detected in
Esswassi during December 2009 with a
ratio of dominance of 10.44% (Table 1).
It parasitizes larvae of S. amygdali.
Fig. 3. Photo of the male of Rhaphitelus
maculates.
The morphological description
was given by Hedqvist (24). In female
(Fig. 4), the club is with long distal spine.
The funicle is short and highly expanded,
and segments were much wider than
longer. In male, funicular segments are
slender, very long, and densely hairy. R.
maculates parasitizes larvae of S.
amygdali.
Fig. 4. Details of Rhaphitelus maculatus (Not to the same
scale).
Cheiropachus
quadrum.
It
parasitizes S. amygdali larvae (Fig. 5). It
Tunisian Journal of Plant Protection
was detected in December 2009 with a
ratio of dominance of 14.88% (Table 1).
48
Vol. 8, No. 1, 2013
Fig. 5. Photo of female of Cheiropachus quadrum
The morphological description of
C. quadrum, also called Cheiropachus
colon, was given by Hedqvist (24). Front
femur is swollen. The prothorax viewed
from side is much shorter than wider.
Abdomen of female pointed at apex;
forewing may have dark spots. Legs of
male are brown (Fig. 6).
Fig. 6. Details of Cheiropachus quadrum (Not to the same scale).
The location of Pteromalidae and their
abundance are shown in Table 1.
Location and abundance of parasitoids
Pteromalidae.
Tunisian Journal of Plant Protection
49
Vol. 8, No. 1, 2013
Table 1. Abundance of Pteromalidae Parasoitoids of Scolytus amygdali in the period from May
2009 to June 2010 in both orchards located at Souassi and Jemmel
Abondance
Species
Period/locality
rate (%)
September-December 2009 (Souassi)
53.26
Cerocephala eccoptogastri
May-June 2010 (Jemmel)
May-June 2009 (Souassi, Jemmel)
10.44
Rhaphitelus maculatus
September-December 2009 (Jemmel)
Cheiropachus quadrum
September-December 2009 (Jemmel)
Pteromalidae parasitoids of S.
amygdali collected from fruit trees in
Tunisia where the most important group.
Among Pteromalidae reported, the most
abundant species was C. eccoptogastri
(53.26%) followed by Ch. Quadrum
(14.88%) and R. maculatus (10.44%).
14.88
pupae of S. amygdali on almond branches
in the center-east of Tunisia. The wasps
were labeled and identified using a key
adapted from Boucek (13) as a first
recorded species in a first reported
country. Only females were obtained.
This Hymenopteran wasp (Fig. 7)
is classified under the superfamily of
Chalcidoidea, family of Eupelmidae,
subfamily of Calosotinae and the genus of
Eusandalum.
Eupelmidae (Calosotinae). Eusandalum
merceti. Individuals of this species were
obtained during October 2009 as
ectoparasitoids of the mature larvae or
Fig. 7. Female of Eusandalum merceti taken by a Canon Power Shot S50
camera attached to a MZ 12.5 Binocular.
E. merceti, also described under
the name Polymoria merceti, was
identified using the key adapted from
Boucek (13) by Askew and Aldrey (3).
Only females were used for the
identification because they are more
Tunisian Journal of Plant Protection
easily distinguished; since the male was
not collected. Forewing is clear,
yellowish to lightly infumate beyond
basal cell, postmarginal vein of forewing
is not or hardly longer than stigmal vein.
Head with frontal crest coarsely alveolate
50
Vol. 8, No. 1, 2013
(Fig. 7), only two vertical rows of
alveolae between inner orbit and scrobes,
the alveolae with rasp-like edges. Female
gaster relatively longer, its last tergite
laterally compressed and more than twice
as long as broad (Fig. 7).
in Cross and Moser (18). A full mature
female measures 400 µm long and 300
µm in width, with white to yellow color.
The male is long and larger than the
female.
The abdomen of the female is
expanded (Fig. 8). Only few males appear
first grouped around the genital opening
of the female (Fig. 9). With the release of
the female genital opening copulation
takes place immediately. Then females
seek other hosts and the cycle resumes.
Mite parasitoid family of Scolytus
amygdali.
Peymotidae. Pyemotes sp. One mite
from the genus Pyemotes was detected as
natural enemies for the almond bark
beetle S. amygdali. This mite was
identified to the genus level using the key
Fig. 8. Female of Pyemotes sp. obtained from the body of
Scolytus amygdali (ESM)
The presence of Pyemotes sp. was
mentioned in burrow systems during
rearing beetle on all larval stages as well
as in adults.
These mites are active in warm T°
above 25°C. For this reason, they showed
increased activity during the breeding
beetles. These mites attack all stages of
beetles, even sick ones or their natural
enemies.
Tunisian Journal of Plant Protection
The results of the Petri dish
bioassay show that Pyemotes sp. attacks
all developmental stages, and even the
natural enemies of S. amygdali from the
first day post-treatment.
post
After three days,
all the animal material in Petri dishes was
attacked at 100% under laboratory rearing
conditions (Fig. 10).
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Vol. 8, No. 1, 2013
Fig. 9. Male of Pyemotes sp. collected from the body of
Scolytus amygdali (SEM)
Fig. 10. Pyemotes sp., a: on Raphitellus maculatus, b: on Scolytus amygdali larvae, c: on S. amygdali adult,
d: Male, e: Female.
amydali,
C.
cornigera
and
C.
eccoptogastri (7, 10). A single
Cerocephala was collected from S.
amygdali (7) in Tafrout in 1981. C.
eccoptogastri was well met on
Phloeotribus scaraboides (8). Mendel
(29) has reared it from S. amygdali, S.
multistriatus,
and
S.
rugulosus
mediterraneus (19). The same author
mentioned
the
Pteromalid
C.
eccoptogastri as a cryptoparasitoid (the
parasitoid enters the bark beetle galleries
to find and parasitize host larvae of larvae
and pupae). R. maculates was mentioned
DISCUSSION
Information on parasitoids of S.
amygdali in Tunisia is lacking. On the
other side, those of Morocco were
reported by Benazoun (7) and Benazoun
and Schvester (10). In Tunisia, some
Pteromalidae parasitoids were reported in
the Universal Chalcidoidae Database
(32). Number of researchers has
mentioned those wasps; C. quadrum (26),
R. maculatus (1) and C. cornigera (1). C.
eccoptogastri was first recorded in
Tunisia (39). Two Ceracephala species
have been previously reared from S.
Tunisian Journal of Plant Protection
52
Vol. 8, No. 1, 2013
on P. scaraboides (1, 8, 16, 21, 39) and L.
was also mentioned by the same author. It
varius (28) on olive. It was also
was recorded in the Canary Islands by
mentioned on Hylesinus fraxini (31), on
Askew and Aldrey (3). Other Eupelmidae
S. nitidus (14) and on elm bark beetles in
species have been reared from S. amydali
Serbia (36). On P. scaraboides, C.
such as Eupelmus urozonus (33).
quadrum was the most abundant species
Benazoun (7, 10) studying S. amygdali in
(8, 15). This is an ectoparasite protandric,
Morocco did not mention any parasitism
polyphagous, and largely subservient to
by species of Eupelmidae family. Similar
the third and fourth larval stage of several
results were obtained by Mendel (29).
bark beetles (26). The wasp was reared
Only two species have been
from S. amygdali (7, 10, 29), S.
reported as predators of scolytides: P.
multistriatus (23), R. mediterraneus and
ventricosus and P. scolyti. The mite P.
R. rugulosus (30, 35), H. oleiperda (1,
ventricosus is polyphagous according to
25), L. varius (28), P. scaraboides (1, 8,
Schvester tests; they can attack S.
16, 22, 39), H. fraxini (31), S. nitidus
rugulosus and Scolytus sp. beetles (7, 8,
(14), and the elm bark beetles in Serbia
10). Beaver (6) has recorded P.
(36). The general biology of parasitoids is
ventricosus on S. miltistriatus. In the
similar for most species; they usually
United States, P. ventricosus has been
locate their host by walking on the bark
recorded from Lyctus planicollis in
Mississippi, S. multistriatus in Louisiana,
paralyzing the larvae or the pupae by
and a wasp nest in Virginia (18).
injecting venom and laying a single egg
on the paralyzed host. Eggs and larvae
ACKNOWLEDGMENTS
develop quickly. Overwintering usually
The authors would like to thank Dr. Gary
occurs as pre-pupae or pupa stages, in the
Gibson (Agriculture and Agri-Food Canada,
host gallery (26).
Canadian National Collection of Insects) and Dr
The holotype female from Madrid was
Mircea-Dan Mitroiu (The 'Alexandru Ioan Cuza'
University of Iasi, Faculty of Biology, Laboratory of
labeled by Bolivar (11) as P. merceti on
Animal Biology, Iasi, Romania) for their valuable
Eccoptogaster multistriatus and Ulmus
help in the identification of the species and the unit
campestris. This host is now known as S.
of ESEM Borj Cedria for the production of the SEM
multistriatus (3, 11). A male from Madrid
pictures.
__________________________________________________________________________
RESUME
Zeiri A., Braham M. et Braham M. 2013. Les parasitoïdes de scolyte de l’amandier
Scolytus amygdali en Tunisie. Tunisian Journal of Plant Protection 8: 45-56.
Depuis 2009, la biologie et le cycle de vie du scolyte de l’amandier Scolytus amygdali ont été étudiés
en Tunisie. Des branches infestées d'amandier, de prunier, d’abricotier et de pêcher ont été ramenées au
laboratoire et placées dans des boîtes en plastique. Les adultes de S. amygdali et leurs ennemis naturels
ont été collectés. Parmi les parasitoïdes trouvés sur S. amygdali, nous avons identifié trois espèces
appartenant à la famille des Pteromalidae, qui sont Cerocephala eccoptogastri avec un coefficient de
dominance moyen de 53,26%, Cheiropachus quadrum avec 14,88% et Rhaphitelus maculatus avec
10,44%. Le parasitoïde Eusandalum merceti de la famille des Eupelmidae a été collecté en Octobre
2009 et c’est la première signalisation de ce parasitoïde en Tunisie. Il se présentait comme un ectoparasitoïde des larves matures et des nymphes de S. amygdali. Les larves de S. amygdali était aussi
également attaquées par une espèce d’acarien: Pyemotes sp. Plusieurs bioessais ont été effectués dans
des boîtes de Pétri afin d'évaluer les dommages causés par cet acarien sur le scolyte étudié. Les
résultats ont montré que cet acarien attaque tous les stades de S. amygdali et les hyménoptères
parasitoïdes associés.
Tunisian Journal of Plant Protection
53
Vol. 8, No. 1, 2013
Mots clés: Cerocephala eccoptogastri, Cheiropachus quadrum, Eusandalum merceti, parasitoïde,
Pyemotes sp., Rhaphitelus maculates, Scolytus amygdali, Tunisie
__________________________________________________________________________
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‫ أ ه ط ت‬.2013. ‫اھ‬
Tunisian Journal of Plant Protection 8: 45-56.
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‫ أ‬،‫ا ا ي‬
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‫ت أ! ن‬$% ‫ أ‬. ‫ﻧ‬
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‫ درا دورة ة‬،2009 ‫م‬
،
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‫ و‬. - (@ ‫اءھ ا‬. ‫ وأ‬S. amygdali ‫ = ت‬9-0>‫ و‬،‫ات‬$1? ‫ا‬
‫ل‬.-0 Cerocephala eccoptogastri ‫ ھ‬Pteromalidea
‫ أﻧ اع‬F6F G 31
،amygdali
>‫در‬
‫ل‬.-0 Rhaphitelus maculatus ‫ و‬%14.88 ‫ل‬.-0 Cheiropachus quadrum ‫ و‬%53.26 ‫دة‬
Eupelmidae
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‫ ھ ا‬K C@ ‫ ا‬L(1 ‫ول‬M‫ ا‬K *N5 ‫ ن ھ ا ا‬I‫و‬
ً %,‫ أ‬S. amygdali ‫' ت‬$, 0> Q 5 0I . *: ‫ ا‬amygdali
.Pyemotes sp. ‫ رو ت ھ‬IM‫ط ﻧ ع ا‬
.S. amygdali ; ‫ روس‬IM‫ھ ا ا‬
0> ‫ار ا‬$:M‫ ا‬, 5 ‫ي‬$5 ‫أط( ق‬
>
‫( رات‬5S‫ة ا‬. 9,$>‫ أ‬.'‫و‬
‫ ت‬W 1!
‫ ت‬C@ ‫( ه ا‬+‫ أ‬Y I‫ و‬S. amygdale ,‫@ ر‬5 ‫ط ار ا‬M‫ ا‬J 0> > Q, ‫ روس‬IM‫ أن ھ ا ا‬VW 5 ‫ت ا‬$Q‫وأظ‬
. Q ‫ا‬$ 5 ‫> ? ا‬M‫ا‬
،Cerocephala eccoptogastri ،Cheiropachus quadrum ، ‫ ﻧ‬،‫ ت‬C‫( ه ط‬+‫ أ‬: 5C ‫ ت‬0 I
Scolytus amygdali ،Pyemotes sp. ،Rhaphitelus maculates ،Eusandalum merceti
__________________________________________________________________________
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