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First record of Coccinella septempunctata algerica (Coleoptera, Coccinellidae) as host of Dinocampus coccinellae (Hymenoptera, Braconidae, Euphorinae) in Algeria

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Primer registre de Coccinella septempunctata algerica (Coleoptera, Coccinellidae) com a hoste de Dinocampus coccinellae (Hymenoptera, Braconidae, Euphorinae) a Algèria Aquest estudi es va portar a terme en camps situats a la regió de Boumerdes, prop d’Alger (Algèria), entre els mesos d’abril i setembre de 2019. Es van registrar dues espècies de Coccinellini, Coccinella septempunctata algerica (Kovàr, 1977) i Hippodamia variegata (Goeze, 1777), com a hostes del parasitoide Dinocampus coccinellae (Schrank, 1802). El percentatge de parasitisme observat durant el mostreig va ser baix. Els nostres resultats suggereixen que D. coccinellae no està ben adaptat a Harmonia axyridis (Pallas, 1773). Aquest treball mostra que el parasitoide té més predilecció per C. septempunctata algerica que per H. variegata (16,7% i 2,2% de parasitisme). Atès el baix percentatge de parasitisme per D. coccinellae, no sembla que aquest parasitoide pugui reduir l’eficàcia del biocontrol mitjançant marietes. Aquest és el primer registre publicat de Dinocampus coccinellae com a parasitoide de C. septempunctata algerica a Algèria.
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Arxius de Miscel·lània Zoològica, 19 (2021): 65–72 Aitaider et al.
ISSN: 16980476
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First record of
Coccinella septempunctata algerica
(Coleoptera, Coccinellidae)
as a host of Dinocampus coccinellae
(Hymenoptera, Braconidae, Euphorinae)
in Algeria
L. Aitaider, A. Meriem, S. Doumandji
Aitaider, L., Meriem, A., Doumandji, S., 2021. First record of Coccinella septempunctata
algerica (Coleoptera, Coccinellidae) as a host of Dinocampus coccinellae (Hymenoptera,
Braconidae, Euphorinae) in Algeria. Arxius de Miscel·lània Zoològica, 19: 65–72, Doi: https://
doi.org/10.32800/amz.2021.19.0065
Abstract
First record of Coccinella septempunctata algerica (Coleoptera, Coccinellidae) as host of
Dinocampus coccinellae (Hymenoptera, Braconidae, Euphorinae) in Algeria. This study
was conducted in elds in the Boumerdes region near Algiers, Algeria between April and
September 2019. Two species of Coccinellini, Coccinella septempunctata algerica (Kovàr,
1977) and Hippodamia variegata (Goeze, 1777) were recorded as hosts of the parasitoid
Dinocampus coccinellae (Schrank, 1802). The percentage of parasitism observed during the
sampling was low. Our results suggest that D. coccinellae is not well adapted to Harmonia
axyridis (Pallas, 1773). This work shows that the parasitoid has a greater preference for C.
septempunctata algerica than for H. variegata (16.7 % versus 2.2 % of parasitism). Given
the low percentage of parasitism due to D. coccinellae, it does not seem that this parasitoid
is able to reduce the effectiveness of biocontrol by ladybeetles. This is the rst published
record of Dinocampus coccinellae as a parasitoid of C. septempunctata algerica in Algeria.
Key words: Dinocampus coccinellae, Coccinella septempunctata algerica, Hippodamia
variegata, Parasitoid, Parasitism rate
Resumen
Primer registro de Coccinella septempunctata algerica (Coleoptera, Coccinellidae) como
huésped de Dinocampus coccinellae (Hymenoptera, Braconidae, Euphorinae) en Argelia.
Este estudio se desarrolló en campos situados en la región de Boumerdes, próxima a Ar-
gel (Argelia), entre los meses de abril y septiembre de 2019. Se registraron dos especies
de Coccinellini, Coccinella septempunctata algerica (Kovàr, 1977) e Hippodamia variegata
(Goeze, 1777), como huéspedes del parasitoide Dinocampus coccinellae (Schrank, 1802).
El porcentaje de parasitismo observado durante el muestreo fue bajo. Nuestros resultados
sugieren que D. coccinellae no está bien adaptado a Harmonia axyridis (Pallas, 1773). Este
trabajo muestra que el parasitoide tiene mayor predilección por C. septempunctata algerica
que por H. variegata (16,7 % frente a 2,2 % de parasitismo). Dado el bajo porcentaje de
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Arxius de Miscel·lània Zoològica, 19 (2021): 65–72 Aitaider et al.
parasitismo por D. coccinellae, no parece que este parasitoide pueda reducir la ecacia
del biocontrol mediante mariquitas. Este es el primer registro publicado de Dinocampus
coccinellae como parasitoide de C. septempunctata algerica en Argelia.
Palabras clave: Dinocampus coccinellae, Coccinella septempunctata algerica, Hippodamia
variegata, parasitoide, tasa de parasitismo
Resum
Primer registre de Coccinella septempunctata algerica (Coleoptera, Coccinellidae) com a
hoste de Dinocampus coccinellae (Hymenoptera, Braconidae, Euphorinae) a Algèria. Aquest
estudi es va portar a terme en camps situats a la regió de Boumerdes, prop d'Alger (Algèria),
entre els mesos d’abril i setembre de 2019. Es van registrar dues espècies de Coccinellini,
Coccinella septempunctata algerica (Kovàr, 1977) i Hippodamia variegata (Goeze, 1777),
com a hostes del parasitoide Dinocampus coccinellae (Schrank, 1802). El percentatge de
parasitisme observat durant el mostreig va ser baix. Els nostres resultats suggereixen que
D. coccinellae no està ben adaptat a Harmonia axyridis (Pallas, 1773). Aquest treball mostra
que el parasitoide té més predilecció per C. septempunctata algerica que per H. variegata
(16,7 % i 2,2 % de parasitisme). Atès el baix percentatge de parasitisme per D. coccinellae,
no sembla que aquest parasitoide pugui reduir l'ecàcia del biocontrol mitjançant marietes.
Aquest és el primer registre publicat de Dinocampus coccinellae com a parasitoide de C.
septempunctata algerica a Algèria.
Paraules clau: Dinocampus coccinellae, Coccinella septempunctata algerica, Hippodamia
variegata, Parasitoide, Taxa de parasitisme
Received: 27/11/2020; Conditional acceptance:18/01/2021; Final acceptance: 01/02/2021
Lina Aitaider, Ahlem Meriem, Salahedine Doumandji, Department of Agricultural and Forest
Zoology, High National School of Agronomy, Avenue Hassen Badi, El–Harrach, 16200 Algiers,
Algeria.
Corresponding author: L. Aitaider. E–mail: linaait282@gmail.com or l.aitaider@edu.ensa.dz
Introduction
Ladybeetles are of great economic importance as they feed on several potential pests, thus
controlling populations in many agricultural systems. They intervene both in larval and adult
stages (Dixon, 2000; Isikber and Copland, 2002; Lundgren, 2009; Obrycki et al., 2009).
The bioecology of ladybeetles has been well documented in Algeria, especially in the work
of Saharaoui (1987, 1994) and Sharaoui et al. (2001). These species may be subject to
the action of one or more species of natural enemies, such as Dinocampus coccinellae.
The biology of this parasitoid has been well documented by Obrycki (1989), Majerus et al.
(2000), Firlej et al. (2005), Berkvens et al. (2010), Maure et al. (2011), Silva et al. (2012),
Koyama et al. (2013), Minaar et al. (2014), Dindo et al. (2016), Ceryngier et al. (2018),
and Maqbool et al. (2018). Studies concerning the natural enemies of Coccinellidae and
Dinocampus coccinellae in Algeria, however, are rare, and studies to date only report their
presence. Dinocampus coccinellae is a parasitoid of another ladybeetle species, Hippodamia
variegata (Saharaoui, 1994). This braconidae is a solitary endoparasitoid that exclusively
parasitizes Coccinellid species (Firlej et al., 2005; Berkvens et al., 2010; Minaar et al., 2014).
It reproduces by thelytokous parthenogenesis (Okuda and Ceryngier, 2000; Riddick et al.,
2009). Only one larva will develop inside the host even if the host has been parasitized
several times (Ceryngier et al., 2012). Once it emerges from the host, the larva spins a
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Arxius de Miscel·lània Zoològica, 19 (2021): 65–72 Aitaider et al.
cocoon between the legs of the host (Davis et al., 2006; Maure et al., 2011). The ladybee-
tle remains partially paralyzed throughout the parasitoid pupal stage (Maure et al., 2011).
The host usually dies afterwards (Dheilly et al., 2015). The rate of ladybeetle parasitism by
D. coccinellae can uctuate signicantly depending on location, season, and host species
(Maure et al., 2016). The objective of this work was to study host–parasitoid relationships
between D. coccinellae and the two–coccinellid species, C. septempunctata algerica and
H. variegata, parasitism rates in the eld and in the laboratory.
Material and methods
Field survey
Samples of C. septempunctata algerica, Psyllobora vingintiduopunctata, Harmonia axyridis
and Hippodamia variegata were collected over two–hour periods every 15 days from April
to September 2019. Sampling was conducted on cultivated plants (Zea mays, Phaseolus
vulgaris, Solanum tuberosum) and weeds around elds (Leucanthemum vulgare, Daucus carota,
Malva sylvestris, Galactites tomentosa, Galium aparine, Lysimachia foemina). The beetles
were collected by hand at two stations: Ouled Hadadj and Ouled Moussa in the Bou-
rmedes region (36º 45' 37.23' N, 3º 28' 20.52'' E) (g. 1). The collected ladybeetles
were placed in plastic boxes (26 cm x 18 cm × 2 cm), kept at 22 ºC with a photoperiod of
14 h of light and 10 h of darkness, and fed with aphids taken from Daucus carota, in order
to check for the possible emergence of parasitoids. The emergence of parasitoids was
recorded daily for 20 days.
Fig. 1. Location of the collection site of Coccinellidae species, Boumerdes (Algeria).
Fig. 1. Localización del punto de recolección de especies de Coccinellidae, Boumerdes
(Argelia).
37º 0' 0'' N
36º 45' 0'' N
36º 30' 0'' N
47' 0'' E 2º 58' 0'' E 3º 9' 0'' E 3º 20' 0'' E 3º 31' 0'' E 3º 42' 0'' E 3º 53' 0'' E 4º 4' 0'' E
37º 0' 0'' N
36º 45' 0'' N
36º 30' 0'' N
47' 0'' E 2º 58' 0'' E 3º 9' 0'' E 3º 20' 0'' E 3º 31' 0'' E 3º 42' 0'' E 3º 53' 0'' E 4º 4' 0'' E
Algeria
Boumerdes
Ouled Hadadj
Ouled Moussa
N
0 3 6 12 18 24 km
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Arxius de Miscel·lània Zoològica, 19 (2021): 65–72 Aitaider et al.
Laboratory experiment
Each parasitoid that emerged from eld–collected ladybeetles was placed in a Petri dish
of 10 cm diameter and 1 cm in height. The non–parasitized adult ladybeetles collected in
the eld were placed in plastic boxes. Every 10 days, for three months, 10 individuals of
Coccinella septempunctata algerica and 10 of H. variegata were placed in separate petri
dishes. In each petri dish, we placed three individuals of D. coccinellae. Three individuals of
Psyllobora vingintiduopunctata and Harmonia axyridis were placed in separate petri dishes,
each with one parasitoid. The parasites used in this experiment were those collected directly
in the eld or taken from the ladybeetles collected. Behavior of some ladybeetles in the
following days indicated they were parasitized. These parasitized ladybeetles were installed
alone in a Petri dish and left for three weeks for observation and to verify the emergence
of the parasitoid. The biological aspects of D. coccinellae were monitored in the laboratory
at 24 ºC. The results were evaluated in terms of number and percentages of successfully
parasitized ladybeetles (parasitism rate) (i.e. ladybeetles that produced a cocoon and adult
parasitoid/number of ladybeetles exposed). The time (in days) was calculated: from the
exposure of the hosts to the detection of the parasitoid cocoons; and from the detection of
the cocoon to the emergence of the adult (duration of the pupal stage).
Results
Field survey
A total of 476 ladybeetles were collected. C. septempunctata algerica and H. variegata were
the most abundant, with 416 individuals found on Daucus carota. Thirty–three D. coccinellae
emerged from the adults (table 1). Adult ladybeetles were parasitized from April, reaching
a maximum of parasitism in June. Rates of parasitoid emergence were 20.3 % (n = 64)
Table 1. Monthly eld data of parasitism of Coccinella septempunctata algerica and
Hippodamia variegata by Dinocampus coccinellae: Nh, number of hosts; ND, nuber
of D. coccinellae; Pr, parasitism rate.
Table 1. Datos mensuales de campo del parasitismo de Coccinella septempunctata
algerica y Hippodamia variegata por Dinocampus coccinellae: Nh, número de
huéspedes; ND, número de D. coccinellae; Pr, tasa de parasitismo.
C. septempunctata algerica H. variegata
Nh ND Pr Nh ND Pr
April 42 2 4.76 % 20 0 0 %
May 55 8 14.55 % 33 1 3.03 %
June 64 13 20.31 % 30 2 6.67 %
July 54 3 5.56 % 23 0 0 %
August 32 3 9.38 % 14 0 0 %
September 30 1 3.33 % 19 0 0 %
Totals 277 30 10.83 % 139 3 2.16 %
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Arxius de Miscel·lània Zoològica, 19 (2021): 65–72 Aitaider et al.
for C. septempunctata algerica and 6.7 % for H. variegata. No parasitism was recorded in
P. vingintiduopunctata or H. axyridis. All the eld–collected ladybeetles from which D. coccinellae
emerged in the laboratory were females. This was veried by examining the genitalia of all
parasitized individuals with an optical microscope.
Laboratory experiment
Dinocampus coccinellae emerged from 15 of 90 (16.7 %) laboratory parasitized adults of
C. septempunctata algerica and from two of 90 (2.2 %) adults of H. variegata. Each parasi-
toid larva leaving its host pupated inside a cocoon spun between the host's legs and then
emerged as an adult wasp (g. 2). We observed that all parasitized ladybeetles died after
the emergence of the parasitoid except for two individuals that remained alive but were not
active. No parasitoid emerged from Psyllobora vingintiduopunctata or Harmonia axyridis.
Figure 3 summarizes the life–cycle of the parasitoid and the duration of each stage of
development (from host exposure to the emergence of adult wasp). We observed that D.
coccinellae started to attack C. septempunctata algerica within 24 h and after two days started
to attack H. variegata when we put them together. The incubation period of D. coccinellae
eggs and larval development was not quantied. After the larva emerged a cocoon was formed
within 24 h. The adult emerged from after eight days for C. septempunctata algerica
and after nine days for H. variegata. The developmental cycles of the parasitoid in the two
hosts C. septempunctata algerica and H. variegata are comparable.
Fig. 2. A, adult of C. septempunctata algerica with cocoon of D. coccinellae on
Solanum tuberosum; B, larva of D. coccinellae; C, cocoon of D. coccinellae after the
emergence of adult wasp.
Fig. 2. A, adulto de C. septempunctata algerica con capullo de D. coccinellae en
Solanum tuberosum; B, Larva de D. coccinellae; C, capullo de D. coccinellae después
de la emergencia del coleóptero adulto.
A B C
0.8 mm 5 mm 15 mm
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Fig. 3. Developmental cycle of D. coccinellae parasitizing C. septempunctata algerica
and H. variegata.
Fig. 3. Ciclo de desarrollo de D. coccinellae en la parasitación de C. septempunctata
algerica y H. variegata.
Discussion
During the survey, the ladybeetle most frequently found was C. septempunctata algerica.
This study reports the parasitism of Dinocompus coccinellae on this species for the rst time
in Algeria. The parasitism rate was higher on C. septempunctata algerica (between 3.33 and
20.31 %) than on H. variegata (between 0 to 6.7 %). Obrycki (1989), Orr et al. (1992) and
Triltsch (1996) also found a higher parasitism rate (12.5 to 47 %) on C. septempunctata.
The rates of parasitism species of ladybeetles vary in the literature. Berkvens et al. (2010)
reported a rate of between 0 and 14.7 % for Harmonia axyridis, and Rebolledo et al. (2009)
and Tavoosi Ajvad et al. (2012) both found rates of approximately 30 % on H. variegata. Our
results differ somewhat from those of the cited authors. We did not observe parasitism by
D. coccinellae on H. axyridis collected in the elds near Boumerdes. It is of note H. axyridis
is an introduced species in Algeria; it was rst reported in Algiers by Lakhal et al. (2018).
Majerus et al. (2000) and Davis et al. (2006) noted that females of C. septempunctata are
more often parasitized than males. These authors suggested that due to their size, females
would provide more trophic substance for the development of D. coccinellae larvae. The
results of our study support this hypothesis.
In conclusion, our ndings suggest that C. septempunctata algerica in Algeria is a
sub–optimal host for D. coccinellae as for other ladybeetle species because the number of
ladybugs that were parasitized was low compared to the number of ladybugs that were not
parasitized. The parasitoid fauna of ladybeetle parasitoids in neighboring regions of Algeria
is known to contain species that have not yet been studied for this country. The present
work is a preliminary study that should be completed by surveys in other biotopes in order
to understand the procession of natural enemies of Coccinella septempunctata algerica
and other Coccinellidae species.
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Acknowledgements
My thanks to Mr. Ceryngier who identied the species of parasitoid, and my colleague
Lakhal Mohamed Amin for his invaluable help during the experiment.
References
Berkvens, N., Moens, J., Berkvens, D., Samih, M. A., Tirry, L., De Clercq, P., 2010. Dino-
campus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe.
Biological Control, 53(1): 92–99, Doi: 10.1016/j.biocontrol.2009.11.001
Ceryngier, P., Nedvěd, O., Grez, A. A, Riddick, E. W., Roy, H. E., San Martin, G., Steen-
berg, T., Vesely, P., Zaviezo, T., Zuniga–Reinoso, A., Haelewaters, D., 2018. Predators
and parasitoids of the harlequin ladybird, Harmonia axyridis, 266 in its native range and
invaded areas. Biological Invasions, 20: 1009–1030, Doi: 10.1007/s10530-017-1608-9
Ceryngier, P., Roy, H. E., Poland, R. L., 2012. Natural Enemies of Ladybird Beetles. In:
Ecology and Behaviour of the Ladybird Beetles (Coccinellidae): 375–443 (I. Hodek, H. F.
van Emden, A. Honěk, Eds.). Blackwell Publishing Ltd., Doi: 10.1002/9781118223208.ch8
Davis, D. S., Stewart, S. L., Manica, A., Majerus, M. E. N., 2006. Adaptive preferential selection
of female coccinellid hosts by the parasitoid wasp Dinocampus coccinellae (Hymenoptera:
Braconidae). European Journal of Entomology, 103(1): 41–45, Doi: 10.14411/eje.2006.006
Dheilly, N. M., Maure, F., Ravallec, M., Galinier, R., Doyon, J., Duval, D., Leger, L., Volkoff,
A.–N., Misse, D., Nidelet, S., Demolombe, V., Brodeur, J., Gourbal, B., Thomas, F.,
Mitta, G., 2015. Who is the puppet master? Replication of a parasitic wasp–associated
virus correlates with host behaviour manipulation. Proceedings of the Royal Society B,
282(1803): 20142773, Doi: 10.1098/rspb.2014.2773
Dindo, M. L., Francati, S., Lanzoni, A., Di Vitantonio, C., Marchetti, E., Burgio, G., Maini,
S., 2016. Interactions between the multicolored Asian ladybeetle Harmonia axyridis and
the parasitoid Dinocampus coccinellae. Insects, 7(4): 67, Doi: 10.3390/insects7040067
Dixon, A. F. G., 2000. Insect Predator–Prey Dynamics Lady Birds Beetles and Biological
Control. Cambridge University Press, NY.
Firlej, A., Boivin, G., Lucas, E., Coderre, D., 2005. First report of Harmonia axyridis Pallas
being attacked by Dinocampus coccinellae Schrank in Canada. Biological Invasions, 7:
553–556, https://link.springer.com/article/10.1007/s10530-004-5848-0
Isikber, A. A., Copland, M. J. W., 2002. Effects of various aphid foods on Cycloneda san-
guinea. Entomologia Experimentalis e Applicata, 102(1): 93–97, Doi: 10.1046/j.1570-
7458.2002.00928.x
Koyama, S., Cathleen, E., Thomas, C. E., Takata, M., 2013. Relationship between the size
of the parasitoid wasp Dinocampus coccinellae (Hymenoptera: Braconidae) and host
ladybird species (Coleoptera: Coccinellidae). Trends in Entomology, 9: 39–43.
Lakhal, M. A., Ghezali, D., Nedvěd, O., Doumandji, S., 2018. Checklist of ladybirds of Algeria
with two new recorded species (Coleoptera, Coccinellidae). ZooKeys, 774: 41–52, Doi:
10.3897/zookeys.774.23895
Lundgren, J. G., 2009. Nutritional aspects of non–prey foods in the life histories of predaceous
Coccinellidae. Biological Control, 51: 294–305, Doi: 10.1016/j.biocontrol.2009.05.016
Majerus, M. E. N, Geoghegan, I. E., Majerus, T. M. O., 2000. Adaptive preferential selection
of young coccinelid hosts by the parasitoid wasp Dinocampus coccinellae (Hymenoptera:
Braconidae). European Journal of Entomology, 97(2): 161–164, Doi: 10.14411/eje.2000.030
Maqbool, A., Ahmed, I., Kieltyk, P., Ceryngier, P., 2018. Dinocampus coccinellae (Hyme-
noptera: Braconidae) utilizes both Coccinellini and Chilocorini (Coleoptera: Coccinellidae:
Coccinellinae) as hosts in Kashmir Himalayas. European Journal of Entomology, 115:
332–338, Doi: 10.14411/eje.2018.033
72
Arxius de Miscel·lània Zoològica, 19 (2021): 65–72 Aitaider et al.
Maure, F., Brodeur, J., Ponlet, N., Doyon, J., Firlej, A., Elguero, E., Thomas, F., 2011. The
cost of a bodyguard. Biology Letters, 7: 843–846, Doi: 10.1098/rsbl.2011.0415
Maure, F., Thomas, F., Doyon, J., Brodeur, J., 2016. Host nutritional status mediates degree
of parasitoid virulence. Oikos, 125: 1314–1323, Doi: 10.1111/oik.02944
Minnaar, I. A., Shinner, R., Van Noort, S., Clusella–Trullas, S., 2014. New records of the
parasitic wasp Dinocampus coccinellae (Hymenoptera: Braconidae) and its hosts in South
Africa. African Entomology, 22: 226–229, Doi: 10.4001/003.022.0124
Obrycki, J. J., 1989. Parasitization of native and exotic coccinellids by Dinocampus coc-
cinellae (Schrank) (Hymenoptera: Braconidae). Journal of the Kansas Entomological
Society, 62(2): 211–218. JSTOR: www.jstor.org/stable/25085076
Obrycki, J. J., Harwood, J. D., Kring, T. J., O'neil R . J., 2009. Aphidophagy by Coccinellidae:
application of biological control in agroecosystems. Biological Control, 51: 244–254, Doi:
10.1016/j.biocontrol.2009.05.009
Okuda, T., Ceryngier, P., 2000. Host discrimination in Dinocampus coccinellae (Hymenop-
tera: Braconidae), a solitary parasitoid of coccinellid beetles. Applied Entomology and
Zoology, 35: 535–539, Doi: 10.1303/aez.2000.535
Orr, C. J., Obrycki, J. J., Fanders, R. V., 1992. Host acceptance behavior of Dinocampus
coccinellae (Hymenoptera: Braconidae). Annals of the Entomological Society of America,
85(6): 722–730.
Rebolledo, R., Sheriff, J., Parra, L., Aguilera, A., 2009. Life, seasonal cycles, and population
uctuation of Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae), in this central
plain of Laaraucania region, Chile. Chilean Journal of Agricultural Research, 6(2): 292–298.
Riddick, E. W., Cottrell, T. E., Kidd, K. A., 2009. Natural enemies of the Coccinellidae:
parasites, pathogens, and parasitoids. Biological Control, 51: 306–312, Doi: 10.1016/j.
biocontrol.2009.05.008
Saharaoui, L., 1987. Inventaire des coccinelles entomophages (Coleoptera – Coccinellidae)
dans la plaine de la Mitidja et aperçu bioécologique des principales espèces rencontrées,
en vue d’une meilleure appréciation de leur rôle entomophage. PhD thesis, Nice University.
– 1994. Inventaire et étude de quelques aspects bioécologiques des coccinelles entomo-
phages (Coleoptera: Coccinellidae) dans l'Algérois. Journal of African Zoology, 108(6):
538–546.
Saharaoui, L., Gourreau, J. M., Iperti, G., 2001. Etude de quelques paramètres bioécolo-
giques des coccinelles aphidiphages d'Algérie (Coleoptera–Coccinellidae). Bulletin Société
Zoologique France, 126(4): 351–373.
Silva, R. B., Cruz, I., Figueiredo, M. L. C., Pereira, A. G., Penteado–Dias, A. M., 2012.
Occurrence and biology of Dinocampus coccinellae (Schrank, 1802) (Hymenoptera;
Braconidae: Euphorinae) parasitising different species of Coccinellidae (Coleoptera) in
Neotropical region. Brazilian Journal of Biology, 72(1): 215–219, Doi: 10.1590/S1519–
69842012000100027
Tavoosi Ajvad, F., Madadi, H., Kazazi, M., Sobhani, M., 2012. Seasonal changes of Hip-
podamia variegata populations and its parasitism by Dinocampus coccinellae in alfalfa
elds of Hamedan. Biological Control Pests and Plant Disease, 1: 11–18, Doi: 10.22059/
JBIOC.2012.32070
Triltsch, H., 1996. On the parasitization of the ladybird Coccinella septempunctata L. (Col,
Coccinellidae). Journal of Applied Entomology, 120: 375–378, Doi: 10.1111/j.1439-
0418.1996.tb01622.x
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