Arxius de Miscel·lània Zoològica. Volume 19 (2021) Pages: 65-72

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

Aitaider, L., Meriem, A., Doumandji, S.

DOI: https://doi.org/10.32800/amz.2021.19.0065

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Keywords

Dinocampus coccinellae, Coccinella septempunctata algerica, Hippodamia variegata, Parasitoid, Parasitism rate

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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

Reception date:

27/11/2020

Acceptation date:

01/02/2021

Publication date:

16/02/2021

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Abstract

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

This study was conducted in fields 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 first 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 Argel (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 parasitismo por D. coccinellae, no parece que este parasitoide pueda reducir la eficacia 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’eficàcia 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

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; Saharaoui 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 cocoon between the legs of the host (Davis et al. 2006; Maure et al. 2011). The ladybeetle 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 fluctuate significantly 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 field 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 fields (Leucanthemum vulgare, Daucus carota, Malva sylvestris, Galactites tomentosa, Galium aparine, Lysimachia foemina). The beetles were collected by hand at two stations (fig. 1) in the Boumerdes region (36º 45′ 37, 23″ N,  3º 28′ 20, 52″ E). The collected ladybeetles were placed in plastic boxes (26 cm × 18 cm × 12 cm), kept at 22 ºC with a photoperiod of 14 h of light and 10h 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).

Laboratory experiment

Each parasitoid that emerged from field-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 field 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 field 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) for C. septempunctata algerica and 6.7 % for H. variegata. No parasitism was recorded in P. vingintiduopunctata or H. axyridis. All the field-collected ladybeetles from which D. coccinellae emerged in the laboratory were females. This was verified by examining the genitalia of all parasitized individuals with an optical microscope.

Table 1. Monthly field data of parasitism of Coccinella septempunctata algerica and Hippodamia variegata by Dinocampus coccinellae. Table 1. Datos mensuales de campo del parasitismo de Coccinella septempunctata algerica y Hippodamia variegata por Dinocampus coccinellae.

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 parasitoid larva leaving its host pupated inside a cocoon spun between the host’s legs and then emerged as an adult wasp (fig. 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 summarizes 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 quantified. 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.

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 first 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  sound 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 fields near Boumerdes. It is of note H. axyridis is an introduced species in Algeria; it was first 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 findings 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.

Acknowledgements

My thanks to Mr. Ceryngier who identified 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. Dinocampus 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., Steenberg, 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(4): 1009-1031, 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 sanguinea. 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: 161-164, Doi: 10.14411/eje.2000.030
Maqbool, A., Ahmed, I., Kieltyk, P., Ceryngier, P., 2018. Dinocampus coccinellae (Hymenoptera: 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
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 coccinellae (Schrank) (Hymenoptera: Braconidae). Journal of the Kansas Entomological Society, 62: 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 (Hymenoptera: 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: 722-730.
Rebolledo, R., Sheriff, J., Parra, L., Aguilera, A., 2009. Life, seasonal cycles, and population fluctuation 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 entomophages (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 bioécologiques 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 Hippodamia variegata populations and its parasitism by Dinocampus coccinellae in alfalfa fields 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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