First Report First Report on Natural Enemies of pulverulentus on Faba Bean Crops in Tunisia

Sonia Boukhris-Bouhachem, Manel Hmem-Bourissa, and Rebha Souissi, Laboratoire de Protection des Végétaux, INRAT, Université de Carthage, Rue HédiKarray, 2049 Ariana, Tunis, Tunisia ______ABSTRACT Boukhris-Bouhachem, S., Hmem-Bourissa, M., and Souissi R. 2016. First report on natural enemies of on faba bean crops in Tunisia. Tunisian Journal of Plant Protection 11: 245-250.

The Lixus pulverulentus is known to attack faba bean and to induce many damages on plants. The bioecology studies of L. pulverulentus was conducted at Béja (North-West of Tunisia) and Kairouan (Center of Tunisia). We report here the first identification of a natural enemies of L. pulverulentus (syn. L. algirus), a parasitoid wasp Pteromalus lixiand a predatory fly Zeuxia aberrans at both Béja and Kairouan. Parasitization incited by wasps was of about 0.8-2.6% and that displayed by larvae of flies was around 1.3-4.7%, respectively, which are considered low parasitism rates. Rearing attempts of thiswasp may be useful forbiological control of based on indigenous natural enemies.

Keywords: Diptera, faba bean, Hymenoptera, Lixus pulverulentus, parasitization ______

Lixus pulverulentus (syn. L. algirus) using synthetic insecticides such as DDT (Coleoptera, ) is reported to which has been banned. Targeting of attack faba bean and several Circium, juvenile instars, occurring inside plant Carduus and plants (3, 5, 12). tissues, is more difficult due to their Few researches were undertaken on its cryptic nature (3). According to Weigand biology and its impact on faba bean crops and Bishara (20), seed treatment using (13, 14, 20). The adult consumes leaves, carbofuran did not reduce L.pulverulentus young shoots and even flowers (3). infestation. Insecticide-based treatment Larvae live inside faba bean stem, and in should aim adults before occurrence of late season adults perform a hole causing oviposition. Once larvae inside stems, severe crop damage. During the 70s, chemical control becomes inefficient control L. pulverulentus adults, (20). characterized by a long-life span on In Tunisia, L. pulverulentus has vegetative organs, was relatively easy, become one of the main faba bean pests. In fact, previous surveys undertaken in several Tunisian faba bean-growing Corresponding author: Sonia Bouhachem Email: [email protected] regions showed important infestation rates reaching 41% in Cap Bon, 52% in

Accepted for publication 1 July 2016 Béja, 28% in Bizerte, and 11% in Kef Tunisian Journal of Plant Protection 245 Vol. 11, No. 2, 2016

(11). Few data are available about natural Canada balsam. enemies of L. pulverulentus in Tunisia. Parasitoids and predators were Auxiliary fauna such as parasitic identified using taxonomic characters; Hymenoptera developing on various these include the antennal club and stages of L. pulverulentus seems to be an venation of the forewing in males and interesting alternative to control this females, as well as the male genitalia, insect pest (3). In this context, we using specific keys (6, 16). Specimen performed a faunistic survey of natural identification was confirmed by Prof. enemies associated with the faba bean Michelle Martinez (INRA-Montpellier). , L. pulverulentus, for their Parasitizing percentage was eventual use in a biological control determined by dividing the number of program. parasitized L. pulverulentus larvae by the The study site is located in Béja total number of individuals counted. (North-Western Tunisia), in the research A total of 942 L. pulverulentus station of the Institut National de la larvae were observed on 1800 stems Recherche Agronomique de Tunisie collected in 2008 and 2012 of which two (36°44’05’’N, 9°13’35’’E, 150 m natural enemies of L. pulverulentus were elevation). According to the Institut identified. The first one is Pteromalus lixi National de Météorologie de Tunisie, the (Hymenoptera, Pteromalidae) observed at average temperature of this location is the first time on 18 March in Béja station around 19ºC and a total precipitation is of while the second is Zeuxia aberrans about 600 mm per year, falling from (Diptera, Tachinidae) observed on 25 September to June. This site was chosen March 2008 in the same samples coming because of its history of abundant L. from Béja. From 894 faba bean stem pulverulentus populations. The survey collected at Kairouan, 192 L. was carried out from February to June pulverulentus larvae were counted, 4 2008 and 2012 by collecting 200 were parasitized by P. lixi and 9 by Z. randomly chosen faba bean stems from a aberrans. 2 ha field of the variety “Badii”. During The parasitic wasp is metallic spring 2012, 300 samples were collected green with 1 to 2 mm long, characterized three times (between March and April) by a petiole separating the thorax and from Kairouan (a continental zone with abdomen. Its wings are transparent with arid cold winter of the center of Tunisia, reduced venation and with a coupling with coordinates 35°39’50”N 9°59’10”E). type hamule. Forewings are with Each infested stem was examined postmarginal and stigmal veins well- in the laboratory, and all living L. developed. The antennae with 13 articles pulverulentus larvae were counted. (2:2:6:3) are bent (superfamily Parasitized larvae showing brown and Chalcidoidea), tarsi with 5 articles and matte appearance and pupae of potential the ovipositor is visible characteristic for auxiliary flies were placed individually in the Pteromalidae family) (Fig.1b). It is an plastic boxes with perforated top for ectoparasitoid insect with yellowish larva aeration and stored at room temperature (Fig.1a) feeding on L. pulverulentus until emergence of parasitoids and flies. larvae. Emerging adults were slide mounted in

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Fig. 1. Pteromalus lixi: parasitoid of Lixus pulverulentus, a: Larva; b: Adult

The second natural enemy, an arista (suborder Brachycera) (Fig. 2c). collected on L. pulverulentus larvae, is a Fly larvae are apoda (Fig. 2a) and the Tachinidae fly identified as Z. aberrans. pupa is free, brown-reddish with an The adult is a small fly from 10 to 15 mm average of 7mm long and 2 mm wide. At long, brown provided with an abundant their emergence, the adult performs a chetotaxy (Fig. 2c). The mouthparts are circular whole to get out from the pupa transformed into trunk, the head has two (Fig. 2b). red eyes, the antennae are provided with

Fig. 2. Zeuxia aberrans, a: Larva feeding on Lixus pulverulentus; b: pupa; c: adult.

The prevalence of the Dipteran prevalence of the two enemies within L. predator on the larval stages of L. pulverulentus populations was extremely pulverulentus was more important than low (Table 1). Hymenopteran parasitoid with a This is the first record for P. lixi parasitism rate estimated to 1.3% and and Z. aberrans on the faba bean weevil 0.8%, respectively (Table 1). The L. pulverulentus in Tunisia.

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Table 1. Prevalence of identified natural enemies of Lixus pulverulentus larvae on faba bean crops in spring 2008 and 2012 in Tunisia Béja 2008 Kairouan 2012 Number of Number of Number of Number of Prospection parasitized predatory Prospection parasitized predaceous dates larvae midge Z. dates larvae with midge Z. with P. lixi aberrans P. lixi aberrans 10-03-2008 0 0 18-03-2008 3 0 25-03-2008 1 6 23-03-2012 2 5 02-04-2008 2 2 08-04-2008 1 1 10-04-2012 1 2 17-04-2008 0 1 30-04-2008 1 2 29-03-2012 1 2 16-05-2008 0 0 24-05-2008 0 0 Parasitism (%) 0.8 1.3 2.1 4.7

Pteromalus lixi, synonym of Europe on Lixus sp. infesting Carduus, Habroytus lixi, was reported as primary Centaurea, and Carlina (2). A low level parasitic host of L. algirus in Spain (7, of parasitism of L. pulverulentuslarvae 13). It was also previously cited in Italy was observed. The possible causes for (17), Sicily (15), and Morocco (10). The such low parasitism potential could be the genus Pteromalus, is worldwide cryptic life of L. pulverulentus larvae. distributed with oophagous species Nevertheless, eggs of L. algirus were known to attack eggs, Dictyoptera reported to be parasitized by Anaphes and Lepidoptera. This genus is divided leptoceras (Hymenoptera, Mymaridae) into two sub-genera namely Pteromalus (15), which was responsible for 15-20% and Habrocytus, and the only species in parasitism (13). In this case, it seems Europe which displayed oophagous more related to the efficiency of the ectoparasitic behavior is P. lixi which was parasitoid host research than to L. reported on Lixus anguinus (17). Another pulverulentus larvae accessibility. parasitoid, Anaphes leptoceras is also Besides for hymenopteran species, reported as a parasitoid of L. algirus (13, three diptera were reported as predators 15, 18). Other parasitoids as Norbanus of L. anguinus, Drosophila buschkii, scabriculus are known as endoparatoids Siphonella parallela, and Fannia of L. pulverulentus larvae, in a provincia canicularis. of Madrid (7) and Balearic Islands (2). In In this work, we identified Z. addition, Bracon forticeps was reported aberrans as a new predator of L. as parasite of L. anguinus larvae (17), B. pulverulentus larvae. However, it is worth chrysostigma on L. canescens and mentioning that Z. aberrans was reported Exerites roborator on L. subtilis (19). in the Spanish dipteran fauna (4) as well Calosota obscura was even recorded on as another Tachinidae species namely Lixus sp. (1). Furthermore, Entedon Zeuxia sicardi (Diptera, Tachinidae) insignis and E. thomsonianus are also which was recorded as an endoparasitoid reported as parasitoids of L. cardui on of larval instars in several Iberdorcadion some Carduus plants (8) and in central Tunisian Journal of Plant Protection 248 Vol. 11, No. 2, 2016

(Coleoptera, Cerambycidae) living inside weevil. Nevertheless, studies of P. lixi grass roots (9). and Z. aberrans biology are required. A The survey of endemic natural thorough search on their biology, mass enemies of L. pulverulentus is the first rearing laboratories and their potential use step to establish control strategies of L. in biological control is interesting to pulverulentus. The use of endemic develop in order to find an alternative to biological control agents is a key tool for fight the weevil due to the lack of a successful control of this faba bean effective insecticides against larvae. ______RESUME Boukhris-Bouhachem S., Hmem-Bourissa M. et Souissi R. 2016. Premier signalement d'ennemis naturels de Lixus pulverulentus dans les cultures de fève en Tunisie. Tunisian Journal of Plant Protection 11: 245-250.

Le coléoptère Lixus pulverulentus est un ravageur connu de la fève capable de provoquer des dégâts importants sur les plantes. L'étude de la bioécologie de cet insecte a été suivie dans deux régions de la Tunisie Béja (Nord-Ouest) et Kairouan (Centre). Nous signalons ici la première identification des ennemis naturels de L. pulverulentus, un hyménoptère parasitoïde Pteromaluslixi et une mouche prédatrice Zeuxia aberrans détectés à la fois à Béja et à Kairouan. Le parasitisme induit par l’hyménoptère parasite a été autour de 0,8-2,6% et celui exprimé par les larves de la mouche a été de 1,3-4,7% environ; ces taux de parasitisme sont faibles. Des tentatives d'élevage de cette guêpe peuvent être utiles pour la lutte biologique contre les scarabées moyennement des ennemis naturels indigènes.

Mots clés: Diptera, fève, Hymenoptera, Lixus pulverulentus, parasitisme ______ملخص بوهاشم، سنية ومنال حمام-بوريس ورابحة سويسي. 2016. التقرير األول لألعداء الطبيعية لسوسة ) Lixus pulverulentus( ساق الفول في تونس. .Tunisian Journal of Plant Protection 11: 245-250

تعيش سوسة الفول )Lixus pulverulentus( في وسط ساق النبتة وتسبب العديد من األضرار على النباتات المصابة. أنجزت دراسة اإليكولوجيا األحيائية لحشرة السوسة في باجة )شمال غرب تونس( والقيروان )وسط تونس( لتحديد األعداء الطبيعيين للحشرة. و قد تم ألول مرة تحديد األعداء الطبيعيين لحشرة L. Pulverulentus، وهما كل من طفيل دبور Pteromalus lixi )غشائية األجنحة، Pteromalidae( وذبابة مفترسة Zeuxia aberrans )ذوات الجناحين، Tachinidae( في كل من باجة والقيروان. كانت نسبة التطفل لغشائية األجنحة 0.8% و2.6% بينما يرقات الذباب افترست بما يعادل 1.3% و4.7%، وهي معدالت منخفضة. إن تربية هذه األعداء الطبيعية بأعداد كبيرة تجعل المكافحة البيولوجية ممكنة ضد حشرات السوس في تونس.

كلمات مفتاحية: تطفل، ذوات الجناحين، غشائية األجنحة، فول، Lixus pulverulentus ______

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