Bulletin of Insectology 73 (1): 1-10, 2020 ISSN 1721-8861 eISSN 2283-0332 Thrips fauna in citrus orchard in Tunisia: an up-to-date Imen BELAAM-KORT1, Rita MARULLO2, Sabrine ATTIA1, Synda BOULAHIA-KHEDER1 1Laboratory of Bio-aggressors and Integrated Pest Management in Agriculture, National Agronomic Institute of Tuni- sia (INAT), University of Carthage, Tunisia 2Department of Agriculture, Mediterranean University of Reggio Calabria, Italy Abstract Thrips species that damage citrus are very little known in Tunisia. As a first step to establish an IPM strategy against thrips in cit- rus orchards, an inventory of species was carried out from Navel oranges trees and herbaceous plants in the vicinity. The status of each species was determined and the relationship between thrips damaging citrus, predaceous thrips and both agroecosystem were investigated. Samples of thrips were collected from orange trees, herbaceous plants and soil under canopy. A total of twenty-one thrips species were collected with 6 new findings. To help identification of these species likely to be found in Tunisia, an easy-to- use dichotomous key of all recorded species was designed. The most abundant species in navel oranges trees were Frankliniella occidentalis (Pergande), Thrips major Uzel and Pezothrips kellyanus Bagnall. Six species among the total identified were preda- tors. The thrips fauna living in citrus groves between citrus and weeds is rich, but not all species have the same economic im- portance for citrus. Here, F. occidentalis, P. kellyanus and T. major are the major species at least regarding their abundance. Her- baceous plants in citrus orchards may play a key role in maintaining these species and also predaceous ones providing food when the susceptible citrus organs are not available. The data obtained are critical for biological conservation strategies. Key words: thrips species, citrus tree, herbaceous plants, sampling, Tunisia. Introduction ermis which have been recorded for their severe damage in several regions of Spain (Longo, 1986; Lacasa et al., Thysanoptera are one of the insect orders widespread 1996; Marullo and De Grazia, 2012). In addition, others throughout the world with about 6,164 species belong- thrips associated with citrus fruits have been cited such ing to 782 genera and 2 suborders, Terebrantia and Tu- as F. occidentalis, Thrips major Uzel 1895, T. tabaci, bulifera (ThripsWiki, 2017). Thrips are minute insects Thrips meridionalis (Priesner), Thrips angusticeps Uzel characterized by asymmetric mouth-parts and by four (Navarro et al., 2008; Teksam and Tunç, 2009). These slender wings with a long fringe of marginal cilia (Lew- thrips are polyphagous but they were not reported to is, 1997). Some species like Frankliniella occidentalis cause damage on citrus fruits. According to Lacasa et (Pergande) and Thrips tabaci Lindeman are of econom- al. (1996), the diversity of plants that grow in citrus or- ic importance mainly due to their polyphagy and ability chards may favour the spread of these thrips and en- to transmit pathogens to crops (Mortazavi and Aleofoor, hance their presence in citrus flowers. 2015). In the case of citrus orchards, thrips have been In Tunisia, an inventory achieved in 2012 in citrus or- reported as new important economic pests in several chards reported the presence of 14 species of thrips countries including Tunisia where fruit scars attributed among them the most abundant was T. major with 90%, to thrips are increasingly being reported in recent years then P. kellyanus and F. occidentalis with 3.3% and (Conti et al., 2001; Marullo and De Grazia, 2012; 2.6% of the thrips respectively (Belaam-Kort and Bou- Planes et al., 2015; Belaam-Kort and Boulahia-Kheder, lahia-Kheder, 2017a). 2017a). In different regions of the world many thrips The objective of this research was to improve species are considered pests of citrus such as: Pe- knowledge about citrus thrips as emerging pests and zothrips kellyanus (Bagnall), Scirtothrips aurantii precisely to determine the status of phytophagous spe- Faure, Scirtothrips citri (Moulton), Scirtothrips dorsalis cies found and distinguish dominant from minor spe- Hood, Scirtothrips inermis Priesner, Chaetanaphothrips cies. During three years a more comprehensive invento- orchidii (Moulton 1907), Chaetanaphothrips signipen- ry of thrips fauna living in Tunisian citrus orchards was nis (Bagnall), Frankliniella bispinosa (Morgan), Helio- performed on orange trees, which represent the main thrips haemorrhoidalis (Bouche) and Thrips ha- citrus orchards grown in the monitored area, on weeds waiiensis (Morgan) (Quayle, 1938; Ebeling, 1959; and in soil, to investigate the relationship between these Blank and Gill, 1997; Parker and Skinner, 1997; Lacasa strata regarding thrips damaging citrus fruits and preda- and Llorens, 1998; Bedford, 1998). In the Mediterrane- ceous thrips. an Basin, only three species are considered as citrus Finally, to facilitate the determination of species likely pests: P. kellyanus which has recently become a harmful to be found in Tunisia, a simplified identification key to insect in some Mediterranean regions such as Italy, thrips living in citrus orchards has been developed based Spain and Greece (Marullo, 1998; Varikou et al., 2009; on some important criteria such as wing venation, an- Navarro et al., 2013), H. haemorrhoidalis and S. in- tennal sensoria and number of segments. Materials and methods Mounting and identification of thrips In the laboratory, the adult of thrips were mounted on- Collecting thrips from citrus and herbaceaous plants to slides in Canada balsam medium by using the proto- This work was carried out in four citrus orchards of col of Mound and Kibby (1998). Larvae were mounted Navel oranges variety, two located in Bizerte (Ghar directly into Hoyer’s medium. Melh and Alia) (37°10.1466'N 10°2.0868'E, elevation: Thrips were identified based on a combination of sev- 100 m a.s.l.) and the others in Mornag (Sidi Saad and eral recognized keys: Palmer et al. (1989), Mound and Khlidia) (36°40.7586'N 10°17.517'E, elevation: 32 m Kibby (1998), Zur Strassen (1996; 2003), Moritz et al. a.s.l.). In each orchard, thrips were collected weekly or (2004), Marullo (2003) and Mound and Reynaud monthly on orange trees from March to the end of June (2005). during the 3 years 2015-2017, by picking 50 flowers or The effort deployed to identify the collected material fruitlets which is a standard method used to sample allowed to build a dichotomous key for identification of thrips (Navarro et al., 2011) and also by hitting branch- citrus thrips of Tunisia, based on the major and easy to es onto a funnel of 18 cm diameter (Fauvel et al., 1981) observe morphological characters reported in the litera- from March 2015 until September 2017. ture-selected texts. Concomitantly flowers of herbaceous plants beneath trees were collected and placed in tubes filled with al- Statistical analysis cohol 70° to be examined for thrips species, from or- Data were analysed using the Graph Pad Prism for chards of investigation as well as from others in Tunis analysis of variance (ANOVA), version 5.01 for Win- and Menzel Bouzelfa. dows, Graph Pad Software, San Diego, California, USA (http://www.graphPad.com). All tests were applied un- Collecting thrips from soil of citrus orchards der two-tailed hypotheses and the significance level P Samples of leaves litter and surface soil were also tak- was set at 0.05. Tukey’s test was used to compare en monthly in the same citrus groves under the citrus means. canopy at the rate of 4 samples per orchard. Each sam- ple consisted of a quantity of soil that fills a cylinder of diameter 15 cm/ 10 cm height. The samples were taken Results randomly from a surface area of 20 × 20 cm and 5 cm depth. They were taken back to the laboratory where Composition of thrips species on Navel oranges thrips were extracted using the Berlese funnel. This de- trees and in the soil vice allows the extraction of insects from a litter/soil by Twenty-one thrips species distributed in 3 families a heating system that makes insects escape and fall in were identified from 2290 specimens collected from cit- 70° alcohol tubes. Then thrips were separated from oth- rus trees during 2015-2017 (table 1). Five species be- ers insects and mites under a binocular microscope. longing to both families Thripidae and Aeolothripidae, Table 1. List of Thysanoptera species identified from Navel orange orchards (trees and soil). Species Families Sub-orders Melanthrips fuscus (Sulzer 1776) * Melanthrips pallidior Priesner 1919 ** Ankothrips niezabitowskii (Schille 1910) ** Aeolothrips intermedius Bagnall 1934 Aeolothripidae Aeolothrips collaris Priesner 1919 Franklinothrips megalops (Trybom 1912) Franklinothrips vespiformis (D.L. Crawford 1909) ** Thrips major Uzel 1975 * Thrips tabaci Lindeman 1889 * Terebrantia Thrips angusticeps Uzel 1895 Thrips meridionalis (Priesner 1926) Frankliniella occidentalis (Pergande 1895) * Pezothrips kellyanus (Bagnall 1916) * Thripidae Megalurothrips sjostedti Trybom1908 ** Limothrips cerealium Haliday 1836 Stenothrips graminum Uzel 1895 Chirothrips manicatus Haliday 1836 ** Scolothrips longicornis Priesner 1926 ** Haplothrips tritici (Kurdjumov 1912) Haplothrips minutus (Uzel 1895) Phlaeothripidae Tubulifera Liothrips oleae (Costa 1857) * species collected from both soil and trees; ** species recorded for the first time in Tunisian citrus orchards. 2 Figure1. Ventral abdominal tergite VIII of second instar larva. a) sclerotized teeth for P. kellyanus. b) long finely pointed microtrichia for F. occidentalis. (Scale bars: 30 µm). also recovered from citrus trees were identified from a Abundance and frequency of thrips on Navel or- total of 341 thrips (148 adults, 60 larvae and 133 anges trees and in the soil nymphs) found in the litter/surface layer soils of the four On Navel oranges trees: orchards in 2016 and 2017 (table 1). Fourteen species The majority of thrips species found on Navel oranges belonging to Thripidae and Phlaeothripidae are phytoph- belongs to the family Thripidae (table 2). Among them agous and seven belonging to Aeolothripidae.