Short Communication A Survey of Thrips and their Potential for Transmission of Viruses to Crops in (): First Record of the Species Frankliniella intonsa and Thrips flavus

Sabah Razi, Laboratoire LATPPAM, Département de la Science de l’Agriculture, Université de Biskra, Biskra 07000, Algeria, Ernest C. Bernard, Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, Tennessee, USA, Malik Laamari, Laboratoire LATPPAM, Institut des Sciences Agricole et Vétérinaire, Université de Batna 1, Batna 05000, Algeria ______

ABSTRACT Razi, S., Bernard, E.C., and Laamari, M. 2017. A survey of thrips and their potential for transmission of viruses to crops in Biskra (Algeria): First record of the species Frankliniella intonsa and Thrips flavus. Tunisian Journal of Plant Protection 12: 197- 205.

Thrips are the main phytophagous insects on many agricultural crops and plants in Algeria that have not yet been thoroughly studied. These pests have been reported as vectors of viruses. The investigation was conducted on vegetable crops between 2014 and 2016 in six arid area sites at Biskra. Thrips species were sampled from 14 vegetable crops. Four species were affiliated to the genus Frankliniella (F. occidentalis, F. intonsa), and two to the genus Thrips (T. tabaci and T. flavus). Two sympatric species namely F. occidentalis and T. tabaci were collected from the majority of the vegetable hosts in all the studied sites, while F. intonsa and T. flavus were sampled only from pepper and they were signaled for the first time in Algeria. The current survey updates the information on the Thysanoptera of Biskra region and highlights their importance in agriculture, particularly in the greenhouses. This survey may be useful for producers and scientists to consider the risk of these harmful pests.

Keywords: Algeria, thrips, vectors, vegetable crops, virus ______

Biskra region, known as gate to Thrips are very small and tiny the desert of Algeria, ranks first in insects (adults are about 2 mm long or production of vegetables in the country less) with two pairs of fringed wings and where about 213,266 tons of early are unusually wingless (Lewis 1973). vegetables were produced recently (DSA They are divided into two suborders, 2014). Climatic conditions are favorable Tubulifera and Terebrantia, that differ in to the development of agriculture but the the shape of the last abdominal segment impact of insect pests is also important. and the ovipositor. Tubulifera have the last abdominal segment tubular and the females lack an ovipositor, while Corresponding author: Razi Sabah Email: [email protected] Terebrantia, have the last abdominal segment conical and the females have a well-developed saw like ovipositor. Both Accepted for publication 9 November 2017 larvae and adults of thrips are plant

Tunisian Journal of Plant Protection 197 Vol. 12, No. 2, 2017 feeders, while a few species feed on between 1996 and 2006 in many crops fungus and some others are predators (cowpea, tobacco, tomato, and pepper) in (Lewis 1973). They cause damage to Europe. crops directly by feeding, and by In Algeria, many bacterial and transmitting virus diseases (Bournier viral diseases have been recorded on 1982). More than 300 plant species crops, but there was little information on belonging to 45 different families were the presence or not of thrips species and affected by viruses transmitted by Thrips their ability to transmit diseases. (Bournier 1982). Additionally, thrips can However, Tospovirus was reported in also transmit some bacterial and fungal Algeria by EPPO Global Database diseases (Childers and Achor 1995; maintained by the Secretariat of the Tommasini and Maini 1995). European and Mediterranean Plant Thrips-vectored viruses belong to Protection Organization (EPPO 1997) and the genera Tospovirus, Ilarvirus, by Loebenstein and Lecoq (2012) Carmovirus, Sobemovirus, and suggesting that thrips were their main Machlomovirus (Jones 2005). They are vector. the only vectors of Tospovirus within the This study was focused on Bunyaviridae family (German et al. 1992; determining the presence of thrips and Ullman et al. 1997). Tospoviruses include their potential to transmit plant viruses in TSWV (Tomato Spotted Wilt Virus), the region of Biskra located in arid area which affects vegetable crops, especially which is adequate climate for the tomato, pepper and chrysanthemum, and development of thrips on the vegetable INSV (Impatiens Necrotic Spot Virus) crops grown under greenhouses. which affects mostly the ornamental plants (Bournier 1982). The first stage MATERIALS AND METHODS larvae of thrips acquire the virus (Moritz Study sites. et al. 2004) and transmit it later to plant The research was conducted in as adult thrips (Palmer et al. 1989). In Biskra, located at 400 km from the total, 14 species of Thripidae belonging to capital, in the northeastern of Algeria, on four genera are recorded as virus vectors the northern edge of the desert (Fig. 1). i.e. namely Frankliniella occidentalis, F. Field collection of thrips was carried out schultzei, F. intonsa, F. bispinosa, F. monthly from November to June cephalica, F. zucchini, F. fusca, F. between 2014 and 2016 in six sites. The gemina, Thrips tabaci, T. palmi, T. selected sites are located at different setosus, Scirtothrips dorsalis, elevations in the Northern and Eastern Ceratothripoides claratris, and part of the region. Three sites were Dictyothrips betae. The species F. located in the east of Biskra, and the occidentalis, F. intonsa, F. schultzei, T. others in the west (Fig. 1). tabaci, T. palmi, and D. betae were The selection of sites was based on reported in the Mediterranean area accessibility of crop diversity and (Turina et al.2012). agricultural stations in the region. At each Prins and Goldbach (1998) have location, vegetable crops were estimated $1 billion of annual losses due investigated for thrips. For each crop, an to the infection of tomato by area of 100 m2 was delimited, and 10 host Tospoviruses. Riley et al. (2011) have plants were selected randomly, while the estimated $326 million of losses border plants within each row were attributed to thrips-vectored viruses excluded (Rueda et al. 2007).

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Fig. 1. Geographical location of sampling sites. 1: M’zirâa, 2: Ain Naga, 3: , 4: , 5: , 6: . The details of the studied sites and their geographical coordinates are presented in Table 1.

Table 1. Geographic coordinates of the study sites

Zones Municipality Locality Latitude Longitude Elevation (m) Ain Naga El Mansaf 34°39'02.0"N 6°12'03.2" E - 9

M’zirâa Oued Tarfa 34°43'05.5"N 6°17'19.8" E 33 East Sidi Okba Oued Braze 34°46'22.5"N 5°51'13.2" E 53 Doucen Draa Ben Amraoui 34°37'54.8"N 5°06'23.5" E 180

Lioua El Marmoutha 34°36'02.1"N 5°23'14.6" E 100 West El Ghrous El Marhoum 34°44'02.8"N 5°14'11.5" E 189

Sampling of thrips. plant was taken carefully in a zip bug, Three main types of sampling then transferred to the laboratory, washed techniques were applied for this and thrips were extracted under a investigation; (1) direct sampling (plant dissecting microscope). Collected thrips were checked and thrips were collected were stored in ethanol 60%. The sampling using a fine brush in a vial containing methods varied depending on grown crop, ethanol at 60%), (2) by scouting (plants morphological traits of the plants and on were scouted under a white cloth, thrips the type of damage observed on plant dislodged were collected by a fine brush parts (Palomo et al. 2015). For tomato into labeled vials containing also ethanol and pepper, a white cloth was placed at 60%), and (3) by washing (a part of the under each plant and the top two thirds of

Tunisian Journal of Plant Protection 199 Vol. 12, No. 2, 2017 the plant was vigorously shaken to collect were infested by F. occidentalis and T. the specimens. The washing method was tabaci. These two species were applied for collection of thrips associated encountered in all the investigated sites to Zucchini where 3 young leaves were probably due to their polyphagous taken from each plant in a zip bag behavior. (Palomo et al. 2015) and transferred to F. intonsa and T. flavus were the laboratory for thrips extraction. Only detected only in pepper in all the six adult of thrips were transferred into surveyed sites. This suggested that their labeled vials containing ethanol 60%. distribution is related to host plant and not to the location. Artichoke and carrot Identification of thrips hosted only one species i. e. F. Family and genus of thrips were occidentalis and T. tabaci respectively. identified using morphological methods These crops are not largely cultivated in and taxonomic keys (Mound and Kibby Biskra as compared to pepper and tomato. 1998). According to Mound and Kibby (1998) protocol and due to the small size DISCUSSION of thrips, which required an accurate The reported survey represents a identification and magnification of general distribution of thrips from specimens with a microscope, each thrips different hosts in the selected sites where was glued to a microscope slide. four thrips species (namely F. Specimens were mounted on slides in occidentalis, F. intosa, T. tabaci, and T. Hoyer’s medium (40 ml water; 30 g gum flavus) were identified in the region of arabic, and 200 g chloral hydrate). Biskra (Zur Strassen, 2003). Based on our Morphological methods of findings, the presence of these species identification required the examination of was not related to the location but to the various features of the thrips including host plant as previously noted by Lewis color, size, number of antennal segments, (1973). distribution and number of setae across F. occidentalis was studied by the body and along the forewing (Mound Rechid (2011) and Razi et al. (2013) on and Kibby 1998). Thrips were identified Vicia faba and also by Laamari and using an Olympus compound microscope Houamel (2015) on tomato, pimento and according to Mound and Kibby (1998), pepper in Biskra area. These authors Moritz et al. (1994) and Zur Strassen found that this species is the most (2003). abundant and harmful one, and the most serious pest among Frankliniella species RESULTS (Kirk and Terry 2003). It has a worldwide A total of 14 vegetable crops distribution (Mound and Walker 1982). It belonging to 7 botanical families were feeds on more than 200 host plant species investigated for the presence of thrips that (Zur Strassen et al. 1997) and has been could serve as virus vectors (Table 2). generally considered as a potential vector The survey showed the presence of four of viruses TSVW and INSV (Peters et al. species namely F. occidentalis, F. intosa, 1996; Wijkampet al.1995).The results of T. tabaci, and T. flavus. our investigation highlighted a wide This investigation highlighted that distribution of this species in all the pepper hosted four different species of studied sites, and especially on target thrips but carrot was infested by only one crops. species. The remaining prospected crops

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Table 2. Thrips virus-vectors recorded from the studied crops and municipalities

Virus thrips Botanical family Crop Municipality vector

F. occidentalis Lioua, M’zirâa, El T. tabaci Pepper Ghrous, Doucen, Ain F. intonsa Naga, Sidi Okba T. flavus Lioua, M’zirâa, Ain Naga, Pimento Solanaceae Sidi Okba Lioua, M’zirâa, El Tomato Ghrous, Sidi Okba, Ain Naga Lioua, El Ghrous, Ain Eggplant Naga F. occidentalis T. tabaci Lioua, M’zirâa ,

Ain Naga, Sidi Onion Okba, Doucen, El Alliaceae Ghrous Lioua, M’zirâa, El Garlic Ghrous, Sidi Okba, Ain Naga. Lioua, El Ghours, Ain Brassicaceae Cauliflower Naga. Artichoke Sidi Okba F. occidentalis Asteraceae Lettuce M’zirâa, Sidi Okba, Lioua Doucen , Sidi Okba, Zuchini Ain Naga, Lioua, F. occidentalis M’zirâa, El Ghrous T. tabaci Cucurbitaceae Watermelon Lioua Lioua, M’zirâaa, El Melon Ghrous, Sidi Okba Apiaceae Carrot Lioua T. tabaci F. occidentalis Amaranthaceae Beet Doucen T. tabaci

Furthermore, T. tabaci was also presence of T. tabaci in Algeria but found in all the surveyed crops and sites. without specifying the region and the host It is a polyphagous (Liu and Sparks plants. It is difficult to control this species 2003), and cosmopolitan species (Zur as it develops rapidly resistance to Strassen et al. 1997). This thrips species insecticides (Broadbent et al. 1990; was associated to 32 plant families in Iran Sakimura 1963). (Alavi et al. 2007), 25 plant families in Both F. intonsa and T. flavus, Croatia (Marulloand De Grazia 2013), sampled from pepper were signaled for and 29 families in Italy. T. tabaci is an the first time in Algeria and precisely in important pest of onion, cotton and Biskra area. This result was the first tobacco (Raspudicand Ivezi 1999). observation in all the North Africa, but F. Bournier (1970) was the first to report the intonsa was widespread in Europe and

Tunisian Journal of Plant Protection 201 Vol. 12, No. 2, 2017 China. It is associated to Fabaceae virus-transmitting vector among them according to Podozniak (2011), to Mound (1996) and Singh and Fabaceae, Chenopodiaceae and other Krishanareddy (1995) who described the plant families based on Raspudic et al. Indian isolate of TSWV-W as being (2009) report, and to Fabaceae, transmitted by T. flavus, that was also Asteraceae, strawberry as noted by Lim reported by Boonham et al. (2002). and Mainali (2009). It was often found in The remaining three species, high population densities on its hosts. namely T. tabaci, F. occidentalis and F. Damage caused by F. intonsa was serious intonsa, are the most dangerous pests to on peach, plum and other fruit trees vegetable crops and plants (Mound 1997) (Bournier 1982). It was reported as a due to their capacity to transmit viruses in Tospovirus vector, with less importance the Mediterranean area (Turina et al. as a vector of Tomato Chlorotic 2012). Spot Virus (Bournier 1982). This study was an inventory of Nickel (2008) mentioned that T. thrips as potential vectors of transmission flavus was often intercepted from Europe, of viruses in Biskra. Four species among Mediterranean countries, particularly in them were found in this investigation in North America, Russia and the many host plants. Two species, T. flavus Philippines. It was reported by Priesner and F. intonsa, were recorded for the first (1960) in Egypt and by Minaei (2013) in time in Algeria. However, F. intonsa was Iran. Zur Strassen et al. (2003) considered recorded for the first time in North this species as a semi-cosmopolitan Africa. This work led gardeners and species of many host plants. Moreover, it scientists to know about the presence of was signaled on apple in India (Singh these species in Algerian crops, especially 1989) and classified as harmful pest of in the region of Biskra, and to adopt many other crops (Mound and Azidah appropriate control strategies against 2009; Nickel 2008). Many authors these harmful pests. mentioned that this species is the main ______RESUME Razi S., Bernard E.C. et Laamari M. 2017. Enquête sur les thrips et leur potentiel de transmission de virus aux plantes cultivées dans la région de Biskra (Algérie): Premier signalement des espèces Frankliniella intonsa et Thrips flavus. Tunisian Journal of Plant Protection 12: 197-205.

Les thrips sont les principaux ravageurs de plusieurs cultures et plantes en Algérie et ne sont pas encore étudiés. Ces ravageurs sont connus comme des vecteurs de virus. Cet inventaire a été réalisé sur les cultures légumières durant 2014-2016 dans six stations de la région aride de Biskra. Les thrips ont été inventoriés sur 14 cultures légumières. Deux espèces ont été affiliées au genre Frankliniella (F. occidentalis, F. intonsa) et deux au genre Thrips (T. tabaci et T. flavus). Les deux espèces, F. occidentalis et T. tabaci, ont été collectées dans la majorité des cultures et dans toutes les stations prospectées. Toutefois, F. intonsa et T. flavus étaient échantillonnés uniquement à partir du poivron et ont été signalés pour la première fois en Algérie. Cette présente investigation a mis à jour les informations sur les thrips de Biskra et à leur importance dans l’agriculture et peut être utile pour les agriculteurs et les scientifiques pour prendre en considération ces ravageurs endommageant les cultures.

Mots clés: Algérie, cultures légumières, thrips, vecteurs, virus ______

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______ملخص رازي، صباح وارنست كلود برنارد ومليك لعماري. 2017. جرد حول حشرات التربس وقدرتها الناقلة للفيروسات إل ى المحاصيل الزراعية بمنطقة بسكرة (الجزائر) وأول تسجيل لنوع ي Frankliniella intonsa و Thrips flavus. Tunisian Journal of Plant Protection 12: 197-205.

حشرات التربس هي من أهم أفات النباتات والزراعات في الجزائر والتي لم تدرس بعد. وتعرف هذه اآلفات كعناصر ناقلة لإلمراض الفيروسية. أجري هذا الجرد على الخضراوات من 2014 إلى 2016 بست مناطق جافة في بسكرة. تم تحديد أربعة أنواع من التربس على 14 محصول نباتي. وتم تصنيف نوعيْن من جنس Frankliniella هما F. occidentalis وF. intonsa و نوعيْن من جنس Thrips هما T. tabaci وT. flavus. تم تجميع النوعين .F occidentalis و T. tabaci من غالبية المحاصيل وجميع المناطق. حي ن هذا الجرد المعلومات عن حشرات التربس ببسكرة وب ين أهميتها في الزراعة كما يمكن أن يكون مفيدا للمزارعين وللباحثين لألخذ باالعتبار هذه الحشرات الضارة.

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