New record of aphanogmus clavicornis Thomson (Hymenoptera: Ceraphronidae) as a larval parasitoid of tomato leaf miner Tuta absoluta (Meyrick) in Syria

Tomato (Solanum lycopersicum L.) is an important edible and nutritious fruit regarded by nutritionist as a vegetable. It is an important source of vitamins and significantly contributes to economic development. However, the production of tomatoes is heavily affected by climate change, insect pests, disease and the new devastating pest of tomatoes, the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). This study includes a description of Aphanogmus clavicornis Thomson, 1858 (Hymenoptera: Ceraphronoidea), a primary parasitoid of T. absoluta whose larvae feed on all parts of the tomato plant. It is the first record of T. absoluta as a host of genus Aphanogmus worldwide and a first record of A. clavicornis in both Syria and the Middle East. Description, biology and the taxonomic characters of the new species were provided. The new record of natural parasitism of T. absoluta by A. clavicornis would add knowledge on biological control of the pest and could become an additional option for the integrated pest management of those crops where T. absoluta is a key pest. This finding will be baseline for future research. It would be interesting to investigate if A. clavicornis can be produced in large scale under laboratory conditions and test its potential use as a biological control agent within integrated pest management programs.

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Introduction

Tomato (Solanum lycopersicum L.) is an important edible and nutritious fruit regarded by nutritionist as a vegetable. It is an important source of vitamins (Abdelmaksoud et al., 2020) [1] . It is widely cultivated all over the world. In Syria tomato grows both on small and commercial large scale as a cash crop by vegetable growers. Therefore, tomato production also contributes significantly to economic development and the ability to create employment. Syria was considered to be one of the top producers of tomatoes in the world after Tunisia and Protugal. However, the production of tomatoes is heavily affected by climate change such as heavy storms, drought, humidity, insect pests, disease and the new devastating pest of tomatoes, the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). The superfamily Ceraphronoidea includes three families: Ceraphronidae, Megaspilidae and Stigmaphronidae (Johnson, 2004) [23] . There are 800 species described worldwide, although it is estimated that there could be 2000 species (Masner, 2006) [25] . The Ceraphronidae consists of 317 species in 15 genera world-wide mostly distributed in the Palaearctic Region (Belokobylski & Lele, 2019; Johnson, 2004) [7,23] . It is a family of small endoparasitic wasps (0.5-2 mm) with a black or brown body, forewing with narrow and linear stigma, mesoscutal median furrows, and wide base of mesosctum. The family is easily identified by having a curved stigmal vein, lacking a pterostigma in the forewing. An expanded pterostigma, occipital depression, uniramous anterior protibial spur, a comb of the spur on the pro-and mesotibial spurs, a single mesotibial spur, an undivided synsternite, and axillular setae were observed (Broad, 2009; Mikó et al., 2009) [8,26] . Normally, Ceraphronidae attacks species in the following insect orders: Diptera, Hymenoptera, Lepidoptera, Hemiptera (Homoptera), Neuroptera and Thysanoptera (Alekseev, 1987) [4] . They develop as endoparasitoids or hyperparasitoids (Gauld & Bolton, 1988) [17] . Aphanogmus contains 100 species (Johnson, 2004; Buhl et al., 2010; Evans et al., 2005) [23,9,14] . It contains ectoparasitoids (idiobiont) species (Parnell, 1963) [36] and endoparasitoids (koinobiont) species (Evans et Luhman, 1999) [14,24] . Aphanogmus species are usually parasitoids of cecidomyid flies and are sometimes reared as hyperparasitoids attacking hosts of various insect orders (Evans et al., 2005) [14] . T. absoluta is a Neotropical oligophagous pest attacking cultivated and wild plants with a high preference towards the species of Solanaceae plants especially tomato and other Solanaceous crops (Nurul Huda et al., 2020) [31] . It originated in South Ameria. It was first recorded in 2006 in Europe (Spain) (Urbaneja, 2007) [41] and then spread throughout the Mediterranean Basin, Central Europe and the Middle East (Ferracini et al., 2019) [15] . Since the time of its initial detection, the pest has caused serious damages to tomato in invaded areas, and it is currently considereccd as a key agricultural threat to tomato production in throughout the world (Ferracini at el., 2019) [15] . T. absoluta was first reported for Syria (Almatni, 2010; Ibrahim et al., 2012) [5,20] , neighboring Iraq (18 Abdul Razzak et al., 2010) [2] , Yemen (Husin, 2021), Ethiopia ( 20Reta & Berhe, 2015) [37] , Jordan (Al Antary & Al Shaalan, 2013) [3] and Sudan (22 Mohamed et al., 2012) [27] . Many procedures were carried out to control this dangerous pest since its arrival in Syria (Mofleh et al., 2014) [28] . Desneux et al. (2010) [12] reported that this pest may responsible for the losses of up to 80-100% in tomato plantations if left uncontrolled as it is attacking all aerial parts of the host (leaves, stems and fruits). T. absoluta is a difficult pest to manage because of the larval feeding habits and its ability to build up insecticide resistance (Abdelmaksoud et al. 2020) [1] . Nurul Huda et al. (2020) [31] and Husin (2021) have described the life cycle of this pest. Abdelmaksoud et al. 2020 [1] ; Husin (2017) [21] , Nurul Huda et al. (2020) [31] and Tarusikirwa et al. (2020) [39] gave a review of the problems caused by T. absoluta and its management strategies (Tarusikirwa et al., 2020) [39] . Based on our knowledge, the family Ceraphronidae of Syria and neighbouring countries is poorly studied. This paper deals with reports of a new record of ceraphronid from Syria. The description, biology and the taxonomic characters of the newly recorded species A. clavicornis were provided together with discussion on the significance of this new record as an additional option for the integrated pest management of those crops where T. absoluta is a key pest.

Materials and Methods

The samples of infested tomato plants by Tomato leaf miner T. absoluta were collected from a greenhouse at Al-Snowbar in Lattakia in July, 2019, taken to the Agricultural Research Centre in Lattakia and examined by a stereoscope. The parasitized larvae of T. absoluta were placed in glass tubes and closed with cotton until the emergence of adult parasitoids. The species Aphanogmus was identified using the key (Austin, 1984) and the identification was kindly confirmed by Prof. Peter Neerup Buhl (Natural History Museum of Denmark).

The parasitoid was placed on a slide using Hoyer's medium.

Images were taken with a stereomicroscope equipped with a computer-attached camera and Nikon-Eclipse 80i Digital microscope (40X) equipped with Camera Nikon E8800 (8,0 Megapixel 10x).

The specimen was deposited in the laboratory of Insects at the Scientific Agricultural Research Centre.

Results

This study recorded for the first time T. absoluta as a host of the genus Aphanogmus world-wide and the first record of A.

clavicornis as a larval parasitoid of T. absoluta in both Syria and the Middle East. The description, biology and the taxonomic characters of the new species were provided with discussion on the significance of this new record as additional option for the integrated pest management of those crops where T. absoluta is a key pest.

Aphanogmus clavicornis Thomson, 1858

Examined material 1♀, Syria, Lattakia province, Al-Snowbar, 35°53′12″ N, 35°28′31″ E, collected from tunnel in leaf on larva of T.

absoluta, from greenhouse planted with Tomato plants affected by T. absoluta in July, 2019.

Geographical distribution

Sweden, Denmark, Japan and Russia (Johnson, 2004; Noyes, 2020) [23,33] .

Biology

Larval parasitoid of various insects including Cybocephalidae (Coleoptera), Cecidomyiidae (Diptera), Bethylidae and Ichneumonidae (Hymenoptera) (Oatman, 1985 [34,14,19,35,18] . Host information has not been studied widely.

Taxonomic characters (diagnosis)

Female is 0.5 mm long, black body, yellowish brown antenna, darker scape and clava segments, dark brown tibia and femur, and yellow tarsal segments. Antenna clavate and serrate with 11-segmented and long hair on serrate side, larger terminal segements, pedicel is longer than flagellomeres (Fig. 1a,b), club 3-segmented, scape longer than club, tarsus 7-segmented, and presence of short tibial spur. Mesosoma is almost two times longer than metasoma. Metasoma is almost 1.5 times longer than the head with wide base of metasoma. Striae on metasoma are without mesoscutal median furrow. Forewing with marginal, submarginal and distally curving radial vein (Austin, 1984). Three groups of species are based on the characters of mesosoma and metasoma: clavicornis group: mesoscutal median furrow and metasomal basal carina absent. Tenuicornis group: mesoscutal median furrow absent, metasomal basal carina present. Fumipennis group: mesoscutal median furrow and metasomal basal carina present (Evans et al., 2005) [14] . The species belongs to the first group (clavicornis) According to the morphological straits of these three groups. Depending on the key of Aphanogmus (Szelényi, 1940) [38] , the new recorded species is A. clavicornis Thomson, 1858.

Discussion

This study recorded for the first time T. absoluta as a host of the genus Aphanogmus world-wide and the first record of A. clavicornis as a larval parasitoid of T. absoluta in both Syria and the Middle East. Many pest species, especially lepidopterans, are known to increase their abundance if conditions are favorable and inflict significant damage in agriculture and forestry (EPPO, 2009) [13] . It is well documented that parasitoids especially those belonging to Hymenoptera, are important elements of agroecosystems (Gauld & Bolton, 1988; Evans et al., 2005; Gray et al., 2013) [17,14,20] and are one of the most potent biological control agents that can be used to control the population growth of T. absoluta (Bompard et al., 2013; Mollá et al., 2010) [10,29] . Natural enemies such as parasitoids were successfully used in biological control of T. absoluta (Bompard et [10,29] revealed 13 larval-pupal parasitoid species including Elasmus phthorimaeae Ferriere (Elasmidae) and D. crassinervis occasionally parasitize T. absoluta in Spain (38 Gabarra et al., 2014) [16] . 16 [43] . Natural enemies of T. absoluta have been recorded, in South America 87 species (Ferracini et al., 2019) [15] , in North Africa, Europe and Middle East at least 50 parasitoids and predators some of which are used in IPM programmes, in western Palaearctic area, at least 70 natural enemies (Zappalà et al., 2013) [42] . Having said that there is no record of A. clavicornis attacking T. absoluta. This pest has rapidly spread throughout the Mediterranean Basin, in Europe, North Africa and the Middle East (Ferracini et al., 2019) [15] , Nappo (2013) [30] listed the countries which are affected by T. absoluta: Albania, Algeria, Argentina, Austria, Bahrain, Belgium, Bolivia, Brazil, Bulgaria, Cayman Islands, Chile, Colombia, Cyprus, Czech Republic, Denmark, Ecuador, Egypt, Estonia, Thiopia, Finland, France, Germany, Greece, Hungary, Iran, Iraq, Ireland, Israel, Italy, Jordan, Kosovo, Kuwait, Latvia, Lebanon, Libya, Lithuania, Luxembourge, Malta, Morocco, Netherlands, Palestinian Authority (West Bank), Panama, Paraguay, Peru, Poland, Portugal, Qatar, Romania, Russia, Saudi Arabia, Senegal, Slovakia, Slovenia, Spain, Sudan, Sweden, Switzerland, Syria, Tunisia, Turkey, United Kingdom, Uruguay, Venezuela and Western Sahara (NAPPO, 2013) [30] . Consequently, the wide and rapid spread of T. absoluta has fueled the urgent need for biological and ecological studies to be undertaken. It is well known that agricultural pests can reduce yield, increase costs and lead to the use of pesticides which ultimately contribute to adverse effects on public health, environmental contamination, lost of biological diversity, harm to nontarget beneficial arthropods, unsustainable costs to farmers, pesticide resistance and distruption of existing inregrated pest management. Therefore, pesticide should be used as a final option if other control strategies are insufficient and probable economic damage is expected (Urbaneja et al., 2013) [40] . The new record of natural parasitism of T. absoluta by A. clavicornis would add knowledge on biological control of the pest and could become an additional option for the integrated pest management of those crops where T. absoluta is a key pest. It will be important to investigate if A. clavicornis can be produced in large scale under laboratory conditions and test its potential use as a biological control agent within integrated pest management programs. Finally, there is an urgent need for more collaborative efforts among the researchers as well as growers to control T. absoluta in Syria and other parts of the world.

Acknowledgement

Acknowledgments: This research was supported by the General Commission for Scientific Agricultural Research (GCSAR), Damascus, Syria. The financial funding is greatly appreciated. Our special thanks are expressed to Peter Neerup Buhl (Natural History Museum of Denmark) for helping us in identification of A. clavicornis.

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Aphanogmus clavicornis Female: (a) Female of lateral view;

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Aphanogmus clavicornis Female: (a) Female of lateral view;

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