Tetramesa amica and its parasitoid Eurytoma amicophaga (Hymenoptera, Eurytomidae): two new species associated with medusahead, Taeniatherum caput-medusae (Poaceae)

Abstract Medusahead, Taeniatherum caput-medusae (Poales: Poaceae), is an annual grass native to central Asia and the Mediterranean region. It is a noxious, invasive weed in much of western North America. During field explorations carried out in Greece in 2017, the new phytophagous eurytomid Tetramesa amica Lotfalizadeh, sp. nov. and its parasitoid Eurytoma amicophaga Lotfalizadeh, sp. nov., also new to science, were recorded for the first time on medusahead. These new species are described and characters that enable to recognize them from their closest relatives are summarized. Tetramesa species are generally species-specific gall-inducers. They induce damages that may have a significant impact on the physiology of infested plants by reducing the productivity of flowering heads and seed weight. Based on these data, T. amica Lotfalizadeh, sp. nov. is currently being investigated as a candidate biological control agent of medusahead.

introduction Medusahead, Taeniatherum caput-medusae (L.) Nevski (Poaceae), is a self-pollinating annual grass, native of the Mediterranean region. It has been introduced in northern and north-western Europe, Chile, Australia, as well as in the Americas (Major et al. 1960;Peters 2013;Kyser et al. 2014). This grass is currently listed as a noxious, invasive weed in many states of Western USA, with a 12% spreading rate per year (Rice 2005). In most cases, it becomes quickly established in the localities where it was introduced (Archer 2001). Taeniatherum caput-medusae is highly competitive and replaces more desirable annual grasses and forbs (Sharp et al. 1957), but it is almost worthless as forage.
In the past, a few pathogens, such as Fusarium arthrosporioides, Pseudomonas fluorescens, Ustilago phrygica were reported as natural enemies of T. caput-medusae (Sforza et al. 2004). A species of eriophyid mite, Aculodes altamurgiensis, which is highly specific to medusahead, is currently under investigation as a candidate for biological control (Cristofaro et al. 2020). However, until now no phytophagous insect has been reported to develop on this weed.
Eurytomidae (Hymenoptera, Chalcidoidea) includes 1400-1500 species distributed in 88 genera worldwide (Noyes 2020) and they are mostly parasitoids. In the Palaearctic region, the family includes phytophagous species, mostly in the genera Tetramesa, Bruchophagus and Systole. Most of the 202 described species of Tetramesa are known to be species-specific and their host-range is generally restricted to a single grass species, a genus or, in a few cases, on closely related genera (Phillips 1936;Claridge 1961;Dawah 1987). Eggs are laid in the stems of the host plants and the larvae are stem galling and borers, whereas adults feed on nectar (Claridge 1961;Claridge and Dawah 1994;Al-Barrak et al. 2004). Galls induced by the larvae can reduce the productivity of flowering heads and seed weight (Claridge 1961;Spears 1978) and a few Tetramesa spp. are sometimes considered pests of crops (Phillips 1927;Spears 1978;Spears and Barr 1985). Claridge (1958Claridge ( , 1961, Szelényi (1968), and Zerova (1965, 1967 extensively revised the Palaearctic species of Tetramesa, and Graham (1974) studied the species fauna of England.
The significant impact on their host and their high host-specificity make Tetramesa species interesting candidates for biological control of weeds. Some species of Tetramesa have already been used against invasive grasses such as Arundo donax in the USA (Goolsby and Moran 2009) and Sporobolus spp. in Australia (Witt and McConnachie 2003).
Until now and despite numerous surveys, no Tetramesa has been found associated with the genus Taeniatherum (Noyes 2020). Our study presents the first record of a phytophagous eurytomid wasps associated with T. caput-medusae. We describe Tetramesa amica Lotfalizadeh, sp. nov. and its parasitoid, Eurytoma amicophaga Lotfalizadeh, sp. nov. (Hymenoptera: Eurytomidae).

Materials and methods
Infested samples of T. caput-medusae were collected near the town Alexandroupoli (Greece) close to Greek-Turkish border, from 2017 to 2019 and examined in the labo-ratory. The site was visited once a month, from May to July, and stem galls were collected. Insects were obtained by natural emergence to adults from spikes kept under controlled conditions (24-26 °C, 80% RH, 16L:12D), or by dissecting dry stem galls. Specimens were desiccated using HMDS (Heraty and Hawks 1998) and glued on point cards. Terminology follows Harris (1979) for cuticular sculpture and Lotfalizadeh et al. (2007) for morphology.
Abbreviations used in the text:

results
Two eurytomid species belonging to Tetramesa and Eurytoma were obtained from stem galls on T. caput-medusae. These two species appeared to be new and are described hereafter Diagnosis. Tetramesa amica Lotfalizadeh, sp. nov. differs from other species of Tetramesa by the combination of the following characters: in female, F1-2 longer than broad, F3-5 as long as broad; fore wing with an obscure black spot under marginal vein; gaster longer than head+ mesosoma; marginal vein much longer than postmarginal and stigmal veins; in male all funiculars longer than wide, with long setae, longer than width of funicule; F1-3 as same as long.
Description. Holotype Female. Body length 2.4 mm. Black, coxae black, proand mesofemur brown with a median dark band, metafemur dark brown at apex, all tibiae brown with a faint dark brown median band, tarsi bright yellow, except last tarsomere; tegula dark medially and brown in margin; pronotum with pair of small yellow spots antero-laterally; fore wing hyaline, slightly infuscate below marginal vein; veins yellowish brown. Antenna mainly dark, except scape basally, pedicel in distal half and anellus brownish; ovipositor brown. Setae on body whitish, those on wings blackish.
Male. Length of body 2.1-2.3 mm. Coloration and sculpture as in females, but yellow spots smaller and predominant on face and upper corners of pronotum. Antenna ( Fig. 1D) with seven flagellomeres and long pubescence. Petiole of first tergum short, at most twice longer than its width. Metasoma long, 0.5-0.65 × as long as mesosoma.
The antenna of T. amica sp. nov. resembles that of T. fumipennis except F1 that is not constricted basally (Fig. 1C) (conical in T. fumipennis), with five funiculars, with three clavomeres (respectively six and two in T. fumipennis), head in its lower part wider than in T. fumipennis and gaster more flattened dorsally than in T. fumipennis.
Etymology. The specific epithet derives from the Latin noun amicus (i.e., friendship) and refers to the friendship between entomologists from different countries (France, Iran, and Italy), which made possible the sampling, discovery, and description of this new species.
Variations. Body length ranges from 2.5 to 3.6 mm. Pro and mesofemora, scape sometimes nearly entirely black. Marginal vein slightly to distinctly longer than stigmal vein.
Comparative notes. Eurytoma amicophaga Lotfalizadeh, sp. nov. is distinct from other species of this species group. It is characterized by elongated funiculars, although E. steffani Claridge, 1959 andE. pollux Claridge, 1959 share similar funicular segments. However, E. steffani has all funicular segments longer than broad (F4-5 quadrate in E. amicophaga Lotfalizadeh, sp. nov.). Eurytoma pollux obviously differs from E. amicophaga in the longer head in frontal view, less than 1.2 × longer than broad (wider head, more than 1.3 × longer than broad in E. amicophaga Lotfalizadeh, sp. nov.) and marginal vein more than 1.5 × as long as stigmal vein (less than 1.5 × as long as stigmal vein in E. amicophaga Lotfalizadeh, sp. nov.). Eurytoma amicophaga Lotfalizadeh, sp. nov. is also closely related to E. festucae Zerova, 1977 and may be separated by characters summarized in Table 4. Etymology. The specific name refers to the host species (Tetramesa amica Lotfalizadeh, sp. nov.) with which holotype is associated.

Discussion
Several studies have been carried out on the taxonomy and biology of species of Eurytoma and Tetramesa associated with grasses in the Palaearctic region. However, no revision of these genera has been published so far and the identification of species remains difficult. This is also due to the rather uniform morphology of these wasps that renders their identification challenging (Henneicke et al. 1992;Lotfalizadeh et al. 2007). Tetramesa amica Lotfalizadeh, sp. nov. belongs to the cylindrica species group of Tetramesa. This distinctive group of species is characterized by the alutaceous sculpture of head and thorax, without distinct umbilicate punctures, and with small pronotal yellow spots (Claridge 1961). The cylindrica species group includes T. aciculata (Schlechtendal, 1891), T. cylindrica (Schlechtendal, 1891), T. dispar Zerova, 1965, T. ukrainica Zerova, 1965, T. punctata Zerova, 1965and T. scheppigi (Schlechtendal, 1891 (Claridge 1961;Zerova 1976).
Several species of Tetramesa have been shown to efficiently affect the populations of their host plants. Substantial reduction in seed weight was reported for an undescribed Tetramesa on Aristida longiseta Steud., Sitanion hystrix (Nutt.), Sporobolus cryptandrus (Torr.) and Stipa comata Trin. & Rupr. (i.e., 47, 33, 46, and 60%, respectively), with consequent reduction in seed germination (e.g., up to 99% of A. longiseta seeds not germinating) (Spears and Barr 1985). Witt and Mc Connachie (2003) collected a stem-boring Tetramesa species on Sporobolus pyramidalis P. Beauv, S. africanus Poir. A. Robyns and Tournay and S. natalensis (Steud.) in South Africa. They reported a high rate of prevalence of Tetramesa in stems with up to 33% of S. pyramidalis infested by Tetramesa larvae. Inflorescences of approximately 60% of the infested culms were malformed and significantly shorter than non-infested one. Finally, the stem-galling wasp T. romana is considered one of the best biological control agents released in USA to control giant reed (Arundo donax) (Goolsby and Moran 2009;Goolsby et al. 2016;Moran et al. 2017). Therefore, based on our current knowledge on Tetramesa spp., T. amica exhibits characteristics to be considered a prospective biocontrol agent against T. caput-medusae. Since few biological and ecological informations are currently available on this phytophagous species, more studies are needed to better characterize biological traits, host specificity, duration of immature stages, number of generations, fecundity, and longevity of adults. More information is also needed on its natural distribution in the Western Palaearctic region.
Species of Tetramesa are frequently parasitized by other chalcid wasps or exploited by inquilines. These antagonistic species appear to be also highly specialized on one or a few host species (Dawah et al. 1995(Dawah et al. , 2002Dubbert et al. 1998;Matsumoto and Saigusa 2001). During our field surveys, we discovered that T. amica is parasitized by E. amicophaga Lotfalizadeh, sp. nov. Females of this species exhibits fusiform flagellomeres (Fig. 3C), a relatively long marginal vein (1.2 × as long as stigmal vein) (Fig. 3B), and a horizontal ovipositor (Fig. 4C) which indicate that Eurytoma amicophaga Lotfalizadeh, sp. nov. belongs to the appendigaster species group as outlined in Claridge (1959) and Lotfalizadeh et al. (2007) (named the phragmiticola species group by Zerova (2010)). This species group contains parasitoids of Tetramesa species developing in grass stems. The exact biology of this parasitoid remains to be discovered, and studies are requested to better evaluate parasitism rates of E. amicophaga and how it may affect the performance of T. amica to control medusahead.