Research Article |
Corresponding author: Hossein Lotfalizadeh ( hlotfalizadeh@gmail.com ) Academic editor: Andreas Köhler
© 2020 Hossein Lotfalizadeh, Jean-Yves Rasplus, Massimo Cristofaro, Francesca Marini.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lotfalizadeh H, Rasplus J-Y, Cristofaro M, Marini F (2020) Tetramesa amica and its parasitoid Eurytoma amicophaga (Hymenoptera, Eurytomidae): two new species associated with medusahead, Taeniatherum caput-medusae (Poaceae). ZooKeys 1005: 133-149. https://doi.org/10.3897/zookeys.1005.56353
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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.
Biological control, Chalcidoidea, parasitoid, phytophagous, weeds
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 (
In the past, a few pathogens, such as Fusarium arthrosporioides, Pseudomonas fluorescens, Ustilago phrygica were reported as natural enemies of T. caput-medusae (
Eurytomidae (Hymenoptera, Chalcidoidea) includes 1400–1500 species distributed in 88 genera worldwide (
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 (
Until now and despite numerous surveys, no Tetramesa has been found associated with the genus Taeniatherum (
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 laboratory. 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 (
The following keys were used to identify Tetramesa species:
Abbreviations used in the text:
C1–3 first to third clavomere;
F1, F2, etc. first funiculars, second funiculars, etc.;
Gt1-n Gastral terga 1-n;
OOL ocular–ocellar line (= the shortest distance between posterior ocellus and adjacent eye margin);
POL posterior ocellar line (= the shortest distance between the posterior ocelli).
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
Holotype: female, ex Taeniatherum caput-medusae, 8 May 2017, 27 July 2018, and 21 May 2019 (galls collection dates), by F. Marini (deposited in HMIM); Paratypes: 20♀♀ & 3♂♂, same data as holotype (deposited in HMIM & CBGP).
Highway E90, between E0 Ardaniou Orestiadas and E0 Alexandroupoli Kipon, ca. 5 km west of the border of Greece-Turkey and 1.3 km northeast of Vrysoùla (40°56'58"N, 26°14'59"E), 40 m above sea level, Dimos Alexandroupoli, Greece.
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.
Holotype Female. Body length 2.4 mm. Black, coxae black, pro- and 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.
Head
in dorsal view stout, 1.7 × as broad as long, distinctly wider than pronotum; temple rounded laterally, very short, 2.0 × shorter than eye. POL 2.1 × OOL (13:6). Head in frontal view, wider than height (18:14); malar space shorter than longitudinal eye diameter (6:8). Ventral margin of clypeus slightly emarginated (Fig.
Antenna
(Fig.
Mesosoma
in lateral view elongated (Fig.
Fore wing
(Fig.
Metasoma
elongated, narrowed apically (in lateral view) (Fig.
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.
Tetramesa amica is closely related to Tetramesa inermis Erdös, 1963, T. matrana Erdös, 1969, and T. cylindrica. Diagnostic characters that enable one to discriminate T. amica sp. nov. from these species are presented in Tables
The antenna of T. amica sp. nov. resembles that of T. fumipennis except F1 that is not constricted basally (Fig.
Features distinguishing Tetramesa amica Lotfalizadeh, sp. nov. from Tetramesa inermis Erdös, 1963.
Characters | Tetramesa amica Lotfalizadeh, sp. nov. | Tetramesa inermis Erdös, 1963† |
---|---|---|
Pronotal antero-lateral yellow spots | With a pair of small yellow spots, hardly seen dorsally | With a pair of relatively large spots, well seen dorsally |
Frons sculpture in the lower part | Laterally straight and medially smooth (Fig. |
Entirely straight |
Antennal anellus in female | Wider than long (Fig. |
Longer than wide |
Length of funiculars in female |
F1 ca. 1.5 × as long as wide, F2 longer than broad, F3–5 as long as broad (Fig. |
F1 ca. 1.5 × as long as wide, F2–3 square, F4–5 transverse |
Length of clava in female | Longer than the three pre-claval funiculars together (83:72) (Fig. |
Equal to the three pre-claval funiculars together |
Male antenna | Funicule thick, funiculars constricted basally and apically (Fig. |
Funicule filiform, funiculars without basal and apical constriction |
Sculpture of mesoscutellum | Identical to pronotum (Fig. |
Coarser than pronotum |
Uncus of stigma | Distinct and long (Fig. |
As usual (not especially long) |
Host plant | Taeniatherum caput-medusae | Bromus spp. |
Features distinguishing Tetramesa amica Lotfalizadeh, sp. nov. from Tetramesa matrana Erdös, 1969.
Characters | Tetramesa amica Lotfalizadeh, sp. nov. | Tetramesa matrana Erdös, 1969 |
---|---|---|
Funiculars in female |
F2 longer than broad, F3–5 as long as broad (Fig. |
F2–3 as long as broad, F4–5 transverse |
Length of clava | Longer than the three pre-claval funiculars together (83:72) (Fig. |
Equal to the three pre-claval funiculars together |
Sculpture of mesoscutellum | Identical to pronotum (Fig. |
Coarser than pronotum. |
Propodeum | coarsely rugose (Fig. |
almost non-sloping, highly shiny, densely reticulate |
Host plant | Taeniatherum caput-medusae | Arrhenathrerum elatius L. |
Features distinguishing Tetramesa amica Lotfalizadeh, sp. nov. from Tetramesa cylindrica (Schlechtendal, 1891).
Characters | Tetramesa amica Lotfalizadeh, sp. nov. | Tetramesa cylindrica (Schelechtendal, 1891)† |
---|---|---|
Width of the head (frontal view) | 1.2 × wider than long (Fig. |
0.8 × wider than long |
Length of funiculars of the female |
F1–2 longer than wide, F3–5 quadrate (Fig. |
Only F1 longer than wide, F2–5 quadrate |
Male antenna | Funiculars non-depressed medially (Fig. |
F2–4 depressed medially |
Gastral sculpture | Mainly smooth (Fig. |
Finely alutaceous dorsally |
Length of metasoma | 1.1 × as long as mesosoma + head (Fig. |
As long as mesosoma + head |
Postmarginal vein | 1.4 × the length of marginal vein (Fig. |
As long as marginal vein |
Stigma vein | As long as postmarginal vein (Fig. |
0.7 × the length of postmarginal vein |
Host plant | Taeniatherum caput-medusae | Stipa capillata |
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.
Medusahead, Taeniatherum caput-medusae (L.) Nevski (Poaceae). Adults are phytophagous and lay eggs into medusahead stems. Oviposition and larval development induce a response of the plant, which produces stem galls, from which adults emerge.
Holotype: female, ex Tetramesa amica Lotfalizadeh, sp. nov. on Taeniatherum caput-medusae, 28 May 2017, 27 July 2018, and 21 May 2019 (galls collection dates), F. Marini leg. (deposited in HMIM). Paratypes: same data as holotype, 1♀ & 5♂♂ (deposited in HMIM & CBGP).
Highway E90, between E0 Ardaniou Orestiadas and E0 Alexandroupoli Kipon, ca. 5 km west of the border of Greece-Turkey and 1.3 km northeast of Vrysoùla (40°56'58"N, 26°14'59"E), 40 m above sea level, Dimos Alexandroupoli, Greece.
All funiculars longer than broad, with F1 ca. 2.5 × as long as wide (Fig.
Holotype. Female. Body length 3.3 mm. Coloration: body black; following areas yellow to reddish brown: profemur apically and interiorly, protibia interiorly, mid femur and tibia basally and apically, metafemur apically and metatibia basally, three basal tarsomeres, distal spurs of tibiae; wing veins brown. Valvulae mostly dark brown.
Head
1.3 × as wide as long (164:125) (Fig.
Relative measurements of mesosoma: length 205, width 120, length of pronotal collar 105, mesoscutum as long as mesoscutellum70; width of mesoscutellum 75. Pro- and mesonotum densely punctured (Fig.
Petiole. Gastral petiole transverse, bearing usual dorso-median and lateral teeth, which are acute. Gaster longer than mesosoma (105:90) (Fig.
Male (Fig.
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.
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 and E. 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
Features distinguishing Eurytoma amicophaga Lotfalizadeh, sp. nov. from Eurytoma festucae Zerova, 1977.
Characters | Eurytoma amicophaga Lotfalizadeh, sp. nov. | Eurytoma festucae Zerova, 1977† |
---|---|---|
Width of head (frontal view) | 1.2 × as wide as long (Fig. |
1.9 × as wide as long |
Male antenna | Funiculars long, F1 more than 2 × as long as wide (Fig. |
Funiculars short, F1 distinctly < 2 × as long as wide |
Scape in male antenna | long, 2.8 × as long as wide | short, 2.2 × as long as wide |
F1 length | 2.5 × as long as wide (Fig. |
2 × as long as wide |
Marginal vein | Long, more than 1.5 × as long as stigmal vein (Fig. |
Short, as long as stigmal vein |
Host | Tetramesa amica Lotfalizadeh, sp. nov. on Taeniatherum caput-medusae | Tetramesa brevicollis on Festuca spp. |
The specific name refers to the host species (Tetramesa amica Lotfalizadeh, sp. nov.) with which holotype is associated.
Tetramesa amica Lotfalizadeh, sp. nov. (Hymenoptera: Eurytomidae). Larvae feed on T. amica larvae and adults emerge from the stem galls caused by T. amica larvae on medusahead plants.
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 (
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) (
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 (
The authors are grateful to all colleagues and friends who contributed to the study in some way. Many of them supported our activities: Francesca Di Cristina and Silvia Barlattani (BBCA onlus, Rome, Italy) with technical support; Emilio Guerrieri (IPSP-CNR, Portici, Naples, Italy); Raffaele Sasso (ENEA, Casaccia, Rome, Italy) with their scientific support; Celso Azevedo and Anelia M. Stojanova for review of the manuscript, and the subject editor Andreas Köhler for his valuable help to improve this article.