Anagrus (Anagrus) arboridiae Triapitsyn & Adachi-Hagimori, 2020

Triapitsyn, Serguei V., Adachi-Hagimori, Tetsuya, Rugman-Jones, Paul F., Kado, Natsuko, Sawamura, Nobuo & Narai, Yutaka, 2020, Egg parasitoids of Arboridia apicalis (Nawa, 1913) (Hemiptera, Cicadellidae), a leafhopper pest of grapevines in Japan, with description of a new species of Anagrus Haliday, 1833 (Hymenoptera, Mymaridae), ZooKeys 945, pp. 129-152 : 129

Anagrus (Anagrus) arboridiae Triapitsyn & Adachi-Hagimori sp. nov. Figures 2 , 3 , 4

Type material.

Holotype ♀ (Fig. 3a, b, d ), deposited in ELKU, on slide (Fig. 3c ) labeled: 1. "Japan: Honshu Island Shimane Prefecture, Unnan Oku-Izumo vineyard, 35°17'20"N, 132°55'46"E, 155 m (organic Black Olympia table grapes heavily infested with Arboridia apicalis (Nawa) in a covered vineyard), leaves collected 4.x.2019, N. Kado, N. Sawamura, T. Adachi-Hagimori, S. V. Triapitsyn Emerged 6.x.2019, S. V. Triapitsyn"; 2. [magenta] " Anagrus (Anagrus) arboridiae Triapitsyn & Adachi-Hagimori HOLOTYPE ♀"; 3. "Det. by S. V. Triapitsyn 2019"; 4. [barcode database label/unique identifier] " UCRC [bold] UCRC_ENT 005517345".

Paratypes. Japan: Honshu Island, Shimane Prefecture, Unnan, Oku-Izumo vineyard, 35°17'20"N, 132°55'46"E, 155 m (organic Black Olympia table grapes heavily infested with A. apicalis in a covered vineyard), collected 4.x.2019, N. Kado, N. Sawamura, T. Adachi-Hagimori, S. V. Triapitsyn, emerged from grape leaves: 5.x.2019, S. V. Triapitsyn [4 ♀♀, 6 ♂♂, ELKU, UCRC: 2 ♀♀, 5 ♂♂ on points and 2 ♀♀, 1 ♂ on slides (including 1 ♀ on slide, P. F. Rugman-Jones’ molecular voucher PR19-504, UCRC_ENT 005517353)]; 6.x.2019, S. V. Triapitsyn [15 ♀♀, 10 ♂♂, CNC, ELKU, UCRC: 8 ♀♀, 6 ♂♂ on points and 7 ♀♀, 4 ♂♂ on slides (including 1 ♀ on slide, P. F. Rugman-Jones’ molecular voucher PR19-503, UCRC_ENT 005517352)]. Kyushu Island, Miyazaki Prefecture, Higashimorokata, Aya, Kitamata, 32°00'32"N, 131°14'26"E, 86 m (Katsuki Wines LLC organic vineyard, Chardonnay wine grapes lightly infested with A. apicalis in a covered vineyard), leaves collected 30.x.2019, T. Adachi-Hagimori, S. V. Triapitsyn, emerged 6.xi.2019, S. V. Triapitsyn [1 ♀, 1 ♂ on slides, UCRC].

Other (non-type) material examined. Japan: Honshu Island, Shimane Prefecture, Unnan, Oku-Izumo vineyard, 35°17'20"N, 132°55'46"E, 155 m (organic Black Olympia table grapes heavily infested with A. apicalis in a covered vineyard), collected 4.x.2019, N. Kado, N. Sawamura, T. Adachi-Hagimori, S. V. Triapitsyn: sweeping on vines [1 ♀]; emerged from grape leaves: 5.x.2019, S. V. Triapitsyn [10 ♀♀, 10 ♂♂]; 6.x.2019, S. V. Triapitsyn [27 ♀♀, 22 ♂♂]; 7.x.2019, N. Kado [35 ♀♀, 29 ♂♂]; 8.x.2019, N. Kado [27 ♀♀, 18 ♂♂]; 9.x.2019, N. Kado [24 ♀♀, 12 ♂♂]; 10.x.2019, N. Kado [6 ♀♀, 6 ♂♂]; 11.x.2019, N. Kado [12 ♀♀, 7 ♂♂]; 13.x.2019, N. Kado [7 ♀♀]; 15.x.2019, N. Kado [1 ♀♀, 3 ♂♂]. Kyushu Island, Miyazaki Prefecture, Higashimorokata, Aya, Kitamata, 32°00'32"N, 131°14'26"E, 86 m (Katsuki Wines LLC organic vineyard, Chardonnay wine grapes lightly infested with A. apicalis in a covered vineyard), leaves collected 30.x.2019, T. Adachi-Hagimori, S. V. Triapitsyn: emerged 31.x.2019, S. V. Triapitsyn [1 ♂]; emerged 2.xi.2019, T. Adachi-Hagimori [1 ♂]; emerged 4.xi.2019, T. Adachi-Hagimori [2 ♀♀]; emerged 2.xi.2019, T. Adachi-Hagimori [1 ♂]; emerged 5.xi.2019, S. V. Triapitsyn [1 ♀]. All in 80% ethanol in a freezer [UCRC].

Diagnosis.

The new species is a member of the atomus species group of Anagrus (Anagrus) as defined by Chiappini et al. (1996). Female antenna (Fig. 3a ) with mps on F3 (1), F4 (1), F5 (1 or 2), F6 (2), and clava (3); midlobe of mesoscutum without adnotaular setae; fore wing disc with a distinct subapical bare area (Figs 3b , 4b ); ovipositor (Fig. 3d ) 2.3-2.5 × length of protibia. Male genitalia (Fig. 4c ) with hooked digiti.

Morphologically, A. arboridiae is most similar to A. flaviapex , to which its female specimens with a more or less distinct bare area on the fore wing disc key in Triapitsyn (2015) and Li et al. (2018). Both taxa have one mps on F3 of the female antenna ( Chiappini and Lin 1998). However, male genitalia of A. flaviapex have cone-shaped, straight digiti ( Triapitsyn 1999) and body of the female is mostly brown ( Triapitsyn 2015). Besides A. arboridiae , the three other known species within the nominate subgenus of Anagrus with hooked digiti of male genitalia and three mps on the clava of female antenna, the European A. vilis Donev and the Afrotropical A. scassellatii Paoli and A. sensillatus Viggiani & Jesu ( Chiappini and Mazzoni 2000), were assigned to the atomus species group by them and also by Triapitsyn (2015). More recently, Nugnes et al. (2017) placed these, without providing much of a justification and based solely on the hooked shape of the digiti of male genitalia, in a separate vilis species group of Anagrus (Anagrus) . However, based on other morphological features of both sexes A. arboridiae is not related to A. vilis and either of them are not related to the two aforementioned Afrotropical species. Moreover, in males of A. japonicus from Okinawa Island, shape of the digiti is of an intermediate state between the strongly hooked (such as in A. arboridiae and A. vilis ) and the straight ones (like in most other species within the atomus species group): these are more or less cone-shaped in dorsoventral view but notably curved in lateral view (Adachi-Hagimori et al. unpublished). Because the hooked shape of the digiti is likely to have evolved independently in the different lineages within the atomus species group sensu lato, we agree with the conclusion made by Chiappini and Mazzoni (2000) that by itself this feature should not be used for defining separate species groups without support of any additional characters. Thus, we do not recognize the vilis species group proposed by Nugnes et al. (2017) as a separate entity from the atomus species group.

Females of A. arboridiae are also similar to those A. japonicus that sometimes have an mps on F3, but the former always have distinct light brown and brown patches on the mesoscutum and the basal gastral terga respectively, which the latter species lacks.

An updated key to females of the Japanese species of Anagrus is provided below, as the latest key by Triapitsyn et al. (2019a) is already outdated after the addition of four species herein which are new to the fauna of Japan.

Description.

Female (holotype and paratypes). Body length of dry-mounted, critical point-dried paratypes 400-500 µm, and of the slide-mounted paratypes 415-520 µm. Body (Fig. 2a ) and appendages mostly pale yellow except funicle, occiput and almost all of mesoscutum (except posteriorly) light brown, transverse trabecula and stemmaticum dark brown, clava and two basal gastral terga brown; wings almost hyaline (slightly infumate). Antenna (Fig. 3a ) with scape 3.4-4.1 × as long as wide, with cross-ridges, 2.0-2.3 × length of pedicel; F1 at most slightly longer than wide, almost half of pedicel length; F2 usually notably shorter than following funicular segments but occasionally approximately as long as F3 or even slightly longer (when F3 lacks mps), F4 usually slightly longer than F5 but occasionally subequal to F5, F6 the longest funicular segment; mps on F3 (usually one but often none), F4 (one or two); F5 (one), and F6 (two); clava with three rather short mps (just a little longer than half length of clava), 2.7-3.3 × as long as wide, usually slightly longer (but occasionally approximately as long as) than combined length of F5 and F6. Midlobe of mesoscutum without adnotaular setae. Fore wing (Fig. 3b ) 6.1-7.0 × as long as wide, longest marginal seta 2.5-2.6 × maximum wing width; distal macrochaeta ca. 4 × length of proximal macrochaeta; disc with several rows of setae in addition to admarginal rows of setae (single complete row originating behind apex of venation and two or three irregular rows in the broadest part of disc), leaving a distinct subapical bare area at posterior margin. Hind wing (Fig. 3b ) 21-25 × as long as wide, longest marginal seta 7.4-9.0 × maximum wing width; disc mostly bare except for an almost complete row of microtrichia along posterior margin and 1-3 additional microtrichia at apex. Ovipositor (Fig. 3d ) extending anteriorly almost to mesophragma in slide-mounted specimens and at most barely exserted beyond apex of gaster posteriorly (by at most 0.06 × total ovipositor length). Second valvifers (= external plates of ovipositor), e.g., Chiappini et al. (1996), each with 1 seta. Ovipositor 1.9-2.1 × length of protibia (2.05 × in the holotype).

Measurements (µm) of the holotype (as length or length: width). Body: 545; mesosoma 197; gaster 251; ovipositor 212. Antenna: scape 75; pedicel 38; F1 13; F2 27; F3 39; F4 43; F5 42; F6 48; clava 100. Fore wing 463: 74; longest marginal seta 185. Hind wing 424: 20; longest marginal seta 148.

Male (paratypes). Body length of dry-mounted, critical point-dried paratypes 330-460 µm, and of the slide-mounted paratypes 400-520 µm. Body color mainly as in female except most of mesoscutum brown and most of gaster dark brown (light brown basally) (Fig. 2b ); flagellum light brown. Antenna (Fig. 4a ) with scape 2.6-3.2 × as long as wide, F1 usually at least slightly shorter than following flagellomeres but occasionally either much shorter than F2 or approximately as long as F2. Fore wing (Fig. 4b ) 5.9-6.4 × as long as wide. Genitalia (Fig. 4c ) length 86-90 µm; digiti hooked.

Etymology.

This new species is named after the host leafhopper genus.

Distribution.

Palaearctic region: Japan (Honshu and Kyushu Islands).

Host.

Cicadellidae : Arboridia (Arboridia) apicalis (Nawa). Only A. apicalis was present on the grapevines both in Aya, Miyazaki Prefecture and in Unnan, Shimane Prefecture, with any other leafhoppers being absent, so this host association of A. arboridiae is obvious.

Biology.

In the dissected parasitized eggs of A. apicalis in the organic vineyard in Unnan, Shimane Prefecture, A. arboridiae was observed to develop as a solitary endoparasitoid. Other aspects of its biology are unknown and thus would require further investigations.

Remarks.

The following species of Anagrus are newly recorded for the fauna of Japan.

Anagrus (Anagrus) flaviapex : Japan, Ryukyu Islands, Okinawa Prefecture, Okinawa Island, Itoman, Makabe, Okinawa Prefectural Agricultural Research Center (26°06'37.9"N, 129°41'16.1"E, 52 m), okra (organic experimental plot), 15-18.x.2019, S.V. Triapitsyn, T. Adachi-Hagimori, T. Uesato, Malaise trap [1 ♀, UCRC; P. F. Rugman-Jones’ molecular voucher PR19-505, UCRC_ENT 005517351]. This species has an Oriental and Eastern Palaearctic distribution but is known from different leafhopper and possibly also planthopper hosts ( Chiappini and Lin 1998; Triapitsyn 1999, 2015).

The following dry-mounted specimens of Anagrus were found in T. Tachikawa’s collection during the first author’s visit of ELKU in October 2019 and consequently borrowed, some of them slide-mounted, and then identified. They represent new and interesting host associations for the respective taxa:

Anagrus (Anagrus) atomus (L.): Japan, Shikoku Island, Ehime Prefecture, Kihoku, 24.iii.1966, emerged 28.iii.1966 from eggs of Eurhadina? betularia Anufriev (a tentative identification of the host per the original label in Japanese) [4 ♀♀, ELKU];

Anagrus (Anagrus) avalae Soyka: Japan, Honshu Island, Aomori Prefecture, Hirosaki City, vi.1964, R. Tsugawa, from eggs of Edwardsiana ishidae (Matsumura) [13 ♀♀, 4 ♂♂, ELKU].

Figures

Figure 2. Anagrus arboridiae sp. nov. (paratypes from Unnan, Shimane Prefecture, Honshu Island, Japan) a habitus of female (lateral view) b habitus of male (dorsal view).

Figure 3. Anagrus arboridiae sp. nov. female (holotype) a antenna b fore and hind wings c slide d gaster.

Figure 4. Anagrus arboridiae sp. nov. male (paratypes from Unnan, Shimane Prefecture, Honshu Island, Japan) a antenna b fore wing c genitalia (lateral view).