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Research Article
Description of a new species of Aphanogmus Thomson (Hymenoptera, Ceraphronidae) that parasitizes acarivorous gall midges of Feltiella (Diptera, Cecidomyiidae) in Japan
expand article infoKazunori Matsuo, Tomoko Ganaha-Kikumura§, Suguru Ohno§, Junichi Yukawa|
‡ Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University, Fukuoka, Japan
§ Okinawa Prefectural Agricultural Research Center, Okinawa, Japan
| Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka, Japan
Open Access

Abstract

In 2008–2009, we reared small ceraphronids (about 0.5 mm in body length) from cocoons that had been made possibly by two acarivorous species, Feltiella acarisuga (Vallot) and F. acarivora (Zehntner) (Diptera: Cecidomyiidae) in Okinawa, Japan. Detailed morphological observation revealed that the ceraphronid was a new species of Aphanogmus Thomson (Hymenoptera: Ceraphronidae). We describe it as Aphanogmus flavigastris Matsuo, sp. n. Identification of the Aphanogmus species is essential to evaluate its possibly negative effects on the predatory activity of Feltiella species that have been used as control agents against tetranychid mites.

Keywords

Aphanogmus flavigastris, Feltiella acarisuga, Feltiella acarivora, taxonomy

Introduction

In 2008–2009, small (about 0.5 mm in body length) species of ceraphronids (Hymenoptera) were reared from cocoons that had been made possibly by two acarivorous species, Feltiella acarisuga (Vallot) and F. acarivora (Zehntner) (Diptera: Cecidomyiidae) in Okinawa, Japan (Abe et al. 2011, Ganaha-Kikumura et al. 2012). Preliminary identification revealed that the ceraphronid was a member of Aphanogmus Thomson (Hymenoptera: Ceraphronidae), which contains at least 100 species worldwide (Johnson and Musetti 2004, Evans et al. 2005, Buhl et al. 2010). About 20% of them have been known as parasitoids of various insects including Cecidomyiidae (Diptera), Bethylidae, Ichneumonidae (Hymenoptera) and Cybocephalidae (Coleoptera) (Oatman 1985, Gilkeson et al. 1993, Polaszek and Dessart 1996, Evans et al. 2005). Host information for the remaining 80% has not been provided. At present, two species, Aphanogmus floridanus Ashmead and A. fulmeki Szelényi (=A. parvulus Roberti) have been known to parasitize Feltiella species in the Holoarctic region. The former is an endoparasitoid of Feltiella acarivora (Oatman 1985, Johnson and Musetti 2004) and the latter attacks F. acarisuga, F. acarivora, Aphidoletes aphidimyza (Rondani), and Mycodiplosis sp. (Diptera: Cecidomyiidae) (Dessart 1992).

A few taxonomic studies have focused on Japanese species of Aphanogmus. Ashmead (1904) first recorded Aphanogmus from Japan, describing A. hakonensis Ashmead based on individuals collected from Hakone, Kanagawa. Polaszak and Dessart (1996) detected several cryptic species of Aphanogmus hakonensis and proposed the species complex of A. hakonensis. Ishii (1937) reported an unidentified species of Aphanogmus as a parasitoid of Cybocephalus species (Coleoptera: Cybocephalidae) that feed on Unaspis yanonensis (Kuwana) (Hemiptera: Diaspididae) on citrus in Japan. Evans et al. (2005) considered that Aphanogmus sp. reported in Ishii (1937) was identical to A. inamicus Evans and Dessart. In total, two nominal species, Aphanogmus hakonensis and A. inamicus have been known in Japan.

Larvae of all known Feltiella species feed on tetranychid mites (Acari: Tetranychidae) (Gagné 1995, Gagné and Jaschhof 2014). In particular, Feltiella acarisuga is regarded as an important natural enemy against tetranychid mites that frequently develop pesticide resistance and cause serious damage to various agricultural products (Barnes 1933, Wardlow and Tobin 1990). Therefore, the purpose of this study is to identify the Aphanogmus found in Okinawa, as this is essential to evaluate its effect on mortality of Feltiella species.

Material and methods

We collected more than one larva or cocoon of Feltiella from each collecting site in Okinawa, Japan in 2008–2009. They were kept in petri-dishes to rear Aphanogmus and Feltiella species. Adults that emerged were preserved in 75% ethanol for morphological observation. If possible, host species of parasitoid wasp should be identified by examining remnants of host insect but the male genitalia of host cecidomyiid, which is important for species identification, would not be included in the remnants. Otherwise, host species should be identified before the attack of parasitoid wasps. However, this is not always applicable under natural conditions. Therefore, we regarded host cecidomyiid to be identical to either F. acarisuga or F. acarivora when A. flavigastris emerged from cocoons that coexisted on the same plant with either F. acarisuga or F. acarivora, respectively because we have seldom seen F. acarisuga and F. acarivora on the same plant.

For microscopic study, the ethanol-stored specimens were dried by the method described in Matsuo and Yukawa (2009). Fore wings were mounted on slides in Canada balsam using ethanol and xylene. Several specimens were gold-coated for microphotography with a JEOL JSM-5600LV scanning electronic microscope. High resolution image was taken with the methods described in Matsuo et al. (2012). Adult morphological terminology follows Mikó and Deans (2009), except for wing venation, which follows Dessart (1963). The holotype and paratypes are deposited in the collection of the Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University, Japan.

Results and discussion

Aphanogmus flavigastris Matsuo, sp. n.

Ceraphronidae sp.: Abe et al. 2011: 277.

Ceraphronidae sp.: Ganaha-Kikumura et al. 2012: 323.

Etymology

The specific name, flavigastris, is Latin meaning yellowish gaster, derived from the color of the female metasoma.

Type material

See Table 1.

A list of type specimens of Aphanogmus flavigastris. All specimens are kept in the collection of the Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University, Japan.

Possible host Associated plant* Collecting site (collector**) Host collecting No. specimens Notes
F. acarisuga Pueraria montana Senbaru, Nishihara, Okinawa, Japan (SO) 22 vii 2008 1 female Holotype
F. acarisuga P. montana Senbaru, Nishihara, Okinawa, Japan (SO) 22 vii 2008 1 male Paratype
F. acarisuga Mallotus japonicus Uka, Kunigami, Okinawa, Japan (SO, TGK) 1 viii 2008 1 female Paratype
F. acarisuga Ma. japonicus Uehara, Ogimi, Okinawa, Japan (SO, TGK) 6 viii 2008 1 female Paratype
F. acarisuga Broussonetia papyrifera Gesashi, Higashi, Okinawa, Japan (SO) 21 ii 2009 1 female Paratype
F. acarivora Bauhinia variegata Senbaru, Nishihara, Okinawa, Japan (SO) 18 vii 2008 2 females Paratypes
F. acarivora Melanolepis multiglandulosa Hentona, Kunigami, Okinawa, Japan (SO) 31 vii 2008 2 males Paratypes
F. acarivora Mucuna macrocarpa Oku, Kunigami, Okinawa, Japan (SO, TGK) 1 viii 2008 2 females Paratypes
F. acarivora P. montana Iramina, Yomitan, Okinawa, Japan (SO) 2 x 2008 1 female Paratype
F. acarivora Morus australis Kijoka, Ogimi, Okinawa, Japan (SO) 16 x 2008 1 female Paratype

Description

FEMALE. Body length 0.5–0.6 mm (Figs 1, 2). Head dark brown. Scape yellow; pedicel and all flagellomeres yellowish brown. Mesosoma dark brown. Fore wing with an infuscate area. Fore and mid coxae dark brown, sometimes yellowish in apical half; fore and mid femora yellow, sometimes brownish; hind leg and all tibiae yellow. Metasoma yellow, darker dorsally.

Figure 1.

A female of Aphanogmus flavigastris. Scale bar: 100 μm.

Figures 2–5.

Aphanogmus flavigastris. 2 female body, lateral view 3 female head, frontal view; 4 female antenna, lateral view 5 female mesosoma and metasoma, dorsal view. Scale bars: 2: 100 μm; 3–5: 50 μm.

Head in dorsal view 1.5–1.7 times as wide as long, 1.2–1.4 times as wide as mesosoma; POL: OOL: LOL = 1.8: 1.5: 1.0. Head in frontal view (Fig. 3) 1.0–1.1 times as wide as high; malar space 0.3–0.5 times as long as eye height; lateral margin of torulus distinctly raised; intertorular carina distinct; frontal depression transversely reticulate; ocellar foveae absent; preocellar pit absent; facial pit absent; preoccipital furrow present and extends from anterior ocellus to occipital foramen; preoccipital carina absent; preoccipital lunula absent; occipital carina present; occipital depression absent; occiput smooth. Antenna (Fig. 4) 10 segmented; scape about 0.6 times as long as height of head, as long as distance between inner orbits; pedicel 2.0–2.5 times as long as flagellomere 1; the following segments gradually widened; flagellomere 7 about 2.0 times as wide as flagellomere 1; club 1 segmented.

Mesosoma 1.2–1.4 times as long as wide; 1.3–1.5 times as high as wide; ventral pronotal pit distinct; mesoscutum reticulate, sparsely setose (Fig. 5); setal base slightly pustulate; median mesoscutal sulcus complete; notaulus absent; parapsidal line absent; interaxillar sulcus present; scutoscutellar sulcus angled medially, foveolate, continuous with interaxillar sulcus; dorsal axillar area and mesoscutellum sculptured as mesoscutum, with distinct lateral carina which connects posterior mesoscutellar sulcus (Fig. 6); mesoscutellum 1.4–1.6 times as long as wide; anterior mesopleural sulcus distinct (Fig. 7); anterior mesopleural area finely reticulate with several setae; dorsal mesometapleural carina straight; anterior mesopleural sulcus perpendicularly intersecting dorsal mesometapleural carina; metapleural carina distinct, extends near dorsal mesometapleural carina.

Figures 6–9.

Aphanogmus flavigastris. 6 female scutellum, antero-dorsal view 7 female mesosoma, lateral view 8 female fore wing, upper surface 9 male antenna, lateral view. Scale bars: 6: 20 μm; 7: 50 μm; 8, 9: 100 μm.

Fore wing about 3.0 times as long as wide, with a darkly pigmented band (Fig. 8); radial vein 1.4–1.5 times as long as marginal vein. Metacoxa bare dorsally; longitudinal metacoxal carina present at base.

Syntergum with distinct transverse carina anteriorly, smooth, with 2–3 setae anterolaterally, occupying more than half of total length of metasoma; longitudinal striae of syntergum absent.

MALE. Differs from female as follows: Antenna (Fig. 9) 11 segmented; flagellar setae long, about 2.0 times width of flagellomeres.

Distribution

Japan.

Host insects

Feltiella acarisuga and F. acarivora. Usually one, occasionally two or three adults emerged from a single host cocoon.

Diagnosis

Evans et al. (2005) proposed the following three species groups based on characteristics of the 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.

According to the morphological features of these species groups, the new species belongs to the fumipennis group, while Aphanogmus fulmeki and A. floridanus that have been known as parasitoids of Feltiella species belong to the clavicornis group and tenuicornis group, respectively. Therefore, the new species can be distinguished from Aphanogmus fulmeki and A. floridanus.

Among members of the fumipennis group, the new species shares the following characteristics with species in the Aphanogmus hakonensis complex sensu Polaszak and Dessart (1996): median mesoscutal sulcus present; dorsal axillar area and mesoscutellum with distinct lateral carina; syntergum with distinct transverse carina anteriorly. However, Aphanogmus flavigastris does not belong to the A. hakonensis complex based on the following characters: fore wing with a darkly pigmented band (hyaline in A. hakonensis complex); antenna of female with flagellomere 2–7 not transverse (transverse in A. hakonensis complex).

The new species is most similar to Aphanogmus inamicus as it shares the following characters: median mesoscutal sulcus present; dorsal axillar area and mesoscutellum with distinct lateral carina; syntergum with distinct transverse carina anteriorly; fore wing with a darkly pigmented band; antenna of female with flagellomere 2–7 not transverse. However, Aphanogmus flavigastris can be distinguished from A. inamicus by the following characters: club of antenna 1 segmented (3 segmented in A. inamicus); lateral carina on dorsal axillar area and mesoscutellum more raised than that of A. inamicus; longitudinal striae of syntergum absent (present in A. inamicus); mesosoma dark brown (reddish yellow in A. inamicus); infuscate area on fore wing smaller (from marginal vein to posterior margin of fore wing in A. inamicus).

According to a key to the Palaearctic species of Aphanogmus (Szelényi 1940), the new species runs to A. fasciolatus Förster based on the following characters: antenna clavate; club 1 segmented and longer than the preceding two segments combined; radial vein longer than marginal vein. However, the new species could be distinguished from Aphanogmus fasciolatus by having longer pedicel that is distinctly longer than flagellomere 1 while A. fasciolatus has the pedicel that is shorter than flagellomere 1.

We need to monitor the seasonal abundance of Aphanogmus flavigastris for the successful application of Feltiella species, because its congener A. floridanus that attacks F. acarivora has been regarded to act as a negative force in controlling Tetranychus urticae Koch (Acari: Tetranychidae) on strawberry in California (Oatman 1985). Shimoda et al. (2016) recently developed a remarkable system for trapping Feltiella species and other predators of spider mites using pots of Brassica rapa Linnaeus var. perviridis L.H.Bailey (Brassicaceae), ‘komatsuna’ in Japanese, which bore Tetranychus urticae. They could rear an unidentified species of Aphanogmus from Feltiella acarisuga with the trapping system. This method may be useful to collect plenty of individuals of Feltiella and its parasitoids from ‘komatsuna’ in the fields. Further field surveys are needed to verify the efficacy of this method as a monitoring tool for Aphanogmus flavigastris.

Acknowledgements

We thank Prof. Y. Abe and Dr. T. Ide for their support in taking SEM images. This study was supported partly by Global COE Program (Center of excellence for Asian conservation ecology as a basis of human-nature mutualism), MEXT, Japan to KM.

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