Tetraneura (Tetraneurella) akinire Sasaki, 1904 [Redescription]

Tetraneura akinire Sasaki, 1904
Tetraneura fusiformis Matsumura,1917; Eastop & Blackman 2005
Tetraneura (Tetraneurella) akinire: Hille Ris Lambers, 1970
Tetraneura (Tetraneurella) nigriabdominalis: Hille Ris Lambers, 1970
Tetraneura nigriabdominalis: Eastop & Blackman 2005
See Favret (2021) for other synonymies.

Host plant: Primary host: U. davidiana var. japonica, U. parvifolia, U. carpinifolia, U. rubra, U. minor, U. campestris, U. laciniata, and U. americana. Secondary host: Setaria spp., Eleusine indica and other gramineous species.

Distribution: Almost world-wide (Blackman & Eastop 2021).

Tetraneura nigriabdominalis (Sasaki, 1899) and T. akinire Sasaki, 1904 [Taxonomic history]

An aphid species attacking upland rice was described under the name Schizoneura nigriabdominalis by Chujiro Sasaki (1899), who reported that this species forms large colonies, including apterous adults, in early July on the roots of upland rice in Tokyo. [. . .] Later, Tanaka (1961) transferred this species to Tetraneura, resulting in the combination T. nigriabdominalis. In the revision of Tetraneura by Hille Ris Lambers (1970), T. nigriabdominalis was redescribed with a neotype designated based on a specimen collected from the roots of Oryza sativa in Tochigi Prefecture, Japan. In the revision, Hille Ris Lambers divided this species into four types: first, the gall generation on Ulmus davidiana var. japonica; second, the root generations collected from the roots of upland rice in Japan; third, the root generations collected from grass roots in India and Indonesia; and fourth, the root generations collected from grass roots in Africa and America. Eastop & Blackman (2005) pointed out that all African records of T. nigriabdominalis as well as many of those from Asia should be referred to T. fusiformis, although a Tetraneura species collected on upland rice in East Asia was of the true nigriabdominalis.

Later, Sasaki (1904) described an aphid species that induces galls on the leaves of U. parvifolia under the name T. akinire (“akinire” refers to U. parvifolia in Japanese). The locality is not mentioned, but Tokyo is most likely. The type specimens also considered to be lost. Therefore, nigriabdominalis is a specific epithet of root generation, whereas akinire is for gall generation. [. . .] Tetraneura akinire is currently recognized as a junior synonym of T. nigriabdominalis (Blackman & Eastop 2021; Favret 2021).

Although the name T. nigriabdominalis has been used by many authors for a long time when referring to gall and root generations, the original description has rarely been checked by researchers. In this study, we examined the original description written in Japanese, and concluded that Schizoneura nigriabdominalis Sasaki, 1899 does not belong to Tetraneura, but probably to Anoecia.

Therefore, the name T. akinire Sasaki 1904 was revived for the species that induces galls on U. parvifolia. Tetraneura akinire Sasaki, 1904 is a valid name and a senior synonym of T. fusiformis Matsumura, T. hirsuta (Baker), and T. chinensis Mordvilko. However, it is still unknown whether a Tetraneura species that induces galls on U. davidiana and attacks the roots of upland rice and other gramineous species is T. akinire, and this problem is dealt with in the next section.

Although it is difficult to identify aphid species based on gall morphology, three types of galls remain distinctive in the subgenus Tetraneurella distributed in Japan and South Korea: greenish globular galls (Figure 1A-E), reddish or greenish, spindle-shaped galls (F-I), and reddish small globular galls (J-L). Greenish globular galls and spindle-shaped galls were collected in Japan and South Korea. Morphological observations of emigrant adults and their progeny collected from the three types of galls indicated that greenish globular galls from Japan, spindle-shaped galls, and small-sized globular galls were induced by T. ovaliformis sp. nov., T. akinire sensu novo, and T. sorini, respectively.

Gall formers of spindle-shaped galls (T. akinire) were separated into two clades, both of which were highly supported by bootstrapping (81% and 99%). This result supported the results of Lee et al. (2012), who indicated that T. nigriabdominalis (= T. akinire sensu novo) consisted of two phylogenetic groups (types A and B). In the present study, type A included samples from Japan, Europe, and North America and also included samples from U. parvifolia and U. davidiana var. japonica. This result suggests that members of type A are widely and commonly distributed in Eurasia and are associated with several species of Ulmus without genetic differentiation.

In the phylogeny, no genetic differentiation was detected between American samples (Figure 3, 1-2) and Asian samples (3-6), suggesting that the American T. akinire was introduced from Asia.

Tetraneura nigriabdominalis (Sasaki) (= T. akinire)

Galls are stalked, hairy, elongate, spindle- or pouch-shaped, 15-40 mm high, usually with a pointed apex (fig. 134E), usually bicoloured green and rose-red when mature (see influentialpoints.com). They occur on various Ulmus spp. (canescens, japonica, parvifolia, procera, pumila) in southern and south-east Europe (including Malta – Mifsud et al. 2009), south-west Asia (Iran, Georgia), Kazakhstan (Kadyrbekov 2014e), China, Korea and Japan. It is also in eastern USA on U. minor (Stoetzel 1987, as akinire), and in western USA (California) on U. pumila and hybrid elms (S. Dreistadt, pers.comm.). Galls on Ulmus sp. on high ground in Pakistan (Naumann-Etienne & Remaudière 1995, as akinire) are probably also this species. Alatae (BL 1.4-2.3 mm) (fig. 117E) leave the gall through lateral slits in May-July to found ant-attended colonies on the roots of Poaceae (including Cynodon, Digitaria, Echinochloa, Oryza, Saccharum, Setaria). Apterae on grass roots are greenish‑ or brownish‑white; BL 1.5-2.5 mm. Their presence on the roots of some hosts is indicated by a reddish-purple discoloration of the leaves.

This species is known particularly as a pest of rice (Blackman & Eastop 2000), but many of the references to nigriabdominalis, e.g. in Africa, the Middle East, India and south-east Asia, are referable to T. fusiformis. W. Lee et al. (2012b) distinguished Japanese populations of T. nigriabdominalis (referred to as “Type A” in their paper) from those of T. fusiformis (“Type B”) by their differing mitochondrial COI sequences. Tanaka (1961) studied its host preferences, although he may have had a mixture of T. nigriabdominalis and T. fusiformis. Galli & Bonvicini-Pagliai (1998) studied its relations with ants. Enoki (1986) studied resistance to this aphid in U. japonica. The male genitalia were described and illustrated by Wieczorek (2012). Hille Ris Lambers' (1970b) descriptions of gall generations under this name (his 'Group I material') should be referred to T. fusiformis (Eastop & Blackman 2005). Populations in China were described as a subspecies, T. nigriabdominalis ssp. shanxiensis Zhang & Zhang (as T. akinire ssp.). 2n = 18 (in gall generations); however Galli & Manicardi (1998) reported karyotype variation from 2n =13 to 19.

Galls of both [T. ulmi and T. nigriabdominalis] are stalked and located on the upper side of a leaf. Galls of T. (T.) nigriabdominalis are hairy, elongate or pouch shaped, usually with a pointed apex, whereas the galls formed by T.(T.) ulmi are smooth and shiny and bean shaped(Fig.3). When mature, the galls of T. (T.) nigriabdominalis are usually bicoloured green and rose-red, and those formed by T.(T.) ulmi are reddish-green or yellowish. Galls of both species can co-occur on the same leaf blade(Fig. 3).

Its primary host constitutes different species of Ulmus (e.g. U. canescens Melville, U. davidiana var. japonica Rehder, U. parvifolia Jacq, U. minor Mill., U. pumila L.). Secondary hosts are numerous species of Poaceae family from the genera Agropyron...It is also one of the most important rice pests.