Japanese Tetramorium queens: identification key and species diagnoses (Hymenoptera, Formicidae, Myrmicinae)

In Japan, nine species have been known in the ant genus Tetramorium, of which five or more are considered tramps. A key to the queens of nine Tetramorium species found in Japan is presented. The tramp species T. tonganum Mayr, 1870 is excluded from the key because no queen was available for us, while T. pacificum Mayr, 1870 is included because it was once intercepted at a port in Japan and exotic queens were available. Diagnosis of the queen of each species is provided together with differences between the two female castes. Tetramorium tanakai Bolton, 1977 is resurrected from synonymy with T. kraepelini Forel, 1905 based mainly on the queen characters.


Introduction
Tetramorium Mayr, 1855 is a large ant genus containing slightly less than 600 species worldwide, with very few native species in the New World (AntWiki 2021). Most species are found in tropical and subtropical regions of Africa, Madagascar and Asia (e.g. Bolton 1977Bolton , 1980Hita Garcia and Fisher 2012;Agavekar et al. 2017), though one group, the T. caespitum (Linnaeus, 1758) complex, has developed into more than ten species in northern Eurasia (e.g. Steiner et al. 2006). Some species are common, encountered during most field surveys on ant species diversity and some others are tramps spreading over non-native areas. In spite of their ubiquity, the nesting biology of Tetramorium species has not been studied well and many species are known only from the worker caste. In Japan nine species have been recorded, of which at least five are considered tramps or aliens (Terayama 2020;Yoshimura 2020). Although Tetramorium tanakai Bolton, 1977was synonymized with T. kraepelini Forel, 1905by Japan Ant Database Group (2003, it is highly probable that it is a good species and it is resurrected from synonymy in the present paper. Species accounts for the known Tetramorium fauna of Japan are given by Terayama et al. (2014), based on the worker caste, but information about the queen and male is still very poor even for common species. The present paper is the first attempt to provide an identification key and morphological accounts for all the known Japanese species of the genus, except for T. tonganum Mayr, 1870. We include T. pacificum Mayr, 1870 that was once intercepted at a ferry port in Honshu. This paper is the second part of 'the queens of the Japanese ants' series; the first part dealt with the genus Pheidole (Yamane and Hosoishi 2020).

Materials and methods
We tried to use queen specimens associated with workers, i.e. from colony series, for each species. Although we could examine only one queen for T. cf. kraepelini Forel, 1905, sampled by general collection, we identified it as T. cf. kraepelini, based on the key characters of the T. kraepelini species-complex, colouration and distribution information in Japan. As no queen of T. tonganum, either from Japan or outside Japan, was available, accordingly it has been omitted from the key. In the case of T. pacificum, not established yet in Japan, queens collected in Southeast Asia are used for the key and description. Specimens examined are deposited in the Entomological Laboratory, Kyushu University (KUEC: Fukuoka, Japan) and Seiki Yamane Collection (SKYC: Kitakyushu, Japan).
Measurements TBL: total body length roughly measured from anterior margin of head to tip of gaster; HL: maximum head length (in full-face view in a straight line from mid-point of anterior clypeal margin to mid-point of a transverse line spanning apices of projecting posteriormost portions of head); HW: maximum head width excluding eyes; SL: length of antennal scape; EL: maximum eye length (major diameter); EW: maxi-mum eye width (minor diameter); PtW: maximum petiolar width; PptW: maximum postpetiole width; CI: cephalic index (HW divided by HL × 100); SI: scape index (SL divided by HW × 100); ELI: eye length index (EL divided by head length × 100). All measurements are expressed in mm.

Queen characters
The queens of the Japanese Tetramorium species, except for T. tonganum (queen not available) have the following character conditions in common: i) large eyes, ii) complete set of ocelli present, iii) full wings present (not confirmed in T. cf. kraepelini but distinct scars are seen at position of wing bases), iv) pronotum demarcated from mesonotum with distinct suture, v) mesonotum divided into mesoscutum and mesoscutellum, vi) notaulix absent, vii) mesopleuron divided into upper and lower portions, viii) distinctly defined metanotum and ix) metapleuron only weakly demarcated from lateral face of propodeum. In all Japanese species, the propodeal spine is moderate to well-developed and often stouter than in the worker. Ogata (1991) also provided a useful diagnosis for the queen caste of the Japanese species, but the species examined was not mentioned.
Amongst the Japanese myrmicine queens, Tetramorium queens are easily recognised by the following combination of the conditions: i) antennal club 3-segmented, ii) masticatory margin of mandible generally with seven teeth, iii) lateral portion of clypeus raised into sharp ridge that constitutes part of wall defining antennal insertion and iv) mid-and hind-tibiae each apically with simple spur. Important queen characters for identification of the Japanese Tetramorium species are listed below. Character conditions for the T. tonganum queen are cited from Bharti and Kumar (2012).
Head shape. Much broader than long: T. tsushimae Emery, 1925. Longer than broad or rarely almost as long as broad: other species.
1 Basal 1/6-1/3 of gastral tergite 1 (abdominal tergite 4) with fine longitudinal striae ( Fig. 1f ) or micropunctures that are sometimes superficial; sculptured area mat or weakly shiny (Fig. 1g) . 1c). Body yellowish-brown to brown often with darker gaster (Fig. 2a)  Larger species with total body length 5.5-6 mm. Entire body dark brown to blackish (Fig. 3c). Petiolar node in profile very short (thin), without distinct dorsal face, with rounded apex (Fig. 1e)     Worker much smaller than the queen. Eye smaller; distance between mandibular base and anterior margin of eye longer than major diameter of eye; in the queen, the distance as long as or shorter than major diameter of eye. Mandible more weakly striate and more shiny than in the queen. Entire dorsum of mesosoma puncto-reticulate; in the queen mesonotum longitudinally rugose. Propodeal spine slender and always up-curved apically; in the queen it tends to be more strongly sclerotised, relatively shorter, with broader base than in the worker and apex not distinctly up-curved. Long hairs on antennal scape and mid-and hind-tibiae frequently near suberect; in the queen, these hairs less frequently near-suberect.
Remarks. Tetramorium bicarinatum is an alien tramp species found in disturbed areas in warmer regions of the world except in Africa. It belongs to the T. bicarinatum species group (Bolton 1977) together with T. nipponense in Japan. In the queen this species is most similar to T. nipponense, which inhabits forests, preferring wetter conditions. The possession of 2-3 transverse carinae between the propodeal spines is an important characteristic in distinguishing the two species; in T. nipponense these carinae are lacking or much weaker (at most one distinct carina present). Furthermore, the propodeal spine is straight throughout its length in T. bicarinatum, while it tends to have a slightly up-curved apex in T. nipponense. New queens are attracted to light.
Distribution in Japan. Kyushu and throughout the Nansei Islands (Terayama et al. 2014).
Remarks. Tetramorium cf. kraepelini belongs to the T. scabrosum group (sensu Bolton 1977). The so-called T. kraepelini can be a complex of sibling species. As only one queen was available for examination the variation in structure and sculpture is unknown. One queen from a colony collected from Central Thailand and tentatively identified as T. kraepelini is very similar to the queen examined above; however, the distance between the posterior ocelli is slightly longer than in the Japanese form.  .7). Body yellowish-brown, with gaster much darker. Head almost as long as broad. Frons medially with longitudinal rugae; other portions of head puncto-reticulate. Clypeus irregularly and superficially sculptured and shiny, with median carina. Eye large; distance between anterior eye margin and mandibular base much shorter than half eye length. Pronotum, mesonotum, lateral mesosoma, except for lower portion of mesopleuron and petiolar and postpetiole nodes puncto-reticulate except for lower portion of mesopleuron rather shiny (mesoscutum may have rather distinct longitudinal rugae). Peduncle of petiole smooth and shiny; dorsal face of petiole not defined, smoothly continuous to declivity; subpetiolar process almost missing. Gastral tergite 1 without longitudinal carinae at base. Vertex and mesosoma with many bifid and fewer trifid erect hairs; these hairs much fewer on gastral tergites.  .7). Worker consistently smaller than the queen. Head only slightly longer than broad in the worker. In the worker, dorsum of head rather extensively reticulate, with weak longitudinal rugae, and mesosomal dorsum densely reticulate, completely lacking rugae; in the queen, at least some rugae recognised on mesonotum. Lateral face of mesosoma entirely sculptured; in the queen, lower portion of mesopleuron more or less smooth and shiny. Eye smaller, only slightly longer than distance between anterior eye margin and mandibular base; in the queen, eye distinctly longer than the distance. Bifid hairs denser on gastral tergite 1 than in the queen.
Distribution in Japan. Nansei Islands. The northern limit lies in Kuchinoerabujima and Tanega-shima of the Ôsumi Islands (Yamane and Fukumoto 2017).
Remarks. Tetramorium lanuginosum belongs to the T. obesa species group of the former 'Triglyphothrix Forel, 1890' (Bolton 1976). This group is characterised by the mixture of simple and bifid hairs on the body, with fewer or no trifid hairs. Tetramorium lanuginosum queens have many bifid hairs on the head and mesosoma (very few on gastral tergite 1), but trifid hairs are absent on the gaster and fewer on head and mesosoma. This species is easily distinguished in both the worker and queen by the presence of bifid and trifid hairs on the body, erect hairs on the antennal scape and mid-and hind-tibiae and the petiole without distinction of the dorsum from posterior declivity.
Caste difference. Worker measurements (n = 5): TBL 2.8-3.0 (2.9), HL 0.74-0.79 (0.77), HW 0.63-0.7 (0.66), SL 0.49-0.55 (0.53), EL 0.16-0.18 (0.17), EW 0.12-0.14 (0.13), PtW 0.23-0.26 (0.25), PptW 0.28-0.33 (0.30), CI 84.0-88.6 (86.4), SI 75.4-85.7 (80.2), ELI 24.6-27.3 (25.9). Worker very similar to the queen in coloration, structure and sculpture, with the following differences. Body smaller. Eye smaller, distance between anterior margin of eye and mandibular base slightly longer than major diameter of eye; in the queen, the distance slightly shorter than major diameter of eye. Dorsum of mesosoma entirely coarsely reticulate; in the queen, mesonotum with longitudinal rugae/striae that are dense and often irregular. Lower portion of mesopleuron sculptured and slightly mat; in the queen, lower portion with much weaker sculpture and shiny. Propodeal spine up-curved in apical 1/3; in the queen, the spine tending to be straighter throughout. Petiole tends to be longer than in the queen. Long hairs on antennal scape and mid-and hind-tibiae frequently nearsuberect; in the queen, these hairs less frequently near suberect. Remarks. Tetramorium nipponense belongs to the T. bicarinatum species group (Bolton 1977) together with T. bicarinatum in Japan. The gaster is generally much paler in colour than in the latter. The shape of the petiole that is frequently used to distinguish between these species in the worker caste is not very useful in the queen, though in T. nipponense the petiole tends to be longer and have a weakly convex dorsal face (for further discussion, see Remarks under T. bicarinatum). Queens of this species are frequently attracted to light and also caught with Malaise traps. . Body brown to dark reddish or blackish-brown. Head in full-face view longer than broad, with almost parallel lateral margins. Frons sparsely longitudinally rugose with interspaces superficially sculptured and often shiny; other portions of head puncto-reticulate; antennal scrobe densely but weakly sculptured and rather shiny. Clypeus with three parallel longitudinal carinae; its anterior margin medially impressed but more weakly than in T. bicarinatum and T. nipponense. Mandible very superficially sculptured or almost smooth and shiny. Pronotal dorsum puncto-reticulate; mesonotum with parallel longitudinal rugae that are often wavy or irregular; dorsum and lateral face of propodeum puncto-reticulate or irregularly coarsely sculptured; remaining portions of mesosoma mainly striate to rugose but lower portion of mesopleuron generally smoother and shiny. Petiole in profile long; its node longer than high, with anterior slope gentle and not clearly separable from dorsum and steep posterior slope; petiole and postpetiole both dorsally and laterally distinctly sculptured and mat. Basal 1/3 or more of gastral tergite 1 covered with distinct longitudinal striae. Antennal scape and mid-and hind-tibiae without erect hairs.
Caste difference. Worker measurements (n = 7; 3 specimens intercepted at Kure Port, Japan and 4 from Southeast Asia): TBL 2.9-3.6 (3. Worker very similar to the queen, but with the following characteristics that are different from those of the latter. Body slightly, but constantly larger than in the queen in terms of HL, HL and SL, but eye size smaller than in the latter with ELI 21.3 (worker) vs. 26.7 (queen). Distance between anterior eye margin and mandibular base distinctly longer than major diameter of eye; in the queen, the distance as long as major diameter of eye. Entire dorsum of mesosoma coarsely puncto-reticulate; in the queen mesonotum longitudinally rugose. Mesopleuron entirely with dense minute punctures; in the queen, lower portion of mesopleuron rather smooth and sculpture in upper portion weak.
Specimens examined. No Japanese specimen available. A dealate queen collected in Upper Thompson Nature Park, Singapore on 9.xii.2017 by Sk. Yamane was used for photos (Figs 2e, 4e, 5e).
Distribution in Japan. Not established in Japan.

Remarks.
Tetramorium pacificum belongs to the T. bicarinatum group, in which the anterior margin of the clypeus is notched or impressed at the middle (Bolton 1977). Amongst the species found in Japan, this species is easily distinguished from the others by having a near-smooth mandible and the anterior and dorsal faces of the petiole confluent with a smooth curve. Workers were found in a container at Kure Port, Hyogo-ken, Honshu, transported by a ferry from Zhongshan, China via Hiroshima Port. Up to now, any established population has not yet been confirmed in Japan. Body yellowish-brown, with darker gaster and light brown to yellow legs. Dorsum of head with dense and longitudinal striae that are regular and parallel; interspaces microsculptured and mat. Clypeus with strong median carina; other longitudinal carinae weak, indistinct; anterior margin entire. Distance between anterior eye margin and mandibular base distinctly shorter than major diameter of eye. Dorsum of mesosoma entirely sculptured; pronotum reticulate, with anterolateral corner angulate; entire mesonotum densely with longitudinal striae; in profile lateral face of mesosoma entirely sculptured; upper portion of mesopleuron rugose and lower portion densely punctate (sometimes punctation weak). Propodeum with longitudinally puncto-striate dorsum and transversely puncto-striate declivity, entirely mat, without transverse carinae between propodeal spines; propodeal spine short, apically blunt, only slightly longer than metapleural lobe. Petiolar node anteriorly sharply truncate; petiole and postpetiole entirely sculptured; ventre of petiolar peduncle superficially sculptured and weakly shiny; nodes of both petiole and postpetiole coarsely punctured. Gastral tergite 1 in basal 1/3 densely and minutely punctate or coriaceous, mat or weakly shiny. Antennal scape and mid-and hind-tibiae without erect hairs. Erect body hairs not tapering apicad, apically often truncate or blunt. Worker very similar to the queen, but with the following differences. Body smaller than in the queen. Distance between anterior eye margin and mandibular base as long as or slightly longer than major diameter of eye; in the queen, the distance much shorter than major eye diameter. Mesonotum coarsely rugoso-reticulate, rugae wavy and irregular; in the queen striae fine and regular. Gastral tergite 1 entirely smooth and shiny; in the queen basal area of the tergite micropunctured and mat (sometimes microsculpture very faint and cuticle weakly shiny). Apical truncation of erect hairs on head and mesosoma more distinct; in the queen, erect hairs often not typically truncate.
Distribution in Japan. Nansei Islands, Ogasawara Islands, Volcano Island. Northern limit lies in Kodakara-jima of the Tokara Islands (Yamane and Fukumoto 2017).
Remarks. Tetramorium simillimum belongs to the T. simillimum species group (Bolton 1977). In the queen, it is easily distinguished from other Japanese congeners by the following character conditions: i) dorsum of head with regular longitudinal striae, with interspaces densely sculptured and mat; ii) erect body hairs not sharply pointed apically; iii) petiole anteriorly truncate, with dorsal face clearly separated from anterior slope with sharp angle; iv) basal 1/3 of gastral tergite 1 micropunctate or coriaceous and mat (sometimes weakly shiny). This species is a famous tramp of African origin (Bolton 1977;Yoshimura 2020). . Worker much smaller than the queen. Eye smaller, distance between anterior eye margin and mandibular base as long as or slightly longer than major diameter of eye; in the queen the distance much shorter than major diameter of eye. Eye anteriorly distinctly tapered; in the queen eye anteriorly broadly rounded. Pronotal dorsum rugose except for small area around anterolateral corner reticulate; in the queen pronotal dorsum coarsely reticulate. Mesonotum longitudinally rugose in both castes. Mesopleuron entirely coarsely sculptured; in the queen, sculpture weaker, especially in lower portion.

Tetramorium tanakai
Queen diagnosis. Measurements (n = 1): TBL 2.63, HL 0.66, HW 0.61, SL 0.40, EL 0.19, EW 0.16, PtW 0.30, CI 92.4, SI 65.6, ELI 28.8. Body brown to dark reddishbrown, with gaster very dark. Head reticulate, with frons between clypeus and ocellar region longitudinally rugose. Clypeus with three longitudinal carinae; its anterior margin entire. Posterior ocelli widely separated from each other; distance between them as long as 4.5× ocellar diameter. Dorsum of pronotum and propodeum coarsely reticulate; mesonotum longitudinally rugose (rugae on mesoscutellum irregular); lateral face of pronotum, upper portion of mesopleuron, metapleuron and lateral face of propodeum largely striate/rugose; lower portion and part of upper portion of mesopleuron smooth to very weakly sculptured and shiny; propodeal declivity irregularly sculptured; no transverse carinae between propodeal spines. Petiolar node entirely reticulate; sternite and peduncle microsculptured and mat; postpetiole with smooth area on its dorsum; its lateral face and sternite irregularly sculptured. Gastral tergite entirely smooth and shiny. Antennal scape and mid-and hind-tibiae with many erect hairs. Worker very similar to the queen in structure and sculpture, but differing in the following aspects. Eye smaller, distance between anterior eye margin and mandibular base as long as or slightly longer than major diameter of eye; in the queen the distance much shorter than major diameter of eye. Eye distinctly tapered anteriad; in the queen, eye anteriorly broadly rounded. Mesosomal dorsum entirely coarsely reticulate; mesonotum longitudinally rugose in the queen. Mesopleuron entirely sculptured; sculpture on mesopleuron much weaker especially in lower portion that is extensively smooth and shiny in the queen.
Distribution in Japan. Yaeyama Islands of the Ryukyu Islands (Ishigaki-jima and Yonaguni-jima).
Remarks. Tetramorium tanakai was originally described based on the worker and queen castes collected on Ishigaki-jima, Yaeyama Islands, Japan (Bolton 1977; no queen description provided). The worker is very similar to the Southeast Asian T. kraepelini, but is distinguished from the latter by the bicoloured body (dark brown head and gaster contrasted with lighter mesosoma, waist and legs) and the petiolar dorsum longer than the height of the tergal portion of the petiole (Bolton 1977). The workers sampled from Yonaguni-jima and examined in this study had a nearly entirely dark brown body with yellowish antennae and legs and are clearly different from extensively yellowish-brown workers of T. kraepelini and the Japanese T. cf. kraepelini. The dorsal length of the petiole is variable, generally as long as or slightly longer than the height of the tergal portion. The present study shows that the queen collected from Yonaguni-jima is also similar to that of T. cf. kraepelini in structure and sculpture, but clearly different from the latter in the widely separated posterior ocelli and coarsely reticulate dorsal propodeum as well as much darker body. We also examined queens and workers from two colonies collected in Shuisheliao, Taiwan. These specimens have a more typical bicolorous body and longer petiolar dorsum as in the original description of T. tanakai. The queens have widely separate posterior ocelli as in the queen from Yonaguni-jima. We consider the populations of Ishigaki-jima, Yonaguni-jima and Taiwan all belonging to the same species, T. tanakai. As species delimitation among the T. kraepelini-complex is very confusing, we need to have more colony series from various localities.

Tetramorium tonganum Mayr, 1870
Remarks. This species is a well-known tramp distributed from New Caledonia through the Indo-Australian region to China and Japan and has been introduced to remote islands in the Pacific and Atlantic Oceans (AntWiki 2021). In Japan, it has been recorded from the Ogasawara Islands (Bolton 1977;Terayama et al. 2014). We have no queen specimen of this species from Japan or from any other country. Santschi (1924) described the queen caste, based on a single specimen collected in Samoa. However, this specimen has only one ocellus and, according to his drawing, the eye is located too posteriorly on the head for a queen of Tetramorium. Bharti and Kumar (2012) described  the queen caste of this species, based on material collected from Himachal Pradesh, India. According to their description (text and pictures), the queen of this species is recognised by the following combination of characteristics: i) anterior margin of clypeus entire, ii) no branched hairs present on body, iii) petiole in profile view with rounded anterodorsal and posterodorsal corners, iv) mid-and hind-tibiae without erect hairs, v) smooth lower portion of mesopleuron and vi) entirely smooth first gastral tergite.
Remarks. Tetramorium tsushimae belongs to the T. caespitum species group. In the queen caste this species is easily distinguished from other Japanese congeners by the large and blackish-brown body, broad head, ill-defined antennal scrobe, presence of smooth areas on the mesonotum and very short petiole.

Discussion
This paper is the first attempt to prepare a key to Japanese Tetramorium species, based on the queen and to give morphological diagnoses for them. Material is still very poor; only one or two queens were available for two species, i.e. T. cf. kraepelini and T. tanakai. This shortfall means that the results of this study are tentative, needing further material from colony series.
Nevertheless, we have a strong impression that Tetramorium queens can be sorted into species as for workers. We found some useful characters for identifying queens. For example, in the worker caste, T. bicarinatum is distinguished from T. nipponense mainly based on the relative length of erect hairs along the frontal carina (compared with maximum eye length) and the shape of the petiole. However, these characters are less reliable for the queen. The presence/absence of distinct transverse carinae between propodeal spines is more decisive, and, finally, this character has proved to be also useful for the worker caste (this has not been mentioned by previous authors in- cluding Bolton 1977). Tetramorium tanakai was resurrected from the synonymy with T. kraepelini; the worker characteristics mentioned by Bolton (1977), i.e. bicoloured body with very dark head and gaster and the long petiolar dorsum in T. tanakai, may be important, but in the queen caste, the configuration of the ocelli (very widely separated from each other) is quite distinctive amongst the T. kraepelini-complex. We have only two queens for T. tanakai (and one for the Japanese T. cf. kraepelini) so that our conclusion might remain tentative. However, our view would inspire further research on this difficult group over the entire Asian Region. Ocellar configuration can be a useful character for other Tetramorium species groups in the future when more material is amassed.
As mentioned earlier, there are many other useful queen characters. Some of them overlap with those traditionally used for workers. For example, the pilosity type on the antennal scape and mid-and hind-tibiae is generally common to both the worker and queen castes. On the other hand, the sculpture on the mesonotum in the queen is quite different from that of the worker. In most Japanese species the reticulation in the worker is replaced with longitudinal striae/rugae in the queen. Only in T. lanuginosum queens the rugae are irregular, mixed with reticulae. Rugose mesonotum in the worker caste is seen only in T. smithi. It is unknown which is more ancestral for Tetramorium, reticulation or striation/rugosity. Another difference between the castes is seen in the sculpture type of the mesopleuron; in the queen it tends to be more feebly sculptured than in the worker or nearly smooth in some species.
In conclusion, we think all the Japanese species can be properly identified also in the queen caste. The difficulty is getting males of all species because we have rarely found males in colonies in the field. However, captive colonies can produce winged sexuals through laboratory rearing for a long period. Cooperation between taxonomists and behavioural ecologists is indispensable for obtaining a complete set of material for the taxonomic study of winged ants.