Rediscovery of Achipteria setulosa, with remarks on Japanese species of Achipteriidae and the proposal of species-groups (Acari, Oribatida)

Abstract The first detailed description of adults of Achipteria setulosa Golosova, 1981 with illustrations are provided, based on materials from central Japan. This species is placed in the subgenus Achipteria (Izuachipteria) Balogh & Mahunka, 1979. In addition, the species grouping of the known species in the genus Achipteria is briefly discussed, and three species-groups are proposed based on the structure of the lamellar complex. Furthermore, data on distribution, diversity and habitat ecology of all known species of Achipteriidae in Japan are presented, and a key is provided for the identification of recorded species in this country. The majority of achipteriid species found in Japan are known to be widely distributed in the vast areas of the northern hemisphere; only two species have restricted distributions in Japan. Most species of Achipteriidae in Japan are inhabitants of the litter of various forests, such as natural broad-leaved forests in high mountainous areas, soils of grasslands, wetlands and mosses growing on rocks.


Introduction
The oribatid mites belonging to the family Achipteriidae Thor, 1929 occur frequently, even sometimes with high numbers, in forest soils, litters, meadow soils, liverworts, bogs and at edges of lakes with mosses, but rarely found in arboreal habitats. Representatives of this family are diverse in both northern and southern hemispheres, but in the tropics, achipteriid species are mainly found at high elevations, for example, in cloud forest litter. Achipteriid species whose feeding habits have been studied are saprophages and mycophages that apparently feed opportunistically on available resources of fungi, algae and decaying plant material (Root et al. 2007, Seniczak and Seniczak 2007, Lindo et al. 2008, Norton and Behan-Pelletier 2009.
Some species of Achipteriidae are sensitive to environmental changes, including pollutants, and therefore, they may indicate changes in habitats. Several species of this family serve as intermediate hosts of tapeworms of the superfamily Anoplocephalata, which parasitize on wild and domestic animals (Rajski 1959, Denegri 1993, Seniczak and Seniczak 2007. The family is known from the Holarctic, Oriental and Neotropical regions with most species described from the North America, Europe, Central America and East Asia. Currently, the family Achipteriidae Thor, 1929 includes seven genera, three subgenera, 90 species and four subspecies (Subías 2004(Subías , 2015. Among the genera, Achipteria Berlese, 1885 is largest in terms of species richness, and it includes two subgenera and 35 species (including two subspecies). Most known species belong to the nominotypical subgenus Achipteria (31 species, two subspecies). Balogh and Mahunka (1979) proposed Izuachipteria and Hokkachipteria as new genera based on the character states of interlamellar setae, but Subías (2004) considered these as a subgenus of Achipteria. The main difference between subgenera Achipteria and Izuachipteria is size of interlamellar setae, which are long and thick, extending beyond basis of lamellar cusps in A. (Achipteria), in contrast very short and slender interlamellar setae (or it is completely absent) in A. (Izuachipteria). Only two species have hitherto been grouped into A. (Izuachipteria), namely A. (I.) imperfecta (Suzuki, 1972) and A. (I.) alpestris (Aoki, 1973).
Eleven species of Achipteriidae have been recorded previously from Japan (Aoki 1959, 1961, 1970, 1973, 1976, Suzuki 1972, Fujikawa et al. 1993, Hirauchi and Aoki 1997, Maruyama 2003, Ohkubo et al. 2015. The aim of the present work is to redescribe the morphology of a little known species, A. setulosa Golosova, 1981, which is found for the first time in Japan. This species has character states of the subgenus Achipteria (Izuachipteria), therefore, we combine this species in the latter subgenus. Proposing the species grouping of the known species of Achipteria sensu lato along with review of the composition of the family Achipteriidae in Japan, with remarks on their biogeography, habitat ecology, and construction of an identification key to all known species from this country are the other goal of this study.
The morphological terminology used below is mostly that developed over many years by Grandjean (1932Grandjean ( , 1952, and also that by Norton (1977), Norton and Behan-Pelletier (2009). The specimens were cleared in lactic acid and mounted on temporary slides to view the anterior, lateral and posterior aspects and then preserved in alcohol. A differential interference contrast microscope (Olympus BH 2) was used for investigation in transmitted light. Line drawings were made using a camera lucida attached to the compound microscope.
All measurements are given as a range, with the mean in parentheses. Body length was measured in lateral view, from the tip of the rostrum to the posterior edge of the ventral plate, to avoid discrepancies caused by different degrees of notogastral distension. Notogastral length was also measured in lateral aspect (when the dorsosejugal groove is discernable), from the anterior to the posterior edge; notogastral width refers to the maximum width in dorsal aspect. Setal formulas of the legs (including famulus) are given as numbers per segment for appendages (from trochanter to tarsus) and formulas of solenidia are given separately as number per podosomal segment. Diagnosis. Large species, body length: 718-796 μm; width: 480-576 μm (n = 10). Lamellar setae short, thin, smooth, inserted ventrally on cusps, not reaching tip of cusps; interlamellar setae short, thin, smooth, not reaching basis of lamellar cusps; sensilli long, club-shaped, epimeral regions III and IV with three setae each.
Legs (Fig. 2): Lateral claws thinner than middle one, having small, but distinct serrations on dorsal edge (Fig. 2G). Setation of legs typical for genus, most setae finely barbed except few distal or ventral setae on tarsi, femora and trochanters. Solenidia φ 1 on tibiae I about 2.8 times as long as φ 2 ; setae l" on genua I and II markedly thick; setae s on tarsi II very thick, bearing several strong branches; genua IV curved, markedly longer than others. Formula of setation, including famuli: I (1-5-3-4-20), II (1-5-3-4-  Table 1. Remarks. The character states of the specimens examined here accord well with those studied by Golosova (1981). Only the slight differences are the scarcely barbed sensilli in the Russian specimens (smooth in Japanese specimens), and number of epimeral setae (Russian specimens has fewer setae than Japanese ones). Until now, the present species was known only from the type locality, Kuril Islands in the Russian Far East. The original description, illustration and differential diagnosis of this species were not sufficient, and hence we present here some supplementary details.
Achipteria (I.) setulosa resembles the two other Japanese species, A. (I.) alpestris and A. (I.) imperfecta in having short and slender interlamellar setae. However, A. (I.) alpestris is different from Achipteria (I.) setulosa by the strongly-developed median horn-like projection of the rostrum, the relatively shorter sensilli, and much smaller body size. Another Japanese species, A. (I.) imperfecta has no interlamellar setae, relatively thick sensilli, different dentation of lamellar cusps, and much smaller body size.

Discussion
In the comprehensive checklist of oribatid mites of Japan, Fujikawa et al. (1993) presented eight species of Achipteriidae belonging to five genera, namely Achipteria, Anachipteria, Parachipteria, Hokkachipteria and Izuachipteria, but the two latter taxa are now considered as subgenera of Achipteria.
Most of achipteriid species found in Japan are known to be widely distributed in vast areas of the northern hemisphere. Thus, Achipteria coleoptrata (Linnaeus, 1758), A. curta Aoki, 1970, A. nitens (Nicolet, 1855, Anachipteria achipteroides (Ewing, 1913) and Parachipteria punctata (Nicolet, 1855) are widely distributed through Holarctic region. Some of these species were also recorded from the other biogeographic regions, e.g. in addition to their common distributions in Europe (everywhere), North America (USA and Canada), and Asia (Russian Far East, Siberia, Kazakhstan, Mongolia and Japan), A. coleoptrata, A. curta and P. punctata were reported from India, Table 1. Homology of leg setation and solenidia of Achipteria (Izuachipteria) setulosa (Golosova, 1981)* Vietnam, subtropical part of China and Santa Helena islands (Wallwork 1977, Haq and Sumangala 2003, Wang et al. 2003, Chen et al. 2010. Two other species, such as Anachipteria grandis Aoki, 1966 and Parachipteria distincta (Aoki, 1959) (Aoki 1991, Ryabinin and Pan'kov 2002, Ohkubo et al. 2015, Subías 2015. Among these species, P. distincta is most common species in Japan, which is ubiquitous in this country. Some other species, such as A. curta, A. (I.) alpestris, A. (I.) imperfecta and An. grandis are rather common, especially in its northern and central regions of the country. The other species (A. coleoptrata, A. nitens, A. serrata, An. achipteroides, P. truncata, P. punctata) are relatively rare, and known to be distributed only in one prefecture each. Most species of Achipteriidae in Japan are the inhabitants of the litter of various forests, such as natural broad leaved forests in high mountainous areas, soils of grasslands, wetlands and mosses growing on rocks.

Legs Trochanter Femur Genu Tibia Tarsus
As mentioned above, Achipteria sensu lato is the largest genus of Achipteriidae, and it encompasses diverse species in terms of morphological characters. Balogh and Mahunka (1979) attempted to classify species of Achipteria using the size of the interlamellar setae, but this proposal was not broadly accepted. In this sense, validity of the subgenus Achipteria (Izuachipteria) might not acceptable, but further detailed studies are required on the morphology of both adults and immature stages to clarify the status of this subgenus, which is beyond the scope of the present work.
The structure of lamellar complex is quite diverse in various species of Achipteria, e.g. some species have anteriorly narrowed, elongate triangular lamellae pointed distally with sharp lateral cusps, which is a typical lamellar complex for Achipteriidae and an apomorphic character, according to Weigmann (2010). The other species have very broad lamellae distally with large cusps, which is a plesiomorphic character, according to the above-mentioned author. In case of the latter lamellar complex, the distal ends of lamellar cusps are mostly bent downwards, but in various species, these bending cusps are being either dentate or evenly rounded distally. Based on these different characters, it might be possible to establish at least two subgenera within the genus Achipteria. However, we do not do so, because of the below given reason.
As stated by Weigmann (2010) there are many genera of oribatid mites, creation of which were based upon single conspicuous character or some combination of characters, whose value for assessing phylogenetic relations is questionable. Moreover, Behan-Pelletier (2001) and Lindo et al. (2008) declared that the shapes of the lamellae vary extensively not only within the family Achipteriidae, but even among different families of poronotic Brachypylina, and the polarity of these variations is unclear. They justified that proposing a separate generic taxon based on character of the lamellae is not appropriate.
Although it is not preferable to establish new subgeneric level taxa based on the characters of lamellar complex, it is suggested to classify the known species of Achipteria into three species-groups. The first species-group, which we call the coleoptrata-group, has lamellar complex with anteriorly narrowed, elongate triangular lamellae pointed distally with sharp lateral cusps, but without medial cusps. Besides the type species, A. coleoptrata, this species-group includes such species as A. bicarinata Moskacheva, 1973, A. borealis (Banks, 1889, A. cucullata Moskacheva, 1973, A. elegans Schweizer, 1956, A. holomonensis Cancela da Fonseca & Stamou, 1987, A. italica (Oudemans, 1914, A. oregonensis Ewing, 1918, A. quadridentata (Willmann, 1951) and A. sumatrensis Willmann, 1931 The second species-group, the serrata-group, has very broad lamellar complex, and the cusps are distally serrated with various dens or teeth. Achipteria serrata has strong serration on the distal end of lamellar cusps, and some other species with same character could be included in this group, e.g. A. (I.) alpestris, A. curta, A. (I.) setulosa and A. catskllensis Nevin, 1977. The third group, the nitens-group, has similar structures of the lamellar complex to the serrata-group, but the distal end of lamellar cusps are not serrated, i.e. bluntly rounded or sometimes with pointed lateral tooth. This species-group includes A. baleensis Ermilov, Rybalov & Kemal, 2011, A. clarencei Nevin, 1977, A. hasticeps (Hull, 1914, A. (I.) imperfecta, A. nitens (Nicolet, 1855), A. longesensillus Schweizer, 1956, A. longisetosa Weigmann & Murvanidze, 2003and A. verrucosa Rjabinin, 1974 This grouping might be useful for further classification of Achipteria species, and it should mentioned here that we do not include some hitherto known species of Achipteria (e.g. A. armata (Banks, 1895), A. hasticeps (Hull, 1914), A. languida (Nicolet, 1855), A. minuta (Ewing, 1909), A. moderatior Berlese, 1923 into any speciesgroup, due to their unclear diagnostic characters.
It is evident that the large lamellar complex is for protecting the dorsal, lateral and anterior parts of the prodorsum and especially the anterior legs in redrawn position, but in some species of Achipteria the lamellar complex became distinctly smaller; the structure and function of different lamellar complexes are the interesting topics of the future studies.
In conclusion, the following key can be used to identify the adults of all known species of Achipteriidae in Japan.
A key to adults of known species of Achipteriidae in Japan  Aoki, 1976