Isotomidae of Japan and the Asiatic part of Russia. I. Folsomia ‘inoculata’ group

Abstract The paper considers blind species of the genus Folsomia having two pairs of macrosetae on both meso- and metathorax and united in so-called ‘inoculata’ group, which is given a new, more laconic definition. Morphological characters important in the group’s taxonomy are discussed and a further division into four subgroups is proposed. Eight new species, i.e., F. amurica Potapov & Kuznetsova, sp. n., F. breviseta Potapov & Kuznetsova, sp. n., F. calcarea Potapov, sp. n., F. imparis Potapov & Hasegawa, sp. n., F. laconica Potapov & Kuznetsova, sp. n., F. tertia Potapov, sp. n., F. trisensilla Potapov, sp. n., and F. tubulata Potapov & Babenko, sp. n., are described. F. hidakana Uchida & Tamura and F. inoculata Stach are redescribed basing on new material, for the latter species the Stach’s individuals were also examined. A key to species of the group is given.


Introduction
The present revision is based on a vast material recently collected by the authors in various parts of the Eastern Palaearctic and older collections kindly provided by our colleagues. All used materials are deposited in the Tottori Prefectural Museum (Japan) and Moscow State Pedagogical University (Russia).
Traditional methods of morphological taxonomy were mainly used. Multi-dimensional scaling was also applied for variability analysis of widespread F. inoculata. Nine metric characters (ratios) were defined for 84 individuals from five large regions of the Palearctic (see the legend to Fig. 89). Metric characters were inferred from body measurements as following ratios: PAO length : inner edge of unguis, PAO length : width of Ant.I, manubrium length: mucro length, dens length: mucro length, dens length: macrosetae length at the end of abdomen, head diagonal : PAO length, macrosetae length at the end of abdomen : mucro length, accp2-s length : accp3-s length (Abd.V), macrosetae length at the end of abdomen : accp3-s length (Abd.V). The correlation index was used to estimate the distance between individuals. Only adults and subadults of a similar size were studied for this analysis, as well as for the species descriptions.

Remarks on Folsomia inoculata group
The group was firstly characterized by three basic characters, i.e., the presence of dorsal macrosetae on Th.II-III, posterior position of medial s-setae on abdominal segments, and the presence of ventral setae on Th.III (Potapov 2001). Now it became clear that there are some important exceptions, namely three species with mid-tergal position of s-setae (breviseta sp. n., calcarea sp. n., and torpeda) and two species without ventral setae on Th.III (breviseta sp. n. and hidakana). Otherwise, all these species are obvious members of the same very characteristic East Asiatic group. This fact forces us to propose a new definition of the group: Folsomia with eyes absent, macrosetae on dorsum (= Md) of each Th. II and III present resulting in 22/333 formula, body shape tubular, head massive, PAO long and slender.
All species of the group also share several ordinary characters: four sublobal hairs on maxillary outer lobe, bifurcate maxillary palp, labral formula 4/5,5,4, not reduced edge of labrum, unguis without lateral or inner teeth, the absence of foil setae at the tip of abdomen. Therefore, we exclude all these characters from the species diagnoses given below.
Folsomia inoculata holds a unique position in the group due to s-pattern on Abd.V, chaetotaxy of furca, and specific appearance (for details see Remarks for the species).

The state of knowledge of the group
We believe that representatives of the 'inoculata' group were previously collected and recorded by other researchers in the eastern areas of Asia. In the associated regional papers (Yosii 1939(Yosii , 1977Tanaka 1970, Lee 1973Kurcheva 1977;Solntseva and Molodova 1979;Suma 1997;Yamauchi and Suma 1999;Furuno et al. 2000; Niijima and Position of s-setae on tergites. The group show a high diversity of position of medial s-setae relatively to p-row -four patterns can be discriminated (Table 1). Three most frequent variants are shown in Figs 1-3.
S-pattern on Abd.IV and V. Position and differentiation of s-setae on Abd.V is one of the keys to understanding of evolution of the genus Folsomia (Potapov and Greenslade 2010). Most species of the 'inoculata' group show '4+1' or weakly differentiated '3+1+1' s-pattern widely distributed in the genus (Fig. 4). Three new species (F. laconica sp. n., F. tertia sp. n., and F. trisensilla sp. n.) loose two s-setae: lateral accp-s in dorsal pair of s-setae on Abd.IV and anterior as-s on Abd.V resulting in a pattern showing in Fig. 6. These three species also loose corner accp-s on Th.II and ms on  Abd.I (Figs 55,58,65). These three s-setae loss (on Th.II, Abd.IV, and Abd.V) is a unique character for the genus: s-formula 33/22224 (instead of common for the genus 43/22235) was known neither in the 'inoculata' group nor in the genus, although similar but not identical reduction is typical of several species of the 'sensibilis' group (33/22225). In the latter case, as-s-setae of Abd.V remain in the set. Another trend is a differentiation of complete terminal set: s-setae of Abd.IV can undergo shortening (Fig. 5). Differentiation of Abd IV-V s-pattern is most marked in F. inoculata (Fig. 7). Front setae on coxa of leg I. Species of the 'tatarica' subgroup, F. inoculata, F. brevisensilla, F. breviseta sp. n., and F. tertia sp. n. have two such setae, F. laconica sp. n., F. trisensilla sp. n., and species of the 'macrochaetosa' subgroup -three, and F. hidakana -four (Fig. 8). This trait probably reflects general number of setae on legs and furca while shows some exceptions.
Setae on ventrum of metathorax. The species of the 'inoculata' group normally have three ventral setae on each side of Th.III, one of which is long and two are short (Fig. 9). Several species have fewer or more variable number of ventral thoracic setae or all these setae are subequal in size (F. inoculata, F. brevisensilla, and all species of the 'tatarica' subgroup). Two species sharply differ from other congeners of the group having no ventral setae on Th.III (F. breviseta sp. n., F. hidakana) (Fig. 10).

Characters of lower taxonomic value
-PAO in all 'inoculata' species is slender, with parallel edges, and more than 1.3 times longer than width of Ant.I (Figs 14,24,62,78) that is probably a sharp characteristic of the group discriminating it from adjoining 'fimetaria' and 'sensibilis' groups. The socalled "inner denticles" along its edges and middle constriction are usually seen in all species in different extend while both characters considerably vary within populations. -All species have three basal ms-setae on Ant.I: one ventral and two dorsal. Two dorsal bms-setae are arranged in a longitudinal line, proximal bms is longer (Figs 14,23,24). The proximal bms usually hardly differs from common setae and herewith should be carefully excluded if calculating common setae on Ant.I. Species of the 'tatarica' subgroup have proximal bms clearly shorter than common setae (Fig. 78) while its length also varies depending on specimens. -The members of 'hidakana', 'macrochaetosa', and 'laconica' subgroups have minute subapical setae on posterior side of dens. The size of the seta varies depending on specimens and often hardly detectable. Small wrinkle in which this seta set in is always visible. Description. Body size from 1.0 (one adult male) to 1.7 mm. Body shape relatively tubular, general appearance not typical of 'inoculata' group due to short macrosetae (Fig. 12). Without ocelli and pigmentation. Cuticle with fine, hexagonal primary granulation ("smooth"). PAO slender and long, middle constriction varies, 'inner denticles' usually well developed, PAO length 1.8-1.9 as long as width of Ant.I and 2.3-2.5 as long as inner unguis length (Fig. 14). Labium complete, guard setae e7 present, three proximal and four basomedian setae. Ventral side of head with 4+4 postlabial setae. Ant.I with 13-15 common setae, two ventral s-setae (s) and three basal micro s-setae (bms): two dorsal bms (short and long) and one ventral bms. Ant.II with three bms and one latero-distal s, Ant.III with one bms and four distal s (lateral s absent, Fig. 15). Several tubular s-setae on Ant.IV. Organite small.
Remarks. Folsomia breviseta sp. n. combines several characters rare for the group: short macrosetae and s-setae, anterior position of medial s-setae on body tergites, the absence of ventral setae on Th.III. A loss of lateral s-setae on Ant.III is a very peculiar character while the nature of this character is not easy to interpret since all species of the family Isotomidae, if not all Collembola, have these s-setae. The absence of s-setae was confirmed in all available specimens. Beyond 'inoculata' group several blind species with two pairs of setae on manubrium can be confused with F. breviseta sp. n., for example, F. bisetosa Gisin, F. cephalota Bu et al., and F. sensibilis Kseneman. All these species belong to other groups and therefore differ essentially by characters of high rank.
Distribution and ecology. The species is known only from the type locality where it inhabits mountain forests and tundra.
Remarks. Our specimens fit to the original description of F. hidakana in all significant features. Uchida and Tamura (1968) did not show in figures a subapical rudimentary seta on posterior side of dens and short latero-central setae (l2) on manubrium (probably overlooked). We also found wider variability in most characters that is certainly explained by larger material we have studied. Macrosetae on figures in first description (Figs 28, 35 in Uchida and Tamura 1968) seem to be shorter than in our material. Folsomia hidakana is a peculiar species due to anterior position of medial s-setae on thoracic segments, 5+5 or more latero-distal setae on ventral tube (vs 4+4 that is more common for the group), four setae on posterior furcal subcoxa (fewer than common for the group), 3+3 latero-basal and 1+1 latero-central setae on posterior side of manubrium (fewer than common for the group). The absence of ventral setae on Th.III is the main differentiated feature of F. hidakana shared only with allopatric F. breviseta, the two species are combined in the formal subgroup 'hidakana' by us. From 'macrochaetosa' group F. hidakana differ by more setae on body and more lateral position of accp1-s on Abd.V (see Fig. 28 vs Figs 29,32). Being often mixed with habitually similar species (often with F. imparis sp. n.), F. hidakana is normally easy to recognize by scattered pigment grains on body.
Specimens collected in Japan, both in Honshu and Hokkaido, differ from specimens from Russia by three (vs two) s-setae on Ant.I. In Japanese populations the individuals with two s rarely occur so we keep both variants within diagnosis of F. hidakana.
As a whole, distributional range of the species appears to cover southern area of the Russian Far East, North Korea, and northern half of Japan (Fig. 90). It inhabits forest litter and decaying wood in low mountains, rare in higher altitudes.
Remarks. The species most resembles F. macrochaetosa and F. imparis sp. n. and is characterized by the absence of unpaired setae on anterior side of manubrium, short accp3-s-setae and long p1 setae on Abd.V (Table 2).
Distribution and ecology. Known from three neighboring localities of inner part of East Asia (Fig. 90). The species occurs in forest litter at different altitudes.
Derivatio nominis. The species is common in areas around Amur River lowlands.

Folsomia brevisensilla Potapov & Babenko, 2000
Material. Far East of Russia, Magadanskaya Region, Ten'kinsky District, village Kulu, 04.ix.1995, coll. S. Bukhkalo. Remarks. The species resembles F. inoculata sharing with the latter species a middle-sized furca, short s-setae on body, their position on tergites, and undifferentiated ventral setae on Th.III. Nevertheless, F. brevisensilla does not possess several unique characteristics of the latter species, e.g., large and tubular accp3-s on Abd.V and the absence of subapical seta on posterior side of dens.
Distribution. It is the most northern species of the 'inoculata' group since known so far only in the basin of Kolyma River (NE Asiatic part of Russia).
Description. Body size from 0.9 to 1.4 mm. Body without pigmentation, its shape as in F. amurica sp. n. Cuticle with fine hexagonal primary granulation ("smooth"). Ocelli absent. PAO slender, constricted, 1.4-1.7 as long as width of Ant.I and 1.7-1.9 as long as inner unguis length. Labium with five usual papillae (A-E), guard setae e7 absent, three proximal and four basomedian setae. Ventral side of a head with 4+4 postlabial setae. Ant.I with 15-17 common setae, two ventral s-setae (s) and three bms, one long (inseparable from common setae) and two short, Ant.II with three bms and one laterodistal s, Ant.III with one bms and with five distal s (including one lateral), without additional s-setae (Fig. 46). Several tubular s-setae on Ant.IV. Organite stick-like, small.
Remarks. Folsomia imparis sp. n. is well defined by the presence of unpaired setae on anterior side of manubrium shared only with F. hidakana (belongs to another subgroup) and F. setifrontalis (has anterior setae on ventral tube). Main differences from the other species of the subgroup 'macrochaetosa' are shown in Table 2.
A typical form, called preliminary as f. 1 (Fig. 32) has short p1-setae on Abd.I. In Japan and Primorsky Krai we often recorded specimens with long p1, as long as a1 (f. 2 in Table 2) which was not mixed with f. 1 by samples even if reported in the same areas.
Additionally, a closely related form was also recorded in two more eastern localities (see the Material part, F. sp. aff. imparis). It differs from all species listed in Table 2 having much more setae on body tergites: particularly, posterior row of Abd.IV has seven (vs. 3-4) p-setae between medial s-setae. The final decision on the status of these polychaetotic specimens was not made by us and calls for more information on their ecology and distribution.
Distribution and ecology. The species is widely distributed in Far East of Russia, Korea and in the most northern part of Japan (Fig. 90). We suppose some records of F. fimetaria in Hokkaido refer to this species. F. imparis sp. n. is rather common in different forest litter, often in rotten wood.
Derivatio nominis. The species has unpaired setae on anterior side of manubrium. Description. Body size from 0.9 to 1.5 mm. Body without pigmentation, cuticle with fine primary granulation. Ocelli absent. PAO slender, constricted, 1.4-1.6 as long as width of Ant.I and 1.4-2.2 as long as inner unguis length. Labium with five usual papillae (A-E), guard setae e7 absent, three proximal and four basomedian setae. Ventral side of a head with 4+4 postlabial setae. Ant.I with 15-16 common setae, s-setae of antennae as in F. imparis sp. n. Organite stick-like, small.
Remarks. F. amurica sp. n., F. imparis sp. n., F. macrochaetosa, and F. setifrontalis combine a group of species with long macrosetae and furca, sparse setae covering, and posterior position of median s-setae on all tergites. The differences between the species of this subgroup are shown in Table 2.
Distribution. Scattered records all over the coastal areas from Magadan (Russian Far East) to South Korea (Fig. 90). Remarks. Folsomia setifrontalis is sharply defined by the presence of anterior setae on ventral tube that is a unique character for the genus. Populations from Primorsky Krai differ from the type specimens (South Kuril Islands) by the presence of unpaired setae on manubrium and longer accp3-s on Abd.V. Considering this variability, a wider diagnosis is proposed for the species. So far, the chaetotaxy of ventral tube remain a key characteristic of this species.
Distribution and ecology. Less common than the sympatric F. imparis sp. n. and F. macrochaetosa. Rare records in forest litter of southern part of Far East of Russia. Description. Body size approximately 1.3 mm (Fig. 51). Without pigmentation. Cuticle with fine primary granulation ("smooth"). Ocelli absent. PAO slender, not constricted or slightly constricted, 1.5-1.7 as long as width of Ant.I and 1.7-2.0 as long as inner unguis length. Labium complete, guard setae e7 present, three proximal and four basomedian setae. Ventral side of head with 4+4 postlabial setae. Ant.I with 16-17 common setae, two ventral s-setae (s) and three basal micro s-setae (bms): two dorsal (short and long) and one ventral. Ant.II with three bms and one latero-distal s, Ant.III with one bms and with five distal s (including one lateral), without additional s-setae. Ant.IV with stick-like organite.
Distribution and ecology. Known from three locations in Russian Far East and North Korea (Fig. 90). It occurs in forest litter.
Remarks. Two setae at the middle of posterior side of dens are always absent in the type populations (Fig. 63, Khabarovsky Krai). Specimens from Kamchatka possess these setae (always rudimentary and one sometimes asymmetrically lost) (Fig. 67). We accept a wide diagnosis of the new species considering both variants.
An odd population was found near Uril (Amurskaya Region) differing from the typical ones by having 4+4 (vs 3+3) anterior setae on manubrium (left out of diagnosis of the new species so far).
For difference between F. trisensilla sp. n. and F. laconica sp. n. see Remarks to the latter. Distribution and ecology. Known from forest litter in three localities in Eastern Asia (Fig. 90).
Derivatio nominis. The new species name reflects the presence of three (vs four, as common for the genus) s-setae on dorsal side of Abd.V that is characteristic of the 'laconica' subgroup.
Description. Body size from 0.9 to 1.2 mm, shape of corpus rather tubular, slender. Without pigmentation. Cuticle with fine hexagonal primary granulation ("smooth"). PAO slender, insignificantly constricted, 1.6-1.8 as long as width of Ant.I and 2.1-2.2 as long as inner unguis length. Labium complete, guard setae e7 present, three proximal and four basomedian setae. Ventral side of head with 4+4 postlabial setae. Ant.I with 14-15 common setae, two ventral s-setae (with one thick) and three basal micro s-setae (bms): two dorsal (short and long) and one ventral. Ant.II with three bms and one latero-distal s, Ant.III with one bms and with five distal s (including one lateral), without additional s-setae. Organite normal, small.
Remarks. The new species belongs to the 'laconica' subgroup due to incomplete s-set on body. It differs from two other members, F. laconica sp. n. and F. trisensilla sp. n., by reduced chaetotaxy on anterior (2+2 instead of 3-4+3-4 setae) and posterior sides (1+1 vs 2+2 lateral setae) of manubrium. F. tertia sp. n. has the shortest macrosetae among species of the subgroup and somewhat resembles members of the 'tatarica' subgroup.

Folsomia calcarea
Description. Body size near 1.1 mm (for the largest subadult female). Body slender, tubular (Fig. 69). Cuticle with fine hexagonal primary granulation ("smooth"). Ocelli absent. PAO slender, constricted, 1.8-2.5 as long as width of Ant.I and 2.3-2.7 as long as inner unguis length. Labium with five usual papillae (A-E), guard setae e7 absent, three proximal and four basomedian setae. Ventral side of head with 3+3 postlabial setae. Ant.I with 11-12 common setae, two ventral s-setae (s) and three basal micro s-setae (bms), two dorsal (middle-sized and short) and one ventral (short), Ant.II with three bms and one latero-distal s, Ant.III with one bms and with four distal s (lateral s absent), without additional s-setae. Organite short and small.
Distribution and ecology. Known only from the type locality. The species possibly belongs to calciphilous fauna.
Derivatio nominis. The species was recorded in calcareous soil. Description. Body size 0.8-0.9 mm. Body slender, tubular (Fig. 70). Cuticle orthogonal, finely reticulated. Ocelli absent. PAO slender, not constricted or slightly constricted, 1.5-1.8 as long as width of Ant.I and 2.3-2.4 as long as inner unguis length (Fig. 78). Labium with five usual papillae (A-E), guard setae e7 present, three proximal and four basomedian setae. Ventral side of head with 3-4+3-4 postlabial setae. Ant.I with eleven common setae, two ventral s-setae (s) and three basal micro s-setae (bms) (Fig. 78), two dorsal (middle-sized and short) and one ventral (short), Ant.II with three bms and one latero-distal s, Ant.III with one bms (not found in one specimen) and with five distal s (including one lateral), without additional s-setae. Organite short and small.
Distribution. Known from the type locality. Derivatio nominis. The species is named after tubular shape of body.  . The furca is of middle size, in an intermediate position between short-furcated 'tatarica' and long-furcated 'macrochaetosa' subgroups; posterior chaetotaxy of the dens is uncommon: seta at the middle present whereas subapical one normally absent (fig. XIV, 6 in Stach, 1947), the latter, although often small, is present in all other species of the 'inoculata' group. Appearance of the species is rather specific enabling its recognition under low magnification (Fig. 81).

Folsomia inoculata
Available vast material on this species shows a wide variation in several characters (chaetotaxy of manubrium and dens, shape of PAO, body length) which, however, are individual or population-dependent and does not indicate several species.
According to the original description, PAO is not constricted in F. inoculata, which was also shown in associated figures by Stach (1947, figs XIV, 7 and XIV, 8). This peculiarity was a reason for Niijima and Hasegawa (2011) to retain F. ezoensis Yosii, 1965 (described from Japan, PAO constricted) and F. inoculata Stach, 1947 (described from Poland, PAO not constricted) as two separate species. In our material, PAO is normally constricted in both western and eastern Palearctic (incl. Japan) while the character continuously varies depending on the specimen being, in fact, not constricted in an extreme variant (Fig. 83). A constricted PAO that is unlike the original description was also indicated for European populations by , Schulz (1999), andFjellberg (2007).
The modern detailed description of the species is given in Fjellberg (2007). Among other characteristics, a reduction of dorsal chaetom of manubrium was stressed, particularly lateral pair (l2) lost, only one pair of setae was shown in pr-and m-groups (fig. 23B-C in Fjellberg 2007). Such chaetotaxy was found by us only in specimens from Helgoland (NW Germany, coll. J. Schulz) (Fig. 86). Specimens from other localities normally have a pair of lateral setae and two or more pairs of setae at least in pr-group (Fig. 88). The presence of lateral setae l2 is not stable; few individuals missing them on both sides (sometimes asymmetrically) were recorded by us in the North Caucasus (Fig. 87), Germany, France, and Japan. Thus, a wide variation of chaetotaxy of posterior side of manubrium can be concluded for F. inoculata.
Size of the body ranges between 0.9 and 1.7. Specimens from eastern populations appears to be smaller than in western ones, but the whole variation is strongly overlapping (0.9-1.5 vs 1.1-1.7 mm, respectively).
The performed multivariate analysis of metric morphology did not reveal any irregularities, and noticeable differences between eastern and western populations were not detected (Fig. 89). Nevertheless, individuals of a particular population often resemble each other and this may be partly explained by the same phenological condition.
The species is facultatively parthenogenetic and its populations mostly consist of females. Males were seen by us only in four "central" localities: in Middle Ural mountains (upper flow of Pechora River), East Siberia (Podkamennaya Tunguska), Caucasus (Aibga Range), Turkey, and Kazakstan (West Altai).