New and little known Isotomidae (Collembola) from the shore of Lake Baikal and saline lakes of continental Asia

Abstract Collembola of the family Isotomidae from the shores of Lake Baikal and from six saline lake catenas of the Buryat Republic (Russia) and Inner Mongolia Province (China) were studied. Pseudanurophorus barathrum Potapov & Gulgenova, sp. nov. and Parisotoma baicalica Potapov & Gulgenova, sp. nov. from Baikal and Ephemerotoma buryatica Potapov, Huang & Gulgenova, sp. nov. and Folsomia mongolica Huang & Potapov, sp. nov. from saline lakes are described here. A morphological description of epitokous males of Scutisotoma acorrelata Potapov, Babenko & Fjellberg, 2006 is given. A list of 23 species of the family Isotomidae found in the shores of studied lakes is provided based on literature sources and newly collected material.


Introduction
The springtail fauna of lake shores in Asia is poorly known. Some data is available from lakes of western Siberia (Stebaeva 1981(Stebaeva , 2006Berezina 2006) where changes in species composition along forest-steppe lakesides were studied. Basing on those materials several specialised species have been discovered at saline lakes (Stebaeva 1978). In 2014 and 2015 a Chinese-Russian team of researchers investigated the Collembola of more eastern areas of arid zone of continental Asia. Saline lands associated with six saline lakes of Buryatia (Russia) and Inner Mongolia (China) were studied resulting in the discovery of two new species.
Approximately 10-20 million years old Lake Baikal, a huge ancient reservoir of fresh water at the centrum of Asia, has exceptionally high faunal diversity and endemism (Martens 1997). Several new species of Collembola have been described from the lake shore (Potapov 1991;Babenko et al. 1994Babenko et al. , 2011Potapov et al. 2006;Huang and Potapov 2012;Potapov and Gulgenova 2013). Recent collecting on shingly beaches revealed two new species of the specialised littoral fauna of the lake.
In the present paper we describe four new species, two from saline lakes and two from Baikal, and provide a list of springtails of the family Isotomidae recorded from the surveyed lakes.

Materials and methods
Collembola were sampled in catenas of six saline lakes in 2014 and 2015. Shores of the following lakes were studied: Alginskoye (53. 633°N (Fig. 58). Tullgren/Berlese funnels were used to extract Collembola from 492 soil cores, 125 cm 3 each. Samples were collected from four positions at each catena: lowest accumulative part, two transit parts and upper alluvial part (steppe). One of the views of the catena at Lake Verkhneye Beloye is shown in Fig. 59. All parts were saline and covered with halophytes. On Lake Baikal shore, the springtails were collected in 2008-2017 by floatation in water of shingle and sand.  Fjellberg (1999), elements of maxillary head follow Fjellberg (1984), labrum follow Yosii (1976), and chaetotaxy of p-row of tergites in Parisotoma Bagnall, 1940follow Potapov (1991. Description. Size 1.0-1.5 mm. Body broad, with long legs (Fig. 1). Pigmentation from almost white to pale grey, forming a diffuse net interrupted by intersegmental areas. Cuticle finely reticulated ("smooth"), size of polygons much smaller than bases of setae. Large specimens sometimes with regularly scattered hardly visible small pits. Lateral parts of intersegmental area with secondary granulation (Fig. 6). Ocelli absent. PAO small, not constricted, ca. 0.3 as long as Ant.1 width and ca. half as long as U3 (Fig. 8). Maxillary outer lobe with simple maxillary palp and four slender sublobal hairs (Figs 2, 3). Labral formula as 3/556 (Fig. 3). Labral edge reduced, apical ridges absent. Apical row (p-row) of labral setae projecting above mouth aperture (Figs 2 and 3), normally with six setae: p1, p2, and p3 on each side, lateral pair (p3) more slender and long. Medial pair p1+p1 is sometimes replaced with one (p0) giving five setae (p0, p1, p2) in apical row and labral formula 3/555 (Fig. 3). Setae of two rows (m, p) of labrum and sublobal hairs form a basket surrounding the mouth. Labium with all papillae (A-E), papillae A without guards (Fig. 4). Guard a1 detached and integrated to papilla B which, in result, supplied with five guards (a1, b1-4). Guards b2, b3, b4 set together, on lateral expansion of papilla B. Papilla C without guards, D with four guards in normal position. E with seven guards, lateral process and two lateral guards enlarged. Terminal setae of all papilla short. All elements of hypostomal group (H, h1, h2) considerably enlarged and bent towards labrum complementing the upper "basket" (Figs 2, 4). Main part of labium with three proximal, four basomedian and five basolateral setae. Maxillary head modified: capitulum slender and formed by fused claws, lamellae enlarged. Lamellae 1 and 2 well beyond capitulum, each supplied with apical and inner rows of cilia. Outer edge of lamella 1 gently ciliated, sometimes wavy. Lamella 3 expanded, with strong teeth (Fig.  5). Ventral side of head with 5-6+5-6 postlabial setae. S-setae and bms-setae of antennae slender and resemble common setae. Ant.1 with two basal, ventral and dorsal, bms, two ventro-lateral s, and ca. 30-40 common setae (Fig. 8). Ant.2 with three bms and one laterodistal s. Ant.3 with one bms, five common s (two outer, two inner, and one lateral spine-like), and a group of additional thin s-setae located on dorsal and inner sides of segment ( Fig. 9), inner additional s-setae hardly differ from common setae. S-setae on Ant.4 weakly differentiated, subapical organite rudimental, apex without bulb (Fig. 10).
Affinity. This remarkable species is characterised by two (more rarely one) additional setae on labrum that is so far unknown in Pseudanurophorus Stach, 1922 and other Collembola as well. Labral formula 5,5,4 (vs. 5,5,5-6 in P. barathrum sp. nov.) is invariable in Isotomidae and it is clear that the character is often omitted although being implied in the descriptions. Other mouth parts are also strongly modified: labral edge is reduced; two anterior setal rows and the sublobal hairs form a basket surrounding the mouth; hypostomal setae and lateral process are enlarged; guard a1 is integrated with papilla B; guards b2, b3, b4 set on lateral expansion of B; maxillary head has slender capitulum and expanded lamella. Unusually high number of setae on tibiotarsi and ventral tube and the dense and short abdominal hair cover is an apparent adaptation to live in close contact with water, as in many other littoral species. The new species belongs to the "boerneri" group due to three prelabral, 4+4 or more postlabial setae, simple maxillary palp and other characters (for details see Potapov 1997). It most resembles two species with short macrosetae P. arcticus Christiansen, 1952and P. montanus Martynova, 1971(1971a, for which labral formula is unknown. Following the first description and Fjellberg's comments (1975) on P. arcticus paratypes, these two species have much fewer setae in axial group of tergites and yet have macrosetae on last abdominal segments (vs. absent in P. barathrum sp. nov.). Pseudanurophorus arcticus is described and subsequently recorded in the Arctic and P. montanus in the mountains of Middle Asia.
Distribution and ecology. Several records from the littoral zone of the shore of Lake Baikal, none found inland. It is one of the common species in shingly beaches.
Name derivation. It is named after the specific mouth parts (barathrum -a glutton in Latin, among other translations). Description of epitokous males with fully developed ejaculatory duct in shore of Lake Baikal. Size ca. 1.2 mm, subequal to adult females. Macrosetae erect, slightly serrated, well developed on all body tergites and head. Three first segments of antennae with thickened setae (Fig. 16). In females, subadult males and juveniles macrosetae are only developed on thoracic (only lateral pair) and two last abdominal segments (Fig.  14). Number of macrosetae 3,3/3,3,3,3, their arrangement as common for Anurophorinae (in position Md, Mdl and Ml), apart from Abd.IV on which Mp and Mdl are in common position while macrosetae Ml is absent and Md shifted backwards and set in posterior row of setae. Common arrangement of macrosetae on Abd.IV for Anurophorinae shown in Fig. 18. Ventral side of Abd.VI with two thin curved macrosetae (vs. of normal shape in females). Head with macrosetae at posterior edge, in ocellar field, and between antennae. Front of head slightly swollen (vary). Antennae bent downwards. Three first segments of antennae thickened. In fully developed variant Ant.1 with three spiny setae (sp), Ant.2 with one sp and two ventral trichobothria, Ant.3 with two sp, one ventral trichobothrium and few (two or three) male "spurs" (Fig. 15). Thicknesses of sp vary. Tibiotarsus 3 with setae X and B5 insignificantly modified, set in wider sockets than in female.

Remarks.
Considering the dimorphic species S. muriphila (Grinbergs, 1968) and S. stepposa (Martynova, 1975) (for details see Grinbergs (1968), Chimitova and Potapov (2011)), S. acorrelata is the third member for the genus Scutisotoma Bagnall, 1948 which shows well developed sexual dimorphism. Males of S. acorrelata are less  (14) and adult male in reproductive stage (16) (pigmentation not shown) 15 Ant.1-3 in adult male in reproductive stage, lateral view 17 macrosetae on Abd.IV in adult male of S. acorrelata 18 common arrangement of macrosetae on Abd.IV in Anurophorinae. Abbreviations: bms-basal micro s-seta, de-ductus ejaculatorius, s-s-seta, is, ls, os-inner, lateral, and outer s-setae of antennal organ, sp-spiny setae, vt-ventral trichobothrium, msp-male spurs, Md, Mdl, Mp, Ml-macrosetae of Abd.IV. modified than in the two other species and polymorphism was not evident in our material. In taxonomical terms, the presence of epitokous males is a character of low value at generic level. It is probably optional in several genera. At species level, the diagnostic value of epitokous males is questionable. In many genera of the family Isotomidae the epitokous males are probably more frequent than usually considered. The short duration of the reproductive instar may have left many epitokous forms undetected.
Distribution and ecology. The species was described from shore of Lake Baikal (Potapov et al., 2006) and was further recorded at saline Alginskoye Lake and freshwater Bolshaya Eravna Lake. It lives in seaweed debris and in coarse sand. Description. Size 0.6-0.9 mm. Body as common for Anurophorinae with short furca (Fig. 27). Pigmentation grey, as in Proisotoma minuta (Tullberg, 1871). Cuticle finely reticulated, size of largest polygons smaller than bases of setae. Ocelli 8+8, G and H smaller (Fig. 23), all ocelli usually look subequal by pigmentation. PAO with three guard setae along posterior margin, elliptical, not constricted, as long as 0.4-0.6 of Ant.1 width and 0.7-1.1 as long as U3 (Fig. 23). Maxillary outer lobe with simple maxillary palp and four sublobal hairs. Labral formula as 2/554. Labium with all papillae (A-E), papillae A-D with normal number of guards (1,4,0,4), E with four guards (Fig. 21). Main part of labium with three proximal, four basomedian and five basolateral setae. Ventral side of head with 4+4 postlabial setae. Ant.1 with two basal, ventral and dorsal, bms, two ventro-lateral s, and eleven setae, without p-setae (Fig. 23). Ant.2 with three bms and one laterodistal s. Ant.3 without bms and with five distal s (including one lateral spine-like), inner s of AO small (Fig. 22). All s-setae on Ant.1-3 very short. S-setae on Ant.4 weakly differentiated, subapical organite small. Apex of Ant.4 with bilobed bulb (Figs 24-26), well visible in dorsal view (Fig. 25). In fully grown animals the bulb can look trilobed due to slight secondary division of one of the lobes (Fig. 26).
Affinity. The species belongs to recently described genus Ephemerotoma Potapov, Kahrarian, Deharveng & Shayanmehr, 2015 due to simple maxillary palp, reduced number (four) of guards on labial papilla E, two prelabral setae, complete set of ms-setae on tergites (11/111), and tergal s-setae on abdomen set in front of p-row. Ephemerotoma buryatica sp. nov. does not share a significant character of the genus, the "two transverse rows" pattern of s-setae on Abd.V. The sexual dimorphism common for the genus Ephemerotoma [E. porcella (Ellis, 1976), E. skarzynskii Potapov, Kahrarian, Deharveng & Shayanmehr, 2015, E. huadongensis (Chen, 1985)] is not observed in the new species. Small and rather slender body, short furca, shape of unguis, and absence of sexual dimorphism indicate a preference for deeper edaphic habitat than in its congeners.
Regarding all genera of the Proisotoma complex, a peculiarity of the new species is the bilobed apical bulb on Ant.4, which is otherwise known only in Proisotoma bulba Christiansen & Bellinger, 1980 (California, U.S.A.). The generic position of P. bulba is obscure because of lack of information on mouth parts and s-setae on body. In other characters, E. buryatica sp. nov. differs from P. bulba by fewer setae on dens (3/4 vs. 4-5/5-6), shorter dens (dens : mucro = 9 : 1 in bulba), teeth on tenaculum (3+3 vs. 4+4) and characters of unguis and tibiotarsi (bulba has inner tooth on unguis and a clavate tenent hair). In Proisotoma complex, a similar furca is shown, for example, for Weberacantha echinodermata Fjellberg, 2006 andScutisotoma robustodens Huang &Potapov, 2012, which belong to other genera. Mouth parts (two prelabral setae, simple maxillary palp and reduced number of e-guards) of E. buryatica sp. nov. resemble the "asiatica" group of the genus Subisotoma but several other characters of great value are different (e.g., presence/absence of anterior setae on manubrium).
Distribution and ecology. Known only from one locality in SW Buryatia where it inhabits soil of dry steppe at upper part of a salt-lake catena. The species probably occurs in all seasons since it was recorded in May, July and October in the type locality. It was highly aggregated in October which that suggests a resemblance to the "ephemeral" species of the genus Ephemerotoma.
Name derivation. It is named after the type locality. Description. Size 1.0-1.3 mm. Body of normal shape (Fig. 32). Usually without pigmentation apart from two contrasting black ommatidia on each side of head (Figs 32, 33). Darker specimens with diffuse black grains also on head and trunk. Specimens with weak eye pigmentation sometimes occur among normal ones, while cornea of ocelli are still distinct. Juveniles almost unpigmented. Cuticle with weak hexagonal primary granulation ("smooth"), thin belts of courser granulations at posterior edge of head, between Abd.IV and V and on medial line of thorax. Two widely separated large subequal ocelli on each side of head, like in F. quadrioculata (Tullberg, 1871) (Fig. 38). PAO narrow, well constricted, 1.1-1.4 as long as width of Ant.1 and 1.6-1.9 as long as inner unguis length. Maxillary outer lobe with four sublobal hairs, maxillary palp simple. Labral formula as 4/554. Labium with five papillae (А-Е) and full set of guard setae (e7 present), with three proximal and four basomedian setae. Ventral side of a head with 4-5+4-5 postlabial setae. Ant.1 with three ventral s-setae and three short basal ms-setae (bms), two dorsal and one ventral (Fig. 38), Ant.2 with three bms and one latero-distal s, Ant.3 with one bms and with five distal s (including one lateral), without additional s-setae. S-setae on Ant.4 weakly differentiated. Organite small.
Affinity. The species belongs to "heterocellata" group due to simple maxillary palp. F. mongolica sp. nov. is very similar to two other species inhabiting arid landscapes of continental Asia: F. pseudodecemoculata Stebaeva, 1971 and F. heterocellata . All three forms have no body pigmentation and share several important characters: structure of furca, body chaetotaxy, number of s-setae on antennae. The only sharp difference is number of ocelli on each side of the head: two in F. mongolica sp. nov., four in F. heterocellata, and five in F. pseudodecemoculata. The last species has shorter PAO than in the new species. F. montana Martynova, 1971Martynova, (1971b (high mountains plateaus of Kirghisia) also belongs to "heterocellata" group and has 2+2 ocelli, but differs by three basal setae on posterior side of dens (vs. four in F. mongolica sp. nov.), 3+3 (vs. 4+4) laterobasal setae on posterior side of manubrium, and shorter PAO. Distribution and ecology. The species is probably distributed in Inner Mongolia (China). This halophilic species is abundant on saline lands but also inhabits dry forest slopes.
Name derivation. It is named after the location of type place (Inner Mongolia Autonomous Region).  Description. Body length from 0,7 to 0,9 mm. Pale with diffuse greyish pigment on body, eye spot less marked than in most species of Parisotoma with one ocellus (Fig. 43). Ant.1 with 5-7 short s-setae ventro-laterally, three basal microsetae, two dorsal and one ventral (Fig. 47). Inner s-setae of AO III large. Ant.4 as common for the genus. One small ocellus on each side of head (Fig. 46). PAO wide, 1.4-1.8 as long as internal crest of Claw 3. Labral formula 4/554, apical folds sharp, as in P. notabilis (Schäffer, 1896). Maxillary outer lobe with four sublobal hairs and trifurcate apical palp. Labial palp with five papillae (A-E) and full set of guards (16, including e7), lateral process expanded. Papilla B with small basal process on its inner side (Fig. 52) (see the remarks). Labium with five basomedian, five basolateral, and four proximal setae. Number of postlabial setae from 3+3 to 4+4 (Figs 48 and 49), in the latter case an additional pair set between a1 and m1 (marked in Fig. 48). Inner mouthparts as usual for the genus: lamella 1 longer than capitulum with apex fan-shaped expanded, with marginal ciliation and one row of long denticles on inner side, lamella 6 with marginal ciliation and several (>3) irregular rows of denticles. Lower subcoxa of Leg 1 with one outer seta (Fig. 44). Tibiotarsi of all legs with only seven setae in apical whorl. Claw slender, without clear teeth (Fig. 55). Empodial appendage with broad lamella. Ventral tube with 3+3 lateral, 3+3 anterior (rarely two or four), and 4-6 posterior setae (Fig. 54). Retinaculum with 4+4 teeth and 2(3) setae. Furcal subcoxa with 27-35 setae. Manubrial thickening simple. Anterior side of manubrium with numerous setae of which 2+2 shorter medial ones in its apical part. Dens with numerous setae on anterior side and eight setae on posterior side (two basal, three internal and three external) (Fig. 56). Mucro with three teeth (Fig. 53).
Slender claw, polychaetosis, short macrosetae, and expanded lateral process of papilla E indicate adaptation to live in contact to fresh water. The combination of 3+3 laterodistal setae on ventral tube and only one outer seta on lower subcoxa of Leg 1 indicate the formal similarity with the eurytopic species P. notabilis (rare at Lake Baikal) but P. baicalica sp. nov. differs by all "littoral" characters mentioned above.
The value of basal process on labial papilla B (Fig. 52) calls for further study. So far it was not mentioned in the descriptions of labium while we have seen it also in P. reducta and P. appressopilosa that may suggest its diagnostic importance for the genus Parisotoma.
Distribution and ecology. Known only from two distant localities on the Baikal shore. A littoral species.
Name derivation. It is named after the location of the type locality.
New species records on the shore of Lake Baikal Other new records of species concern shores of saline lakes and therefore are given in the Table of Appendix 1.

Faunistic notes
Three ecological groups can be recognised among the recorded species: 1. Species widely distributed in the Holarctic and living also at sites distant from the lake shore (notated as W in Appendix 1). This group mostly consists of xerophilic and steppe species (e.g., F. parvulus, A. stebayevae, A. mongolicus, F. mongolica sp. nov.) which occur also on neighbouring arid landscapes of continental Asia. They often prefer saline lands and penetrate to catenas of saline lakes where they can be numerous. The group also include widely distributed eurytopic (P. notabilis, P. minima) and ruderal species (P. minuta). The latter species can be very abundant in lower part of catenas. 2. Lake species (as L in Appendix 1). This group consists of species found so far only in lake shores. They mostly belong to the fauna of Lake Baikal (P. barathrum sp. nov., S. acorrelata, S. baica, S. robustodens, P. appressopilosa, P. baicalica sp. nov.). Folsomia uniramia presumably belongs to the group since it has been recorded only in dunes at this lake shore. S. acorrelata and P. appressopilosa also occur in shore of saline Alginskoye Lake which is close to Baikal Lake. Considering salt-lake catenas, E. buryatica sp. nov. is only species which belongs to this group. 3. Hygrophilic widely distributed species (as H in Appendix 1). In our materials, Isotomurus stuxbergi (Tullberg, 1876) is the only member belonging to this group. It was found once in the Baikal shore.