Revision of Palearctic species of the genus Dimorphaphorura (Collembola: Onychiuridae: Onychiurinae: Oligaphorurini) with description of new species

Abstract In this paper, the Palearctic genus DimorphaphoruraBagnall, 1949 (Collembola: Onychiuridae), is revised. The diagnosis of the genus is defined within the tribe Oligaphorurini based on the development of the furcal area, shape of furcal rudiment, and furcal chaetotaxy. Six new species are described: D. olenaesp. n. from Ukraine, D. inyasp. n . , D. pseudoinyasp. n., D. sibiricasp. n., D. caucasicasp. n. , and D. sophyaesp. n. from Russia. The type species of the genus, D. differensBagnall, 1949 is redescribed, and the lectotype and paralectotypes are designated. All previously known species are redescribed or with additional characters complemented: D. alnus ( Fjellberg, 1987 ) comb. n. , D. chatyrdagi ( Kaprus’, Weiner & Pomorski, 2002 ) comb. n. , D. daii ( Pomorski, Skarżyński & Kaprus’, 1998 ) comb. n. , Dimorphaphorura eremia ( Kaprus’,Weiner & Pomorski, 2002 ) comb. n. , D. hackeri ( Christian, 1986 ) comb. n. , D. irinae ( Thibaud & Taraschuk, 1997 ) comb. n. , D. melittae ( Christian, 1993 ) comb. n. , D. pseudoraxensis ( Nosek & Christian, 1983 ) comb. n. , D. raxensis ( Gisin, 1961 ) comb. n. , D. steposa ( Kaprus’, Weiner & Pomorski, 2002 ). An identification key to all Dimorphaphorura species is provided.


Introduction
established the genus Dimorphaphorura with the type species D. differens for the Tirolian specimens determined and briefly described by Stach (1947) as Onychiurus quadrituberculatus (Bőrner, 1901). The scant diagnoses presented by Bagnall (1949) do not allow for the clear differentiation of Dimorphaphorura from the genera Oligaphorura and Micraphorura created by him in the same paper. For this reason, the three genera have been considered junior synonyms of Onychiurus Gervais, 1841. Only in 1996 did Pomorski re-established Oligaphorura and Micraphorura to the generic level, and Weiner (1996) provided new diagnoses for these two genera and Dimorphaphorura based on new characters, but she wrongly interpreted the chaetotaxy of the manubrial rows, as she joined chaetae on rows mm and ma (1+1), which she considered as dental chaetae. Following the authors' genus level investigations of Onychiuridae, a corrected diagnosis of Dimorphaphorura is presented based on type material of described species. The generic status of Dimorphaphorura is discussed in light of the consideration made by Shvejonkova and Potapov (2011). In addition, a list of species recognized as belonging to the genus is given, and the lectotype and paralectotypes for the species studied are designated. Eleven species belonging to the genus Dimorphaphorura are currently known from the Palearctic region, distributed across mountainous regions (Tirol, Crimea Mts.), caves (Lower Austria, Crimea), and steppe and forest-steppe (Ukraine). These species were originally described in the genera Onychiurus, Onychiurus (Oligaphorura), or Micraphorura by Christian (1986Christian ( , 1993, Fjellberg (1987), Gisin (1961), Kaprus' et al. (2002), Nosek & Christian (1983), Pomorski et al. (1998) and Thibaud & Taraschuk (1997). Three further species were recently described (Shvejonkova & Potapov 2011;Sun & Wu 2012a, b).
The material studied is deposited in the following institutions: ISEA -Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Cracow, Poland; MNH -Museum of Natural History, Geneva, Swiss; NHMW -Naturhistirisches Museum, Wien, Austria; MSPU -Moscow State Pedagogical University, Russia; SIEE -Severtsov Institute of Ecology and Evolution Russian Academy of Sciences, Moscow, Russia; SNHM -State Natural History Museum of Ukrainian National Academy of Sciences, L'viv, Ukraine; TUM -Tromsø University Museum, Department of Natural Science, Norway ZIWU -Department of Biodiversity and Evolutionary Taxonomy, Zoological Institute, Wrocław University, Poland.

Material and methods
The specimens of the species hereby described were extracted from soil and litter samples using Berlese funnels and stored in 90% ethanol. They were cleared in Amann's lactophenol and mounted on slide in Marc-André or Faure's solution. The type material from the collections were studied and redescribed.

Nomenclature
This publication and the nomenclature it contains have been registered in ZooBank. The LSID number is: urn:lsid:zoobank.org:pub:AD9A913A-78E5-49A4-A5DC-F1CDD5538706 It can be found online by inserting the LSID number after www.zoobank.com/

Remarks
Genus Dimorphaphorura is most similar to genera Micraphorura and Oligaphorura. All mentioned genera differ clearly by the organisation of the furcal area, as is presented in Figures 1-3. Micraphorura and Oligaphorura possess 1+1 and 2+2 (in two rows) dental chaetae (= setulae according Pomorski 1996Pomorski , 1998, respectively, showing special basis (Figure 1 and 2). These chaetae could be accompanied by 1+1 manubrial chaetae (ma). Dimorphaphorura is devoid of dental chaetae. Further differation concerns the chaetotaxy of the manubrial area. In Micraphorura and Oligaphorura, chaetae of manubrial row ma migrated anteriorly to the level of dental chaetae. In addition to chaetae ma, species of these two genera always carry 2 or more medial chaetae in rows mm and mp. In Dimorphaphorura, the chaetotaxy of the manubrial area consists of three rows: ma, with 4 (rarely 2) chaetae placed below dental area; row mm, which preserves only 1+1 external chaetae; and row mp, with 4-6 chaetae (external ones as macrochaetae). The dental area is developed differently in all three genera. In Oligaphorura, the dental area is developed as a cuticular fold (like in Protaphorura), in Micraphorura as a cuticular furrow or rather triangular pocket, and in Dimorphaphorura as a fine granulated area. Also, all 11 tibiotarsal chaetae are present in the distal whorl of Micraphorura and Oligaphorura species, whereas in Dimorphaphorura their number could be reduced (11 to 5 chaetae) (Table 1). Bagnall, 1949 (Figures 4-10) Dimorphaphorura differens Bagnall, 1949: 511 (= Onychiurus quadrituberculatus Stach, 1947, nec Börner 1901
Antennal base well marked by finer and regular granulation. Antennae nearly as long as head. Sensory organ of antennal segment III consisting of 5 chaetae, 5 papillae, 2 smooth sensory rods, 2 weakly granulated sense clubs (internal clubs straight and globular, external clubs bigger, weakly ribbed and bent), ventrolateral sensillum present (Figure 7). Antennal segment IV with subapical organite and microsensillum ( Figure 7).
Postantennal organ vesicle with three lobes, located in small cuticular depression, as long as 1.5 nearest pseudocellus. Labral chaetotaxy not seen. Maxillary outer lobe with simple palp, sublobal hairs not seen. Labial type ABC ( Figure 5). Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, mm with 2 external chaetae and mp with 5 chaetae ( Figure  8).
Anal spines 0.48 of length of inner edge of claw and 2.5 times as long as their basal diameter.

Remarks
Dimorphaphorura differens is very similar to D. caucasica sp. n., the other mountain species from North Caucasus (Table 1). Both species have the same pseudocellar formula, the same number of chaetae in the distal tibiotarsal whorl, and an antennal sensory organ with 5 papillae. They differ in the number of chaetae on subcoxae 1 (4, 4, and 5 in D. differens and 3, 3, and 3 in D. caucasisa), the granulation of the abdominal tergum VI (coarse, in the shape of a band in D. differens and homogenous in D. caucasica) and in the size of anal spines (smaller in D. differens).
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, row mm with only 2 external chaetae, and row mp with 4 chaetae.
Anal spines 0.74-0.85 of length of claw inner edge and 2.7 times as long as their basal diameter.
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, row mm with only 2 external chaetae, and row mp with 4 chaetae ( Figure 18).
Anal spines 0.69 times of inner claw edge and 2.4 times as long as their basal diameter.

Remarks
See remarks in D. differens and Table 1.

Etymology
The name of the new species refers to the type locality that belongs to the Caucasus Mts.

Distribution
Russia: North Caucasus.

Additions to the original description
Labial type AC. Maxillary outer lobe with simple palp and with 2 sublobal hairs. Sensory chaetae s on body slightly differentiated. Subcoxa 1 of legs I-III with 2, 3, 3 chaetae respectively. Furcal rudiment consisting of a fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 2-3 chaetae arranged asymmetrically, row mm with 2 external chaetae and row mp with 4 chaetae. Empodial appendage with large basal lamella and 0.9 of claw inner edge.
Furcal rudiment: a fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, row mm with only 2 external chaetae, and row mp with 4 chaetae.
Anal spines 0.33 times of inner claw edge and 5.4 times as long as their basal diameter.
Anal spines 0.79 times as long as inner edge of claw and 3.17 times as long as their basal diameter.

Remarks
The new species, together with D. alnus, D. sibirica, and D. pseudoinyae, belongs to the group of species with 11 chaetae in the tibiotarsal distal whorl (Table 1). They also have microsensilla on thoracic terga II and III, the same type of labial palp (AC), and the same number of dorsal pseudocelli on the head, thorax, and abdomen I-III (32/133/333). D. inyae and D. pseudoinaye present the same number of pseudocelli on abdominal terga IV and V (5 and 4), while the others have 4 and 3 pseudocelli. D. sibirica and D. inyae do not have pseudocelli on abdominal sternum IV, unlike to D. alnus and D. pseudoinyae, which carry 1+1 pseudocelli. The most similar species, D. inyae and D. pseudoinyae, live in different environmental conditions. D. inyae was found on the boulder ridge of Katun river while D. pseudoinyae in Siberian steppe.

Etymology
The name of the new species refers to the type locality in Inya village. Antennae approximately as long as head. Antennal segment I with 8 chaetae, antennal segment II with 13-14 chaetae. Sensory organ of antennal segment III consisting of 5 chaetae, 5 papillae, 2 smooth sensory rods, 2 weakly granulated sense clubs (internal clubs straight and globular, external ones bigger, ribbed and bent), ventro-lateral sensillum present. Antennal segment IV with subapical organite and microsensillum.
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4 chaetae, respectively.
Anal spines 0.70 times as inner edge of claw and 2.2 times as long as their basal diameter.
Antennae approximately as long as head. Antennal segment I with 8 chaetae, antennal segment II with 13 chaetae. Sensory organ of antennal segment III consisting of 5 chaetae, 5 papillae, 2 smooth sensory rods, 2 weakly granulated sense clubs (internal clubs straight and globular, external ones bigger, ribbed and bent), ventro-lateral sensillum present. Antennal segment IV with subapical organite and microsensillum.
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4 chaetae, respectively.
Anal spines 0.6-0.71 of length of claw inner edge and 3.4-4.0 times as long as their basal diameter.

Distribution
Austria: Lower Austria.
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4 chaetae, respectively ( Figure  36).
Anal spines 0.50 of length of inner edge of claw and 2.0 times as long as their basal diameter.

Remarks
See remarks in D. sophyae sp. n. and Table 1.

Etymology
The new species is dedicated to Olena Starostenko, who collected the material of the species.

Description
Holotype length 0.66 mm, length of paratypes: 0.62-0.82 mm. Body shape cylindrical. Colour in alcohol white. Granulation homogenous, with coarse granules around all dorsal pseudocelli. Usually 11 grains around each pseudocellus.
Furcal rudiment: fine granulated area with three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4-5 chaetae respectively.

Remarks
See remarks in D. inya sp. n. and Table 1.

Etymology
The name of the new species is derived from the similar species D. inya sp. n.
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4 chaetae respectively.
Anal spines as spiniform chaetae 5.3 times as long as their basal diameter.

Additions to the original description
Ventral tube with 6+6 distal and 2+2 basal chaetae. Furcal rudiment comprising a fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4 chaetae respectively. Claw without denticle. Empodial appendage shorter than claw (0.8 of claw inner edge), with distinct basal lamella.
Anal spines 0.5 times as long as inner edge of claw and 2.0 times as long as their basal diameter.

Distribution
Austria: Lower Austria.
Furcal rudiment: small area with fine granula-tion and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, row mm with only 2 external chaetae, and row mp with 4-5 chaetae (Figure 44).
Anal spines 0.95 times as inner edge of claw and 2.86 times as long as their basal diameter.

Etymology
The name of the new species refers to the type locality that belongs to the studied region, Siberia.
Furcal rudiment: fine granulated area and three rows of chaetae behind its posterior edge. Row ma with 4 chaetae, rows mm and mp with 2 and 4 chaetae respectively ( Figure  52).
Anal spines 0.77 times as long as inner edge of claw and 3.0 times as long as their basal diameter.

Remarks
Between the species of the genus Dimorphaphorura, only D. sophyae sp. n. has four papillae in the sensory organ of antenna III and empodial appendage equal or longer than claw (Table 1). Based on the pseudocellar formula and the number of chaetae in the distal tibiotarsal whorl (9), the new species is most similar to D. pseuraxensis. Besides the number of papillae in the sensory III organ, both species differ in the type of labial palp (AC in D. sophyae and ABC in D. pseudoraxensis) and in the length of empodial appendage (empodium equal or longer than claw in D. sophyae and shorter than claw in D. pseudoraxensis). Two other species, D. irinae and D. olenae, have the same dorsal pseudocellar formula and number of distal tibiotarsal chaetae (9), but they differ in the pseudocellar formula of abdominal sterna I-IV (0001 in D. irinae, 1111 in D. olenae, absent in D. sophyae and D. pseudoraxensis) and also in the length of empodial appendage (empodium shorter than claw in D. irinae and D. olenae).

Etymology
The new species is dedicated to Dr. Sophya K. Stebaeva, a well-known researcher of Siberian collembolan fauna and our friend.

Remarks
The species was described by Shvejonkova and Potapov (2011) in the genus Micraphorura. However, it possess characters allowing the transfer of this species to the genus Dimorphaphorura. The arragment of the furcal area is typical to the latter genus: without pocket and dental setulae, with only external (1+1) mm chaetae. The species also posses also some distinct (vs. indistinct in species of Micraphorura) chaetae s on the body and a lower number (7)  18. Tibiotarsal distal whorl with 6 chaetae, microsensilla on thoracic tergum III absent…..

Discussion
Recently, Shvejonkova and Potapov (2011), based mainly on published descriptions of species and their used names of genera, considered that "the independence of Dimorphaphorura calls for further ground." For them, "several lines of Oligaphorurini independely undergo the reduction of furcal area, including furrow and number of manubrial seatae as well as the reduction of chaetotaxy of body and tibiotarsi, resulting in low value of these characters at level of generic taxonomy of Oligaphorurini." They considered the independence of Micraphorura and Oligaphorura to be supported by the number and location of dental chaetae only, while shape of dental and manubrial area vary. Shvejonkova and Potapov (2011) proposed a new tentative diagnosis for two of the main genera of the tribe Oligaphorurini, Micraphorura and Oligaphorura, both including species with or (more rarely) without anal spines as well as with different stages of furcal area development. For this reason, comparison of the furcal areas of Oligaphorura, Micraphorura, and Dimorphaphorura is presented in the Remarks to the genus Dimorphaphorura and in Figures 1-3. For the moment it seems appropriate to preserve the genus Dimorphaphorura, whereas further investigations (including molecular sequencing) could resolve problems related to the diagnosis of the three genera mentioned above.