Contribution to the knowledge of Neanurinae of north-western Iran with description of seven new species (Collembola, Neanuridae)

Abstract Seven new species of the subfamily Neanurinae from north-western Iran are described and illustrated in detail. Endonura agnieskaesp. nov. differs from the most similar congener, E. reticulata (Axelson, 1905), in chaetotaxic details and the arrangement of tubercles on the dorsal side of the body. Endonura annaesp. nov. can be easily recognised by its wide labrum, the absence of chaetae C on the head and the presence of a toothed claw. Endonura schwendingerisp. nov. is especially distinctive due to the absence of chaetae A and Ocp on the head and the presence of the male ventral organ. Deutonura brevisetasp. nov. is related and most similar to D. persica Smolis, Shayanmehr & Yoosefi-Lafooraki, 2018, described recently and known from Mazandran Province in Iran. The new species can be easily distinguished by the following set of features: dark pigmented body, presence of chaetae C and Dl3 on the head, absence of microchaetae on the furca rudimentary, presence of thickened macrochaetae on dorsal side of body and absence of cryptopygy. The main characteristics of Deutonura sengletisp. nov. include a white body with dark pigmented eyes, the fusion of tubercles Di and De on the first thoracic segment and the presence of the male ventral organ. Deutonura iranicasp. nov. is superficially similar to D. gibbosa Porco, Bedos & Deharveng, 2010, a species known from the Alps and Jura in Europe, but it differs in the body colour and the number of labial chaetae and chaetae (L+So) on the head. Paravietnura rostratasp. nov., the first member of this enigmatic and intriguing genus known from Iran, is characterised by an unusually elongate ogival labrum and extreme reduction of dorsal chaetotaxy. Furthermore, new records of several other species of the subfamily: Cryptonura maxima Smolis, Falahati & Skarżyński, 2012; C. persica Smolis, Falahati & Skarżyński, 2012; Deutonura persica; Endonura longirostris Smolis, Shayanmehr, Kuznetsova & Yoosefi-Lafooraki, 2017; E. paracentaurea Smolis, Shayanmehr, Kuznetsova & Yoosefi-Lafooraki, 2017; Neanura deharvengi Smolis, Shayanmehr & Yoosefi-Lafooraki, 2018; N. muscorum (Templeton, 1835) and Protanura papillata Cassagnau & Delamare Deboutteville, 1955 are given. The present study is based on the rich material collected by Antoine Senglet and loaned by Peter J. Schwendinger.


Introduction
Springtails, classified within the subfamily Neanurinae, differ significantly in terms of morphology and behaviour from other Collembola. First of all, they have completely lost the furcula and their movement may be defined as exceptionally slow compared to the majority of springtails. Another noticeable difference between them and the majority of other Collembola is the covering of the dorsal and lateral sides of the body by spherical structures naming tubercles, which make them resemble a mulberry. In addition, chaetae covering Neanurinae body are usually strongly developed, elongated and considerably widened, as well as covered with numerous teeth (Deharveng 1983;Smolis 2008). Paradoxically, although they do not have a furcula, i.e. structures enabling express escape from predators, Neanurinae are an example of an evolution success, demonstrated by its over 800 currently described taxa which constitutes nearly one tenth of all the known Collembola (Bellinger et al. 2020;Smolis and Greenslade 2020). Regarding the actual distribution of the subfamily, the largest species diversity is observed both in tropical and temperate forests on all continents, excluding Antarctica (i.e. Yosii 1976;Cassagnau and Deharveng 1984;Deharveng and Weiner 1984;Cassagnau 1988;Deharveng 1989;Deharveng and Bedos 1992;Cassagnau 1996;Deharveng and Suhardjono 2000;Palacios-Vargas and Simón Benito 2007;Zhi-Chun and Jian-Xiu 2008;Palacios-Vargas and Deharveng 2014;Smolis and Deharveng 2015;Luo and Palacios-Vargas 2016;Ji-Gang et al. 2018). Nevertheless, knowledge on global diversity of the subfamily is still insufficient and far from complete as many areas, i.e. the Middle East, North Africa, New Guinea or Central Asia, are poorly surveyed in this respect.
An examination of an exceptionally-rich material of Neanurinae from north-western Iran (Provinces: Gilan, Golestan, Kermanshah, Mazandaran, North Khorasan, Semnan and West Azerbaijan), collected in the early 1970s by Antoine Senglet and loaned for the presented studies by Peter J. Schwendinger (curator of the Muséum d'histoire naturelle in Geneva, Switzerland), has revealed seven unknown species of this subfamily. Their detailed and illustrated descriptions are provided with new records of several other known species classified to Neanurinae.

Materials and methods
The specimens were cleared in Nesbitt's fluid, subsequently mounted on slides in Swan's medium and studied using a Nikon Eclipse E600 phase contrast microscope. Figures were drawn with a camera lucida and prepared for publication using Adobe Photoshop CS3.
The whole material, types as well as the other material, is deposited in the Muséum d'histoire naturelle in Geneva, Switzerland.

Abbreviations
General morphology:
Remarks. Due to the general appearance, dorsal and ventral chaetotaxy, E. agnieskae sp. nov. strongly resembles E. reticulata (Axelson, 1905), Holarctic and circumboreal species occurring in tundra, boreal and temperate biotopes of northern Europe (Scandinavian Peninsula), north-eastern Asia and North America (Smolis et al. 2011). Nevertheless, these species can be easily distinguished from each other by the set of characters: size of the eyes (expressed by the ratio of anterior eye diameter and diameter of base of chaeta Ocm, in agnieskae 2:1, in reticulata 1:1 or 5:4), the number of lateral labial chaetae (in agnieskae three, in reticulata four), the length of chaetae Ocp and A on the head (in agnieskae, equal in length, in reticulata chaeta Ocp, longer than chaeta A), the presence of tubercle Di on Th. I (in agnieskae, present and fused with De, in reticulata, absent), the location of chaeta De2 on Abd. I-III (in agnieskae, connected with tubercle De, in reticulata, free), the location of chaeta s on Abd. I-III (in agnieskae, the line of chaetae De1-chaeta s parallel to the dorsomedian line, in reticulata, not parallel) and the length of chaeta Di1 on Abd. IV (in agnieskae, distinctly shorter than chaeta Di1 on Abd. III, in reticulata, longer or equal to chaeta Di1 on Abd. III). Tubercles Dl and (L+So) on head with 6 and 8 chaetae, respectively. Tubercles Di on Th. I present. Tubercles De on Th. II and III with 3 and 4 chaetae, respectively. Tubercles L on Abd. III and IV with 3 and 6 chaetae, respectively. Abd. IV and V with 8 and 3 tubercles, respectively. Furcal rest without mi. Claw with inner tooth. Tibiotarsi with chaetae B4 and B5 rather short.
Legs. Chaetotaxy of legs as in Table 6. Claw with internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 relatively short and pointed (Fig. 26).
Remarks. Morphologically, E. annae sp. nov. is strongly reminiscent of E. persica Smolis, Kahrarian, Piwnik & Skarżyński, 2016, taxon described from Kermanshah Province in northern Iran (Smolis et al. 2016a). Nevertheless, the new species can be easily recognised by several characters, including: the absence of chaeta C on the head (in persica present), the presence of 6 chaetae Dl on the head (in persica 5), wide and short buccal cone (in persica narrow and long), chaetae E on the head connected with tubercle Af (in persica free), chaetae De2 and De3 on Th. II-III, connected with  (Smolis et al. 2007;Smolis and Kuznetsova 2018). These species differ, however, in a number of details: the shape of the buccal cone (in annae, wide and short, in dentifera and dobrolyubovae, narrow and relatively long), the presence of chaeta C on the head (in annae, absent, in dentifera and dobrolyubovae, present), the presence and location of chaeta E on the head (in annae, present and connected with tubercle Af, in dentifera, present and free, in dobrolyubovae, absent), the number of chaetae (L+So) on the head (in dentifera, 10 chaetae, in annae and dobrolyubovae, 8 chaetae), the presence of tubercle Di on Th. I (in annae, present, in dentifera and dobrolyubovae, absent), the location of chaetae De3 on Th. III and Abd. I-III (in annae, connected with tubercle De, in dentifera and dobrolyubovae, free), the presence of male ventral organ (in annae and dentifera, absent, in dobrolyubovae, present) and the presence of cryptopygy (in annae, present, in dentifera and dobrolyubovae, absent). Tables 7-9 Type material. Holotype: female on slide, Iran, Gilan Province, Paresar, tree holes, leaves, sifting, 2.VII.1973, leg. A. Senglet, sample 7310. Paratypes: 3 females and male on slide, same data as holotype.
Diagnosis. Habitus typical of the genus Endonura. Dorsal tubercles present. 2+2 large pigmented eyes. Buccal cone relatively long, labrum nonogival. Head with chaetae B, C and D. Chaeta O absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with 5 and 7 chaetae, respectively. Tubercles Di on Th. I absent. Tubercles De on Th. II and III with 3 and 4 chaetae, respectively. Tubercles L on Abd. III and IV with 2 and 4 chaetae, respectively. Abd. IV and V with 8 and 3 tubercles, respectively. Furcal rest without mi. Claw with inner tooth. Tibiotarsi with chaetae B4 and B5 long.
Legs. Chaetotaxy of legs as in Table 9. Claw with internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 relatively long and pointed (Fig. 33).
Remarks. Since E. schwendingeri sp. nov. is characterised by chaetotaxic features unknown in other members of the genus, for example, the absence of chaetae A and Ocp on the head, its closer affinities with other Endonura species are currently uncertain and hard to assess. However, taking into account the weak development of tuberculation, delicate buccal cone and the presence of well-developed male ventral organ, the new species seems to be most similar to E. quadriseta Cassagnau & Péja, 1979, a form shortly described from Greece (Cassagnau and Péja 1979), but recently re-described, based on types and a new material from the Crimea (Smolis et al. 2007). Nevertheless, besides characters mentioned above, these taxa differ in numerous features: the number of lateral labial chaetae (in schwendingeri, three, in quadriseta, four), the presence of chaetae C and O on the head (in schwendingeri, absent, in quadriseta, present), the number of chaetae (L+So) on the head (in schwendingeri, 7, in quadriseta, 9), the number of chaetae Dl on the head (in schwendingeri, 5, in quadriseta, 6), the number of chaetae L on Abd. III and IV (in schwendingeri, 2 and 4, in quadriseta, 4 and 7) and the presence of an internal tooth on claws (in schwendingeri, present, in quadriseta, absent).   (Figs 42, 43).
Legs. Chaetotaxy of legs as in Table 12. Claw without internal tooth (Fig. 49). On tibiotarsi, chaeta M present and chaetae B4 and B5 relatively long and pointed.  ). However, these species differ in numerous characters, including the number of lateral labial chaetae (in breviseta, four, in persica, three), the presence of chaetae C on the head (in breviseta, present, in persica, absent), the number of chaetae (L+So) on the head (in breviseta, 9, in persica 8), the presence of chaetae Dl3 on the head (in breviseta, present, in persica, absent), the presence of microchaetae on furca rudimentary (in breviseta, absent, in persica, present) and the presence of cryptopygy (in breviseta, present, in persica, absent). Additionally, male ventral organ in D. breviseta sp. nov. is built of thickened and forked chaetae on Abd. V only (in persica, also on Abd. III, IV and VI).  1.45 mm). Colour of the body bluish-grey. 2+2 large black eyes, in a typical arrangement for the genus (Fig. 53).  (Figs 53,  60). Mesochaetae similar to ventral chaetae, thin, smooth and pointed. Microchaetae similar to mesochaetae, but clearly shorter (Figs 53, 60). S-chaetae of terga thin, smooth and short, notably shorter than nearby macrochaetae (Figs 53, 57, 60).

Deutonura sengleti
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant. III-IV as in Fig. 54 and Table 14. S-chaetae of Ant. IV long and relatively thin, S3 notably longer than others, sensillum sgd of medium size and straight (Fig. 54). Apical vesicle distinct, trilobate. Ventral chaetotaxy of Ant. III as in Fig. 55 and Table 14.
Legs. Chaetotaxy of legs as in Table 15. Claw without internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 of medium size and pointed.
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant. III-IV as in Fig. 64 and Table 17. S-chaetae of Ant. IV long and relatively thin, S3 notably longer than others, sensillum sgd of medium size and straight (Fig. 64). Apical vesicle distinct, trilobate. Ventral chaetotaxy of Ant. III-IV as in Fig. 65 and Table 17.
Legs. Chaetotaxy of legs as in Table 18. Claw without internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 of medium size and pointed.
Remarks. Since juveniles (beginning from the first instar) of the subfamily Neanurinae are characterised by the complete chaetotaxy of the head, thorax and abdomen, we decided to describe the new species despite having only one specimen of the second instar. D. iranica sp. nov. runs in the most recent key to Deutonura species  to D. gibbosa Porco, Bedos & Deharveng, 2010, a form common and widespread in southern France (the Alps and Jura), Switzerland, Italy and Slovenia (Porco et al. 2010). Both species are readily distinguished from most members of the genus by the presence of very prominent and conspicuously bilobed tubercle (Di+Di) on the penultimate abdominal segment. This unique character is additionally associated with the specific chaetotaxic arrangement of chaetae Di, with their shift backwards. D. iranica sp. nov. can be easily separated from D. gibbosa by the presence of white body colour (in gibbosa deep to light blue), the presence of 7 chaetae on cephalic tubercle (L+So) (in gibbosa, 8-9 chaetae), the presence of cephalic chaetae Ocp equal chaetae A (in gibbosa, chaetae Ocp distinctly longer than A) and the presence of 4 lateral labial chaetae (in gibbosa, 3 chaetae).  (Fig. 75).
Remarks. No doubt, the new species is the third member of the remarkable Neanurinae genus Paravietnura Smolis & Kuznetsova, 2018 described recently from the Caucasus (Smolis and Kuznetsova 2018). Paravietnura rostrata sp. nov. seems to be the closest to P. notabilis Smolis & Kuznetsova, 2018; however, it can be easily separated from the mentioned species because of the reduction of its cephalic chaetotaxy (in rostrata, chaetae G and Ocp absent, in notabilis, present), extremely elongated labrum, which is well visible from above (in notabilis, feebly elongated and practically invisible from above), absence of prelabral chaetae (in notabilis, 2 chaetae present), the presence of 1+1 chaetae De on Th. I (in notabilis, 2+2 chaetae present), the absence of chaetae Di3 on Th. (in notabilis, present), reduction of the number of chaetae De on Th. II and III (in rostrata, 1+s chaetae, in notabilis, 2+s and 3+s chaetae, respectively), the absence of chaetae De2 and De3 on Abd. I-III (in notabilis, present), the fusion of tubercles Di on Abd. IV (in notabilis, not fused) and the presence of 1 chaeta Di on Abd. V (in notabilis, 3 chaetae Di present). Note. Similarly to the previous species, C. persica was known exclusively from the Elburz Mts. in Golestan Province (Smolis et al. 2012). The outlined records, from provinces West Azerbaijan, Mazandaran, Semnan and North Khorasan, shows that this form seems to be quite common and widespread in north-western Iran. Note. Until now, the species was known from its type locality only: Hezarjarib Forest in region Neka in Mazandaran Province .
Secondly, in terms of species richness, this fauna should be treated even today as very rich. Especially, the Hyrcanian forest, where sixteen species of the subfamily were noted, seems to be not only a national but also a regional hot spot. The observed situation, however, may not be especially surprising as this huge and diversified area covers almost one million hectares and ranges from west to east through five Iranian Provinces: Ardabil, Gilan, Mazandaran, Golestan and North Khorasan. In addition, this forest is a worldwide and commonly-known refuge for many iconic and spectacular mammals, i.e. the Persian leopard Panthera pardus ciscaucasica, trees, i.e. the Persian ironwood Parrotia persica, the Caspian locust tree Gleditsia capsica and insects, i.e. the longhorn beetle Parandra caspia, the red flat beetle Cucujus muelleri (e.g. Sagheb-Talebi et al. 2014;Mayvan et al. 2015a;Müller et al. 2015;Bussler 2017).
Finally, current and especially future knowledge (many regions of Iran still remain unexplored, see Shayanmehr et al. 2013, Fig . 2) of the Iranian Neanurinae fauna could shed light on key issues such as its origin and relationship with fauna of neighbouring regions. For example, the similarity of Iranian fauna to that of the Caucasus (presence of genera Paravietnura and Persanura) and the east Mediterranean region (presence of Protanura papillata and genus Cryptonura) should already be underlined.