A striking new genus and species of troglobitic Campodeidae (Diplura) from Central Asia

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A striking new genus and species of troglobitic Campodeidae (Diplura) from Central Asia

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A striking new genus and species of troglobitic Campodeidae (Diplura) from Central Asia
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47 A striking new genus and species of troglobitic Campodeidae (Diplura) from Central Asia Alberto Sendra 1,2 Boris Sket 3 Pavel Stoev 4,5 1 Grupo de Investigacin de Biologa del Suelo y de los Ecosistemas Subterrneos, Departamento de Ciencias de la Vida, Facultad de Biologa, Ciencias Ambientales y Qumica, Universidad de Alcal, E-28871 Alcal de Henares, Madrid, Spain 2 Servei de Patrimoni Histric, Ajuntament de Valencia, E-46008 Valencia, Spain 3 Oddelek za biologijo, Biotehnika fakulteta, Univerza v Ljubljani, p.p. 2995, 1001 Ljubljana, Slovenia 4 National Museum of Natural History, 1, Tsar Osvoboditel Blvd., 1000 Soa, Bulgaria 5 Pensoft Publishers, 12 Prof. G. Zlatarski St., 1700 Soa, Bulgaria Corresponding author: Alberto Sendra ( alberto.sendra@uv.es ) Academic editor: O. Moldovan |Received 21 June 2017|Accepted 3 August 2017|Published 21 September2017 http://zoobank.org/9294E54B-C84C-41DE-8C7B-2313FC24419E Citation: Sendra A, Boris Sket B, Stoev P (2017) A striking new genus and species of troglobitic Campodeidae (Diplura) from Central Asia. Subterranean Biology 23: 47. https://doi.org/10.3897/subtbiol.23.14631 Abstract A striking new genus and species of Campodeidae (Diplura), Turkmenocampa mirabilis Sendra & Stoev, gen.n., sp.n. found in Kaptarhana cave in Eastern Turkmenistan is described. is represents the rst record of Diplura from Central Asia and also the rst terrestrial troglobiont found in Turkmenistan. e new taxon shows several unique characters such as the lack of crests on the telotarsus, the presence of a side-shoot process and the shape of barbs on the ventral side of the laminar telotarsal processes hitherto unknown in other members of this family. Although T. mirabilis is tentatively placed in the subfamily Plusiocampinae, its true anities remain uncertain. e new nding provides further support to the importance of Kaptarhana as a refuge for a number of endemic invertebrates. Keywords Turkmenistan, Koytentag Mountain, Turkmenocampa mirabilis, identication key, Plusiocampinae, cave fauna Subterranean Biology 23: 47 (2017) doi: 10.3897/subtbiol.23.14631 http://subtbiol.pensoft.net Copyright Alberto Sendra et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0) which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. RESEARCH ARTICLE Subterranean Biology Published by The International Society for Subterranean Biology A peer-reviewed open-access journal

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48 Introduction Central Asia is a geographical region which covers an area of approximately 4 million square kilometres stretching from the Caspian Sea in the west to the border of China in the east and from the southern borders of Russia in the north to the northern borders of Iran, Afghanistan and China in the South. is vast geographical area is composed of the territories of ve independent countries, the former Soviet republics of Kazakhstan, Uzbekistan, Tajikistan, Kyrgyzstan and Turkmenistan. It is also occa sionally referred to as Middle Asia, with other mainly dry and ecologically similar parts of Afghanistan, Pakistan, Mongolia, and at times Xinjiang and Tibet in western China and southern Siberia in eastern Russia are also included in this denition. e complex political history and highly diverse geography and diverse landscape, the latter in cluding high mountains (Tian Shan), deserts (Karakum, Kyzylkum, Taklamakan) and steppes, as well as the comparatively low level of economic development and transport networks, signicantly hampered the zoological explorations in the area. Diplura is one of the four classes that comprise the subphylum Hexapoda. Accord ing to Koch (2009) and Zhang (2013), at present it includes 976 extant and 1 fossil species. Despite their worldwide distribution, diplurans are virtually unknown from Central Asia. A few species have hitherto been recorded from the adjacent to Central Asian countries, but most records refer to species found distant from the region or even in other zoogeographical realms. e Japygidae genus Kohjapyx with three spe cies, including the troglobiotic species Kohjapyx lindbergi Pags, 1962 from a cave near Kabul have been described from Afghanistan (Pags 1953, 1962; Paclt 1958). In a recent study on the Campodeidae of North Iran, Azadbakhsh and Nozari (2016) recorded the soil-dwelling species Campodea ( Dicampa ) sprovierii Silvestri, 1932 and Campodea ( Campodea ) fragilis Meinert, 1865 from the provinces Mazandaran and Al burz. Even in other, better explored areas in Asia, the knowledge is rather poor. For in stance, the cave fauna of mainland Asia is known to harbour only seven species (Bareth and Cond 1972; Cond 1956b, 1993; Chevrizov 1978; Ferguson 1997). Simlacam pa clayae Cond, 1956 is known from three caves in Punjab, India (Cond 1956b). Plusiocampa ( Didymocampa ) lipsae Cond, 1993 is recorded from several caves in the south of China (Cond 1993). From caves in the Russian Far East, Primorskij kraj (or Primore) Chevrizov (1978) described two genera Plutocampa and Pacicampa, with respectively 3 and 2 troglomorphic species. Furthermore, Ferguson (1997) reported a new species of Pacicampa (Diplura: Campodeidae) from a cave in China. Given the general shortage of dipluran material and the low rate of sampling in almost all parts of Asia, many new species of subterranean diplurans are expected to be found in the near future, especially when large collections such as that of Dr. Louis Deharverg (MNHN) from Chinese caves have been studied. In this paper, a remarkable new genus and species of the dipluran family Campo deidae, found from Kaptarhana cave in South East Turkmenistan, is described. is represents the rst formal record of the subclass from the entire Central Asia and also the rst terrestrial troglobiont found in Turkmenistan.

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49 e true anities of the new taxon remain uncertain as it departs signicantly from all the currently established campodeid genera. It is tentatively placed in subfam ily Plusiocampinae but this may change in future when combined morphological and molecular phylogenetic analysis of Diplura has been undertaken. e exploration of Kaptarhana cave begun at the end of the summer of 1963 when a group of speleologists from Moscow led by V. Andreyev visited the cave and collected some foraminifers, isopods and harpacticoids from the lake. In November 1963, intrigued by these interesting ndings, the cave was visited by the leading (at that time) Soviet biospeleologist S. Ljovuschkin (see Birstein and Ljovuschkin 1965). Ljovuschkin later (1969) published short report on the fauna of the cave mentioning the barklice Psyllipsocus ramburii Selys-Longchamps, 1872 (Insecta: Psocodea) an undetermined species of Pseu doscorpiones and Oniscoidea. Furthermore, in 1972 Starobogatov (1972) described the cave hydrobiid gastropod Pseudocaspia ljovuschkini Until the study of Pavel Stoev and Bo ris Sket in 2015, almost no other biospleological work was carried out in the cave. e new sampling revealed that the cave is also inhabited by spiders, springtails, parasitic ies and cryptophagid beetles. ere is also a large colony of horseshoe bats, Rhinolophus bocharicus. Material and methods Sampling methods e material was collected by Pavel Stoev and Boris Sket from the cave Kaptarhana (see details below) in the course of a rapid speleobiological assessment of the caves of Koy tendag State Nature Reserve of Turkmenistan undertaken in 2015. e mission was carried out under the Memorandum of Understanding between the State Committee on Environment Protection and Land Resources of Turkmenistan and the Royal Soci ety for the Protection of Birds to protect birds and other biodiversity in Turkmenistan. For sampling, pitfall traps, with Ethylene glycol and smelly cheese as bait, were set along the main gallery of the cave, mostly in humid places, in close proximity to large boulders and guano heaps. Pitfall traps were exposed for several days in the last week of May. Subsequently, all the captured animals were transferred to a container with 95% alcohol solution and properly labelled. Despite the fact that both collectors spent 7 hours altogether in the cave, no specimens were found by visual observations, all speci mens being caught by pitfall trapping. e cave was very spacious, with large boulders and passages at dierent levels, making the process dicult for the collection and dis covery of cryptic animals (such as diplurans) by methods other than pitfall trapping. Material processing and identication Specimens were washed in distilled water and inserted between slides and glass cov erslips to be examined under a phase-contrast optical microscope (Leica DMLS) us

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50 ing Marc Andr II solution. e illustrations were made with a drawing tube and the measurements were taken with an ocular micrometer. For measuring the body length, the specimens were mounted in toto and were measured from the base of the frontal process distal macrochaetae to the abdomens supra-anal valve. For measurement of the sensilla and for examination of some minute anatomical parts, six specimens were coat ed with palladium-gold and studied in a Hitachi S-4100 scanning electron microscope. e morphological descriptions and abbreviations used in this paper follow Cond (1956a). Although its function is still unknown, the term gouge sensilla is used for the concavo-convexly shaped sensilla located on the antennae (as described by Bareth and Cond 1981). For the position of macrosetae on the occiput, ma, la and lp Wygodz insky (1944) was followed. Abbreviations NMNHS National Museum of Natural History, Soa. For notal macrosetae : ma medial-anterior, la lateral-anterior and lp lateral-poste rior; for urotergal macrosetae: post: posterior. Results Taxonomy Turkmenocampa Sendra & Stoev, gen. n. http://zoobank.org/206FD93E-D986-4C48-BA78-6D0A49442401 Type species. Turkmenocampa mirabilis Sendra & Stoev, sp. n. Etymology. Turkmenocampa is a composite name comprising Turkmeno-refer ring to the type locality and the sux -campa traditionally used in Campodeidae taxonomy. Gender: feminine. Diagnosis. Head with a frontal process without tuberculate setae (Fig. 1); men tum and submentum short (Fig. 2). Cupuliform organ shallow, having three types, large oval, smaller oval and tree shaped, olfactory chemoreceptors (Figs 8). orax with 4+4 ( ma, la, lp 2,3 ) macrosetae on pronotum and mesonotum, 3+3 ( ma lp 2,3 ) on metanotum (Fig. 3). Femur having one dorsal macroseta; tibia with one ventral mac roseta. Claws simple, with a medial external expansion with laminar lateral processes covered with long barbs on the ventral side (Figs 17). Abdomen entirely lacking lateral-anterior macrosetae, with 1+1 to 4+4 post macrosetae on I to VII tergites (Fig. 4). Sternal macrosetae: I sternite: 7+7; II-VII sternites: 4+4 (Fig. 7), VIII sternite: 1+1. Sexual secondary characters almost absent; a 1 glandular setae present in both sexes in the distal part of subcylindrical appendage (Figs 5).

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51 Figures 1. Turkmenocampa mirabilis Sendra & Stoev, sp. n. 1 Dorsal view of the frontal process and right side of the head, holotype 2 Head, ventral view, E23 female paratype. Scale bars: 0.2 mm. 1 2

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52 Figures 3. Turkmenocampa mirabilis Sendra & Stoev, sp. n. 3 Pro-, mesoand metanotum, left side, holotype 4 Urotergites I-IX, right side, holotype. Scale bars: 0.2 mm 3 4

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53 A key to the genera of Plusiocampinae Paclt, 1957 1(2) Claws with lateral crests .............................................................................. 3 2(1) Claws without lateral crests ....................................................................... 13 3(4) Telotarsal processes setiform ........................................................................ 5 4(3) Telotarsal processes lacking or laminar barbed ............................................. 9 5(6) Telotarsal processes pubescent ....................... Hystrichocampa Cond, 1948 6(5) Telotarsal process smooth ............................................................................ 7 7(8) 4+4 macrasetae on II-VII urosternites, 1+1 macrosetae on VIII urosternite .. ............ Condeicampa Ferguson, 1996 and Plusiocampa ( Dydimocampa ) sinensis Silvestri, 1931 8(7) Not less than 5+5 macrosetae on II-VII urosternites and 2+2 macrosetae on VIII urosternite ................................................ Plusiocampa Silvestri, 1912 9(10) Telotarsal processes lacking ............................ Plutocampa Chevrizov, 1978 10(10) Telotarsal processes laminar barbed ........................................................... 11 11(12) Telotarsal processes broad ............................................................................. ....... Cestocampa Cond, 1956; Vandelicampa Cond, 1955; Patrizicam pa Cond, 1956 and Plusiocampa ( Didymocampa ) lipsae Cond, 1993 12(11) Telotarsal processes narrow ................................. Simlacampa Cond, 1956 13(14) Simple claws, without telotarsal processes, medial-intermediate and lateral-in termediate mesoand metanotal macrosetae ....... Silvestricampa Cond, 1950 14(13) Claws with a side-shoot sharp, laminar and telotarsal processes, without me dial posterior mesoand metanotal macrosetae .... Turkmenocampa gen. n. Turkmenocampa mirabilis Sendra & Stoev, sp. n. http://zoobank.org/DD725FD0-83CD-45F6-994C-A4C103CB9592 Material examined. Holotype: female, 5.8 mm, Turkmenistan, Lebap Province, Koytendag District, v. Gurshun Magdanly (=Svintsovyi rudnik), cave Kaptarhana, N37' E66', alt. 550 m asl, numerous gypsum boulders, guano heaps, cave lakes, pitfall traps with a bait, 24.V.2015, P. Stoev, B. Sket leg. preserved in slide with Marc Andr II, deposited in the NMNH labelled E01. Paratypes: 16 females and 11 males, same locality, date and collectors, preserved in slide with Marc Andr II, deposited in the NMNHS (labelled E02 to E21) and in A. Sendra personal collection (labelled E22 to E28). Etymology. mirabilis is a Latin adjective meaning unusual, amazing, wonderful, remarkable. e specic epithet refers to the unique micro-sensilla in the cupuliform organ which resemble sponges and micro-corals. Description. Body : length of males 3.2.9 mm, females 3.5.2 mm (Table 1). Epicuticle smooth; body with long, thin and smooth clothing setae (Figs 3) which are much shorter and less numerous on the head (Fig. 1); micro-sensilla present on the labial palps and appendages of the rst urosternite (Figs 16 and 19).

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54 Table 1. Body measurements of Turkmenocampa mirabilis. (-) Absent or dicult for observation or measurement trait. Specimen # Sex Length (mm) Length of antennae (mm) Number of antennomeres Leg III length (mm) Number of a1 glandular setae on one appendage E22, paratype 3.2 1.9 33 1.4 E12, paratype 3.3 1.8 33 1.3 8 E28, paratype 3.4 1.7 E17, paratype 3.5 1.6 9 E24, paratype 3.7 1.7 E08, paratype 3.8 1.8 12 E27, paratype 4.0 2.3 23 E11, paratype 4.3 2.2 E14, paratype 4.3 2.1 26 E07, paratype 4.5 2.0 22 E18, paratype 4.7 2.4 29 E20, paratype 4.7 3.1 33 2.3 13 E16, paratype 4.8 3.0 31 2.3 E13, paratype 4.9 2.6 32 2.0 15 E03, paratype 4.9 2.2 25 E19, paratype 4.95 2.5 E15, paratype 5.0 2.7 20 E06, paratype 5.1 2.3 20 E04, paratype 5.2 2.5 15 E21, paratype 5.2 3.6 30 2.3 E26, paratype 5.2 2.4 15 E23, paratype 5.3 2.3 10 E10, paratype 5.6 3.1 31 2.5 21 E01, holotype 5.8 2.7 17 E25, paratype 5.8 4.2 32 2.6 19 E09, paratype 5.9 3.9 33 2.6 E02, paratype 6.2 4.0 33 2.6 18 Head : Antennae shorter than body; composed of 30 antennomeres (Table 1). Sensillum of the third antennomere subcylindrical, slightly swollen, similar in size and shape to the maxilla and labial palps (Fig. 2); sensillum located in ventral posi tion between macrosetae d and e middle antennomeres in adults 2.5 times longer than wide. Gouge sensilla (Fig. 13) 18 m long, with their outside surface lightly grooved and with a pointed apex. Gouge sensilla distributed in a single distal whorl of 6 sensilla on each medial and distal antennomere. Last antennomere is twice the size of the penultimate, with a noticeable shallow cupuliform organ having a wide opening of 25 m of diameter measuring 1/12 th of its length (Fig. 8). Cupuliform organ tightly packed with two types of unknown sensilla and having three dierent types of olfactory chemoreceptors all covered with pores: about fourteen type I, two oviform structures of 7 m long; about six type II, two oviform structures of 3.5 m long and about

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55 Figures 5. Turkmenocampa mirabilis Sendra & Stoev, sp. n. 5 Urosternite I of male, left side, E03 male paratype 6 Urosternite I of female, left side, E02 female paratype; 7 Urosternite VII, left side, E02 female paratype. Abbreviations: apical ( ap ), subapical ( sap ) and medio-ventral ( mv ) setae, glandualr a1 setae. Scale bars: 0.1 mm. 6 7 5

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56 Figures 8. Turkmenocampa mirabilis Sendra & Stoev, sp. n. 8 Cupuliform organ of the latest anten nomere in an adult specimen 9 Cupuliform organ of the latest antennomere in an adult specimen with all olfactory chemoreceptors visible after an articial outpouching of the organ presumably produced by the ethylene glycol in the trap (type I large oval, type II, small oval and type III, tree olfactory chemoreceptors) 10 Type I large oval olfactory chemoreceptor in the cupuliform organ. 8 10 9 twenty type III, tree-shaped structures with branches that overhang the types I and II sensilla (Figs 8). Frontal process slightly developed (Fig. 1), with one long apical and two short posterior setae with 1 tiny distal barbs. ree macrosetae along the line of the insertion of antennae and x setae, in female holotype length ratios: anterior = 0.7, posterior = 0.6, intermediate = 1, x = 0.5; all macrosetae with a few thin barbs along the distal one-third. Occiput of the dorsal head with 6+6 macrosetae, including 3+3 ma, la, lp macrosetae (Fig. 1). Labium (Fig. 2) with a short submentum ( sm ) with 2+2 long macrosetae barbed along the distal half and shorter mentum ( m ) with 4+4 short macrosetae with a few distal barbs. Typical labial palps ( lp ) and palpiforms processes ( pp ). Labial palps covered by more than one hundred neuroglandular setae ending truncated with radial micro-crests on the top (Figs 14); nearby are observed a few micro-sensilla (Fig. 16) adjacent to the row of a few banal setae and the labial sensillum. orax : Slightly elongated thoracic nota. Distribution of macrosetae (Fig. 3): pronotum and mesonotum with 1+1 ma 1+1 la 2+2 lp 2,3 and metanotum with 1+1 ma, 2+2 lp 2,3 All macrosetae long, with thin barbs along the distal half to four-fths; marginal setae longer than clothing setae and with a few distal barbs. Legs slightly

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57 12 13 15 11 14 16 Figures 11. Turkmenocampa mirabilis Sendra & Stoev, sp. n.: 11 Type II small oval olfactory chem oreceptor in the cupuliform organ 12 Type III tree olfactory chemoreceptor in the cupuliform organ 13 Gouge sensilla on the lateral external side of a medial antennomere in an adult specimen (indicated with arrows) 14 Neuroglandular setae of the labial palp in an adult specimen 15 Tips of some neurog landular setae on the labial palp in an adult specimen 16 Microsensillum on the labial palp in an adult specimen (indicated with arrows). elongated, metathoracic legs reaching abdominal segment VIII. Femur IIIII with one long dorsal macrosetae barbed along four-fths. One short ventral macrosetae on tibia I-III well barbed almost from its base. Calcars well barbed from base to tip with long barbs. Tarsus with two ventral rows of setae covered by long thin barbs

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58 Figures 17. Turkmenocampa mirabilis Sendra & Stoev, sp. n., telotarsal process of the metathoracic leg in an adult specimen: 17 Lateral view 18 Lateroventral view. 18 17 on the medial portion. Distal tarsus with smooth subapical setae or with a few thin distal barbs. Subequal claws curved in the medial distal comprising a thick base and a remarkable sharp-ending external expansion or side-shoot, the whole body of the claws with ne longitudinal and semi-transversal striate laminar telotarsal processes and only ventral face covered with long barbs with tip ending in a hook-shape along Figure 19. Turkmenocampa mirabilis Sendra & Stoev, sp. n.: Apex appendage of the rst urosternite in an adult female showing some a 1 glandular setae.

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59 the laminar processes and with a at expansion-shape at the end of the laminar pro cesses (Figs 17). Abdomen : Abdominal distribution of macrosetae (Fig. 4): 1+1 post 1 macrosetae on tergites I-II, 2+2 post 1,2 on III, 4+4 post 2 on IV-VII, 5+5 post on VIII and 7+7 post IX, all long and barbed on the distal two-thirds. Urosternite I with 7+7 (7+8 in three para types) well developed macrosetae barbed on the distal two-thirds; II-VII with 4+4; VIII with 1+1 (2+1 in paratype female 5 mm, E05) (Figs 5). Styli with a long basal tooth with barbs, apical, subapical and medio-ventral setae well barbed (Fig. 7). One complete cerci isolated: 6.7 mm long, with 9 elongated articles plus base, each article progressively longer and covered with long macrosetae with thin tiny barbs along the distal one-third. Sexual secondary features : Male urosternite I (Fig. 5) with two subcylindrical ap pendages, each bearing 8 a1 glandular setae in paratype E12 (a young male, 3.3 mm long) and up to 29 a1 in paratype E18 (adult male, 4.7 mm long) (Table 1). Female urosternite I (Fig. 6) with two subcylindrical appendages thinner than in the males, each bearing 9 to 20 a1 glandular setae (see Table 1 and Fig. 19) Description of Kaptarhana cave Turkmenocampa mirabilis is hitherto known only from the cave Kaptarhana situated near the village Gurshun Magdany, Koytendag District, Lebap Province, Turkmeni stan (Figs 20, 21). Kaptarhana (also spelt Kaptar-Khana) means house of pigeons in Turkmen language as its entrance is used by pigeons for nesting. e cave is located at the foot of Koytentag Mountain (also known as Koytendag, Ktendag, Kugitang, Koitendag, Kugitangtau, Kugitang-Tay, Kugitangtou) in the northern part of Hojapil Sanctuary, on the left bank of the Koyten river. e cave is approximately 450 m long and is situated in Late Jurassic gypsum (Birstein and Ljovuschkin 1965, Ljovuschkin 1969). ere are two main galleries starting from the entrance, one orientated west (160 m long) and the second, approximately 300 m long, in a northeastern direction. Part of the cave is occupied by lakes with saline water. According to Birstein and Ljo vuschkin (1965), the salinity is 11.68 and the pH is 7.8. e same authors provide a detailed chemical analysis of the water comparing it with the neighbouring river Amu Darya, Aral and Caspian seas and the World Ocean. e ionic composition of the lakes shows a high similarity to that of the ocean water and little resemblance to those of the neighbouring water basins. Additional support to the relict origin of the lakes comes from their rich foraminiferan, harpacticoid, isopod and gastropod fauna comprising a number of endemic species of marine origin. A list of species known from Kaptarhana Aquatic : Foraminifera: Entzia macrescens (Brady, 1870) =? Entzia zernovi (Schmal hausen, 1950), =? Entzia polystoma (Bartenstein & Brand, 1938) subsp. caspica Mayer,

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60 Figure 20. Map of Turkmenistan with location of the cave Kaptarhana (Red triangle). Map credit: Atamyrat Veyisov. 1974 (see Filipescu and Kaminski 2011), Birsteiniolla macrostoma Yankovskaya & Mikhalevich 1972, Trochamminita sp., Miliamina sp. Nematoda: Oncholaimidae spp.; Gastropoda: Hydrobiidae: Pseudocaspia ljovuschkini Y.I. Starobogatov, 1972; Isopoda: Microcharon halophilus Birstein & Ljovuschkin, 1965; Maxillopoda: Harpac ticoida: Halectinosoma abrau (Krichagin, 1877), Ectinosoma sp., Schizopera paradoxa (Daday, 1904), Nitocra sp. Terrestrial: Isopoda: Oniscoidea gen. sp.; Pseudoscorpiones; Araneae (new re cord); Collembolla (new record); Diplura: Turkmenocampa mirabilis ; parasitic Diptera; Coleoptera: Cryptophagidae; Chiroptera: Rhinolophus bocharicus.

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61 Habitat Although Turkmenocampa mirabilis has so far been found only in the larger gallery of the cave, some 200 m inside the cave, it might well be that it also inhabits the oth er main passage of the cave. e species is a troglobiont, all records deriving from the aphotic zone of the cave. No specimens were however observed during the exploration of the cave, those that were trapped being found in humid locations, rich in guano. Discussion Phyletic anities e classications of Campodeidae (Cond 1956a; Paclt 1957) and Diplura (Pags 1959) are rather outdated and badly in need of revision. Only some of the higher taxa proposed in Campodeidae seem natural as they appear to receive geographical support. is is particularly so for the diplurans from the Holarctics but, outside this region and towards its edges, most phylogenetic groups appear more or less articial. e traits currently applied in the taxonomy of the group are of little help in clarifying the natural grouping and for developing a sound phylogenetic hypothesis. e shape and distribution of macrosetae and setae, the shape and complexity of pretarsal struc tures, as well as the secondary sexual characters, are the major taxonomic traits used for classifying the existing campodeid taxa. Molecular methods have only recently been applied to the group (Sendra et al. 2012) and the data are still insucient for drawing a more robust phylogenetic analysis. Despite all these taxonomic weaknesses in the current classication, the traits demonstrated by Turkmenocampa mirabilis are solid enough to justify the description of a new species and genus within Campodeidae. e new taxon possesses a combination of several features not present in the other genera, one of which the specic morphology of the olfactory chemoreceptor sensilla of the cupuliform organ is unique in the whole family. Plusiocampinae seems to be a paraphyletic taxon with regard to its only diagnostic character the additional macrosetae on the pronotum as suggested by Paclt (1957). Nevertheless, many of its genera can be considered monophyletic. is refers to the gen era Cestocampa Cond, 1956, Condeicampa Ferguson, 1996, Hystrichocampa Cond, 1948, Patrizicampa Cond, 1956, Plusiocampa Silvestri, 1912, Plutocampa Chevrizov, 1978, Simlacampa Cond, 1956 and Vandelicampa Cond, 1956, all of which have lateral crests in their telotarsus. e absence of this important taxonomical trait in Sil vestricampa Cond, 1950 and Turkmenocampa clearly distinguish them from the other Plusiocampinae. With regards to the subfamily position of the new genus, the presence of more than 3+3 macrosetae on pronotum (vs. up to 3+3 in Campodeinae Cond, 1956) and the absence of scales covering part of the body (vs. present as in Hemicampi nae Cond, 1956 and Lepidocampinae Cond, 1956), places T. mirabilis within Plusio campinae. However, the absence of lateral crests in T. mirabilis and all members of genus

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62 Figure 21. Entrance of the cave Kaptarhana. Photo credit: Aleksandr Degtyarev. Silvestricampa the latter being solely known from the Afrotropical realm (Silvestri 1913; Cond 1950), raises doubts about their placement in Plusiocampinae. e high number of macrosetae in Silvestricampa, with 7+7 macrosetae on the pronotum and presence of medial and lateral intermediate macrosetae on mesoand metanotum as well as the absence of telotarsal processes, clearly dierentiate Turkmeno campa from Silvestricampa Close examination of the genera Plusiocampa and Cesto campa, reveals that several species do not match their original diagnoses. is is the case with subgenus Dydimocampa of Plusiocampa dened by Paclt (1957) with the presence of two dorsal femoral macrosetae. e subgenus is known with two species from China (Cond 1993; Silvestri 1931): the soil-dwelling Plusiocampa ( Dydimocama ) sinensis Sil vestri, 1931 and the cave-dwelling Plusiocampa ( Dydimocampa ) lipsae Cond, 1993. eir chaetotaxy show close similarities with T. mirabilis except for the additional mac rosetae on II-VII urosternites present in P. lipsae Furthermore, P. lipsae has laminar telotarsal processes although with a short sternal pubescence, while they are setiform in P. sinensis P. sinensis has clear lateral crests while they are very small in P. lipsae Another allied species, the soil-dwelling Plusiocampa kashiensis from West China (Chou and Chen 1980), was recently transferred from Cestocampa (Sendra et al. 2012). Despite its poor original description, P. kashiensis shares some similarities with T. mi

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63 rabilis in the distribution of macrosetae on the nota and abdomen and also in having barbed laminar telotarsal processes and claws without crests. However, the species can readily be distinguished from T. mirabilis by the short and abundant clothing setae (vs. long and thin in T. mirabilis ) and the lack of extension of the claws or side-shoot (at least not mentioned in its original description). It might well be that P. kashiensis is actu ally a member of Turkmenocampa but, until a new or type material is studied, a formal transfer has not been suggested at this time. is also refers to the genus Anisuracampa Xie & Yang, 1990 which was described from subtropical China (Xie and Yang 1991) and shows morphological similarities with Dydimocampa Finally, worthy of special mention is the presence of the latero-outside side-shoot of the claw in T. mirabilis It can be considered as a convergent character as it is known in Metriocampa ( Notocampa ) afra Cond, 1950 and is also present basally in Oreocampa mi nutella (Silvestri, 1918), as well as in Haplocampa Silvestri, 1912. It has never been found in combination with telotarsal processes (Cond 1956a) until the discovery of T. mirabilis. Derived morphological characters, troglomorphies It should be emphasised that all Diplura are without external eyes, although George (1963) presumably gave a light-perceptive function to its lateral sense organs, each one being below the integument in the latero-ventral position in the head. Furthermore, Diplura and Campodeidae, in particular show thin integument with no pigment or sclerotized cuticle. ese traits are in all soiland cave-inhabiting species. Nevertheless, the features which clearly dene the troglobiotic campodeids are: increased body size, elongation of appendages and body, more numerous antennomeres and cercal articles, as well as specialisation of sensory organs. Considering all these features, Turkmeno campa mirabilis is undoubtedly a strict cave-dweller showing slightly elongated body and appendages (including the cercal articles and the antennomeres); and a moderate increase in the number of antennomeres reaching up to 33 and up to 10 elongated gouge sensilla in the medial and distal antennomeres. Furthermore, the species pos sesses three striking features which could also be related to its subterranean living envi ronment (see also Cond 1956a; Sendra et al. 2017). Firstly, the olfactory chemoreceptors within the cupuliform organ, which are usu ally present in troglobiotic campodeids. In T. mirabilis, the shape of these olfactory chemoreceptors have no analogue in any other Campodeidae (Figs 8). All troglobi otic campodeids show an increase in size and complexity of the olfactory chemorecep tors and their surface. Troglobionts have more and larger pores than soil-dwellers (Ju berthie-Jupeau and Bareth 1980). e increase in complexity demonstrates a similar pattern showing a multiplication of tiny folds (or collarets) around a spheroid sensilla (Cond 1956a). In the most complex cases (Bareth and Cond 1984; Cond 1974; Cond and Sendra 1989), these folds have a sheet-like shape, in Plusiocampa dallai Ba reth & Cond, 1984 and Plusiocampa alhamae Cond & Sendra, 1989; or digit-shape, in Campodea ( Paurocampa ) pretneri Cond, 1974.

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64 Inside the cupuliform organ, T. mirabilis has three types of olfactory chemorecep tors, about forty sensilla tightly packed in a shallow cuticular invagination perforated by tiny pores (Figs 8). ese sensilla are produced by microscopic evagination at the bottom of the cupuliform organ producing three dierent types of olfactory chemo receptor sensilla. Type I and II have a wide and very short base, dicult to observe, which increases in size into two oval-shaped structures completely covered by pores. In type I, the oval structures are 7 m long by 5 m wide with pores of 0.1.25 m diameter (Figs 9); in type II, the oval structures are 3.5 m by 3 m with pores of 0.25.35 m (Figs 9, 11). Type III are tree-shaped sensilla covered by ir regular pores (0.05.08 m diameter) that start from the cupuliform organ base with a trunk-shaped structure 4.5 m high and 1.1.4 m wide, that it is divided into 2, 3 or 4 branches of 1.1.6 m long extending into 1-2-3-4 spines (Figs 9, 12). e type III sensilla slightly overhang the types I and II and are mostly (Fig. 8) in the centre of the cupuliform organ surrounded generally by types I and II. us in T. mirabilis, the increase in number, complexity and porous surface in olfactory chemoreceptors sensilla follow another evolutionary path, dierent from the pattern observed in numerous troglobiotic species in Plusiocampa and Cestocampa where these sensilla have been examined (eg., Cond 1956a). e other two remarkable features of T. mirabilis refer to the telotarsus and both could be an adaptation for walking on wet and soft surfaces in subterranean environ ment. e claws are 50 m long and curved only at the distal end where they are also slightly thinner. e whole surface of the claws is marked with ne longitudinal and semi-transversal striate of 0.3 m thickness. At approximately 15 m from the base on the lateral external side of the claw, there is a pointed side-shoot process of 12 m length (Figs 17). If side-shoots of the claws have a similar function to the function of lateral crests present in several troglobiotic species of Plusiocampa, Ce stocampa, Paratachycampa and Juxtlacampa which are usually regarded as adaptations to subterranean lifestyle (see, for example Conde 1956a; Bareth and Pags 1994), then they should also be considered derived traits resulting from the long cave evolution. e third interesting feature is the shape of the barbs (about 120 thin barbs 3 m long) on the ventral side of the laminar telotarsal processes, ending mostly in a hook but in a at extension in the apical barbs (Fig. 17). ese two types of laminar barbs have also been observed in other troglobiotic campodeids (Sendra et al. 2012, 2016) and were considered as an adaptation to facilitate movement on wet surfaces (Sendra et al. 2017). Biogeography e cave fauna of Central Asia is outstanding with its poverty of terrestrial troglobionts (Birstein and Ljovuschkin 1967, Ljovuschkin 1969). Kniss (2001) enumerated from the Central Asian caves altogether 80 species, of which 27 were stygoand troglobionts. However, out of 27 strict cave-dwellers, only the springtail Pseudacherontides stachi (Ljo

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65 vuschkin, 1972), found from the Amir-Temir Cave on the western spur of Zeravshan Range of Uzbekistan, is considered troglobiont (Turbanov et al. 2016b). All others, in cluding one sh, inhabit underground waters. Likewise, in adjacent Iran, the cave fauna comprise only 89 species, of which 16 are strict cave-dwellers. Of these, only three are terrestrial troglobites the spider Trilacuna qarzi Malek Hosseini & Grismado, 2015, the millipede Chiraziulus troglopersicus Reboleira, Malek Hosseini, Sadeghi & Engho, 2015 and the isopod Protracheoniscus gakalicus Kashani, Malek Hosseini & Sadeghi, 2013 (Malek-Hosseini and Zamani 2017). Based on climatic, lithological and soil characteristics, Turkmenistan is divided into thirteen ecological regions. Koytendag Mountains form a region of its own and is characterised by desert landscapes on mountainous relief, highly dissected by ravines, foothills with ridges and cuestas and fan plains. Karst processes are well developed in the region. e average annual temperature is about 17C and annual precipitation is approximately 150 mm (Babaev 1994). e ora contains more than 1,900 spe cies, including 332 endemics (see Rustamov et al. 2009). Lying at the intersection of three biomes the Eurasian high mountains (Alpine and Tibetan), the Irano-Turanian mountains and the Sino-Himalayan temperate forests the area supports a high fau nal and oral diversity with a number of endemic plant, sh and invertebrate species (UNESCO Nomination dossier 2015). Due to its remote location, dicult accessibility and restricted border control, as well as the lack of active speleobiologists in Turkmenistan, the biological aspect of the Koytendag caves has only been marginally studied. Despite the great number of caves in the area (some estimates give 300), until now only the invertebrate fauna of the caves Kaptarhana, Gap-Gotan, Hashym Oyuk and Gulshirin, an unnamed cave near v. Svincovyi rudnik, have been explored from the biological viewpoint (Birstein and Ljovuschkin 1965, Ljovuschkin 1969, Starobogatov 1972, Kniss 2001, Turbanov et al. 2016a, b, c). Kniss (2001) reviewed the existing knowledge in his catalogue Fauna of the caves of Russia and adjacent countries and Turbanov et al. (2016a, b, c) provided a checklist of all cave species known from Russia and the former Soviet republics. Until the present time, terrestrial troglobionts have not been registered in Koytendag. e specic composition of the brackish lake in the cave Kaptarhana and its unique stygofauna comprised of species of marine origin suggest a completely dierent geologi cal history of the cave compared to the rest of the region. It is very likely that the saline waters belong to another hydrographic entity, without connection to the subterranean waters of the neighbouring Koyten and Garlyk areas where the stygofauna is represented by other species such as Troglocobitis starostini Stenasellus asiaticus Bogidiella ruoi Gam marus spp., copepods, etc. (Turbanov et al. 2016 ab, Boris Sket, unpublished). It is noteworthy that the terrestrial fauna of the cave also shows dierences compared to the other caves of Koytendag. e authors attempts to nd T. mirabilis in any of the other caves were unsuccessful despite the fact that the same collecting method (baited pitfall traps) was applied in the cave Gap-Gotan. Furthermore, the ptinid beetle Niptus hololeucus (Faldermann, 1835), which is otherwise very abundant in the Gap-Goutan cave (mostly on porcupine scats), is missing in Kaprahana, where the group is repre

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66 sented by an unidentied species of family Cryptophagidae. e unique character of the fauna of Kaptarhana is supported by the nding of very likely new species of Collembola (L. Deharveng, in progress). It may well be that the existing hydrological barrier between Kaptarhana and the other caves also prevents distribution of terrestrial organisms. Taking into consideration that the caves of Central Asia are poorly studied, the possibility is not excluded that this taxon or new species of Turkmenocampa will be found in future in other caves in Koytendag or in the neighbouring parts of Uzbekistan and Afghanistan. Acknowledgements Pavel Stoev and Boris Sket would like to express their deepest gratitude to Stephanie Ward and Elizabeth Ball (both RSPB) for their overall support during the eld mis sion in Turkmenistan, as well as Nurmuhamet Imamov and Dr. Shaniyaz Menliev of Koytendag State Nature Reserve for their guidance and expert local knowledge. We are grateful to Atamyrat Veyisov and Aleksandr Degtyarev for providing the source map of Turkmenistan and the photograph of the cave entrance respectively. We also thank Enrique Navarro and Pilar Gmez from the Electron microscopy facility at the Universitat de Valncia (Spain) for their help in taking the SEM photographs. Journal editor Oana Moldovan and the referees Yun-Xia Luan and Yun Bu provided valuable comments that helped us improve the manuscript. References Azadbakhsh S, Nozari J (2016) First faunistic study of Diplura in north of Iran with records of two species of Campodea (Campodeidae). Entomologica Fennica 27: 53. Babaev AG (1994) Landscapes of Turkmenistan. In: Fet V (Ed.) Biogeography and Ecology of Turkmenistan. Monographiae Biologicae book series 72: 5. Bareth C, Cond B (1972) Diploures Campodids des grottes de Pendjab ( Symlacampa clayae ). International Journal of Speleology 4: 55. https://doi.org/10.5038/1827-806X.4.1.8 Bareth C, Cond B (1981) Nouveaux Campodids de grottes dEspagne. Revue suisse Zoologie 88(3): 775. https://doi.org/10.5962/bhl.part.82407 Bareth C, Cond B (1984) Nouveaux Plusiocampa cavernicoles dItalie Continentale (Diplura Campodeidae). Bollettino della Societ entomologica italiana 116(8): 132. Bareth C, Pags J (1994) Diplura. In: Juberthie Ch & Decu V Encyclopaedia Biospeologica, Socit de Biospologie 1: 277. Birstein YA, Ljovuschkin SI (1965) Faune des eaux souterraines saumtres de lAsie centrale. In ternational Journal of Speleology 1: 307. https://doi.org/10.5038/1827-806X.1.3.5 Birstein JA, Ljovuschkin SI (1967) Some results and problem in studying of the subterranean fau na of the USSR. Zoologicheskii Zhurnal 46: 1509. [In Russian, with English summary] Chevrizov BP (1978) Two new genera of the family Campodeidae from the Far East caves. Zoologichesky Zhurnal 57(2): 197. [In Russian, with English summary]

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67 Chou I, Chen T (1980) Two new species of Campodeidae from Xinjiang (Apterygota, Diplura). Entomotaxonomia 2(2): 157. Cond B (1950) Campodeidae (Insecta Diplura) dAfrique du Sud rcolts par le Dr. R. F. Lawrence. Proceedings of the Zoological Society of London 119(4): 807. https://doi. org/10.1111/j.1096-3642.1950.tb00907.x Cond B (1956a) Matriaux pour une monographie des Diploures Campodids. Mmoires Musum National dHistoire Naturelles, srie A, Zoologie 12: 1. Cond B (1956b) Un Campodid troglobie de lInde. Notes Biospologiques 11: 101. Cond B (1974) Les Paurocampa du groupe de suensoni Tuxen dans les grottes dEurope centrale (Diploures Campodids). Revue suisse Zoologie 81(2): 561. https://doi. org/10.5962/bhl.part.76023 Cond B (1993) Premiers Campodeidae cavernicoles de Chine, comme exemple de lvolution souterraine de la Famille (Diplura). Revue suisse de Zoologie 100(4): 823. Cond B, Sendra A (1989) Description du premier Campodid cavernicole du sud de la pn insule Ibrique (Diplura, Campodeidae). Revue suisse Zoologie 96 (3): 611. Ferguson LM (1997) A report on a new species of Pacicampa (Diplura: Campodeidae) from a cave in China and a comparison of some North American genera to Pacicampa and Plutocampa previously only known from the Far East of Russia. Proceedings of the 12 th International Congress of Speleology, La Chaux-de-Fonds, Neuchtel, Switzerland, August 10. 3: 315. Filipescu S, Kaminski MA (2011) Re-discovering Entzia an agglutinated foraminifer from the Transylvanian salt marshes. In: Kaminski, M.A. & Filipescu, S., (eds) Proceedings of the Eighth International Workshop on Agglutinated Foraminifera. Grzybowski Foundation Special Publication 16: 29. George M (1963) Studies on Campodea (Diplura): the Anatomy of the Glands and Sense-Organs of the Head. Journal of Cell Science 3: 1. http://jcs.biologists.org/content/s3-104/65/1 Juberthie-Jupeau L. Bareth C (1980) Ultrastructure des sensilles de lorgane cupuliforme de lantenne des Campodes (Insecta: Diplura). International Journal Insect Morphology and Embryology 9: 255. https://doi.org/10.1016/0020-7322(80)90019-7 Kniss VA (2001) Fauna of the Caves of Russia and Adjacent Countries. Bashkir State Univer sity, Ufa, 237 pp. [In Russian, with English summary]. Koch M (2009) Diplura. In: Resh VH, Card RT (Eds) Encyclopaedia of Insects, Second Edi tion, Elsevier, pp. 281. https://doi.org/10.1016/B978-0-12-374144-8.00084-9 Ljovuschkin SI (1969) On the subterranean fauna of Soviet Central Asia. In: Proceedings of the 4 th International Speleological Congress. IV (Ljubljana, 1969), 145. [in Russian] Malek-Hosseini MJ, Zamani A (2017) A checklist of subterranean arthropods of Iran. Subter ranean Biology 21: 19. https://doi.org/10.3897/subtbiol.21.10573 Paclt J (1957) Diplura. In Genera Insectorum. P. Wytsman, Crainhem, 212E, pp. 123. Paclt J (1958) Iapygidae (Ins. Diplura) des Senckenberg-Museums. Senckenbergiana biologica 39(1/2): 85. Pags J (1953) e 3 rd Danish Expedition to Central Asia. Zoological Results 8. Japygidae (Insecta) de lAfganistan. Videnskabelige Meddelelser Dansk Naturhistorisk Forening 115: 159. Pags J (1959) Remarques sur la classication des diploures. Travaux du Laboratoire de Zoologie et de la Station Aquicole Grimaldi de la Faculte des Sciences de Dijon 26: 1.

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68 Pags J (1962) Japygidae (Insecta, Diplura) de lAfghanistan II. (Contribution ltude de la Fauna de lAfghanistan. 58). Comptes rendus du 86-e Congrs des Socits savantes, Montpellier 1961: 735. Rustamov EA, Welch GR, Brombacher M (Eds) (2009) Important Bird Areas in Turkmenistan priority sites for conservation. Ashgabat, Turkmenistan: Ministry of Nature Protection, 192 pp. Sendra A, Arnedo MA, Ribera C, Teruel S, Bidegaray-Batista L, Cond B (2012) Revision of Cestocampa Cond (Diplura, Campodeidae), with description of a new species from caves in the eastern Iberian Peninsula. Zootaxa 3242: 43. Sendra A, Palacios J, Garcia A, Montejo M (2016) New Species of Campodeidae (Diplura) from Mexican caves. Zootaxa 4072(5): 540. https://doi.org/10.11646/zootaxa.4072.5.2 Sendra A, Jimnez-Valverde A, Rochat J, Legros V, Gasnier S, Cazanove G (2017) A new and remarkable troglobitic Lepidocampa Oudemans, 1890 species from La Runion Island, with a discussion on troglobiomorphic adaptations in campodeids (Diplura). Zoologischer Anzeiger 266: 95. https://doi.org/10.1016/j.jcz.2016.11.005 Silvestri F (1913) Tisanuri raccolti dal Dr. I. Trgrdh nel Natal e nel Zululand. Arkiv fr Zo ologi 8(1): 1. https://doi.org/10.5962/bhl.part.1063 Silvestri F (1931) Campodeidae (Insecta, ysanura) dell Estremo Oriente. Bollettino del Lab oratorio di Zoologia generale ed agraria del R. Isttituto superiore di Portici 25: 286. Starobogatov Ya I (1972) New species of gastropods from springs and subterranean waters of Middle Asia. Proceedings of the Zoological Institute of the Academy of Science USSR 51: 165 (in Russian). Turbanov IS, Palatov DM, Golovatch SI (2016a) e State of the Art of Biospeleology in Russia and Other Countries of the Former Soviet Union: a Review of the Cave (Endogean) In vertebrate Fauna. 1. IntroductionCrustacea. Entomological Review 96, No. 7: 926. https://doi.org/10.1134/S0013873816070162 Turbanov IS, Palatov DM, Golovatch SI (2016b) e State of the Art of Biospeleology in Rus sia and Other Countries of the Former Soviet Union: a Review of the Cave (Endogean) Invertebrate Fauna. 2. Arachnida-Acknowledgements. Entomological Review 96, No. 9: 1297. https://doi.org/10.1134/S0013873816090116 Turbanov IS, Palatov DM, Golovatch SI (2016c) e State of the Art of Biospeleology in Rus sia and Other Countries of the Former Soviet Union: a Review of the Cave (Endogean) Invertebrate Fauna. 3. References. Entomological Review 96, No. 9: 1334. https:// doi.org/10.1134/S0013873816090128 UNESCO Nomination dossier (2015) Mountain ecosystems of Koytendag. Government of Turkmenistan, Ashgabad, 2015, 429 pp. Wygodzinsky PW (1944) Contribuao ao conhecimento da familia Campodeidae (Entotrophi, Insecta) do Mexico. Anales de la Escuela Nacional de Cincias Biolgicas 3 (3): 367. Xie R, Yang Y (1991) Description of two new genera and three new species of Campodeidae in Chine (Diplura). Contributions Shanghai Institute of Entomology 10: 95. Zhang ZQ (2013) Phylum Arthropoda. In: Zhang ZQ (Ed) Animal Biodiversity: An Outline of Higher-level Classication and Survey of Taxonomic Richness (Addenda 2013). Zootaxa 3703: 1. https://doi.org/10.11646/zootaxa.3703.1.1


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