A new cave‐dwelling millipede of the genus Bollmania Silvestri, 1896 from Yunnan, China, with remarks on the reduction of the second female leg‐pair (Diplopoda: Callipodida: Caspiopetalidae)

Bollmania beroni sp. n., described from a cave in Jianshui County, Yunnan, China is the first true troglo‐ and hygrophilic species in the genus. The new locality extends the range of Bollmania ca 2500 km towards SE, ca 1700 km SW of the only other Chinese record. Notes are given on B. orientalis (Silvestri, 1895), B. nodifrons Lohmander, 1933 and B. oblonga Golovatch, 1979, based on new material from Turkmenistan and Tajikistan, and on two unnamed, probably new species from Afghanistan. An updated key to the eight described species is presented. Original observations and illustrations of second female legs in various callipodid genera are presented, along with a literature review of this character, which has so far received little attention from taxonomists.


Introduction
Millipedes of the order Callipodida have long been known to occur in southern North America and the Mediterranean realm, and have recently become known also from East Asia (Golovatch 1981(Golovatch , 1983Wang and Zhang 1993;Zhang 1993;Wang 1996;Wang and Mauriès 1996;Shear 2000;Shear et al. 2003;Stoev 2004). This region is considered the third centre of callipodidan diversity by Shear (2000), and is even suspected to surpass the other two in terms of number of species by Shear et al. (2003). Three suborders, six families (Shelley 2003) and ca 36 genera constitute the order, though the higher group systematics is outdated and badly needs re-consideration (Stoev and Enghoff 2003). The world distribution of the Callipodida was recently reviewed by Shear et al. (2003).
The family Caspiopetalidae Lohmander, 1931 comprises only one genus: Bollmania Silvestri, 1896 with eight species or subspecies hitherto described: B. orientalis orientalis (Silvestri, 1895) and B. orientalis ajderensis Lohmander, 1933, from Kopetdagh Mts, Turkmenistan;B. serrata Lohmander, 1933, B. nodifrons Lohmander, 1933and B. oblonga Golovatch, 1979B. nematogona (Attems, 1951) and B. gracilis Golovatch, 1983, from Iran;and B. kohalana (Attems, 1936) from Kohala, Pakistan. A ninth species was described in the PhD thesis of Khatoon (1998) from near Islamabad, Pakistan; however, the description has never been properly published and should not be taken into consideration until this happens. Golovatch (1983) provided a key to species in the genus based largely upon the shape of the male gonopods. Females and/or juveniles have been recorded from Afghanistan (Lindberg 1961(Lindberg , 1962, Pakistan (Golovatch 1991) and east China (Golovatch 1981), thus extending the current range of the genus from central to eastern Asia ( Figure 19).
The current paper is the fourth one of a series aimed at updating our knowledge of Eurasian genera of Callipodida (see also Enghoff 2003, 2004;Stoev 2004). Here, we describe a new species of the genus Bollmania, deriving from the material collected by the First Bulgarian-Chinese Speleological Expedition in Yunnan, South China. Formally, this is the first species to be described from the country although the occurrence of the genus there was reported by Golovatch (1981). Judged solely by geography, Shear et al. (2003) considered the last record as representing an unidentifiable genus and species of the family Paracortinidae rather than a species of Bollmania. In the light of the new findings this assumption can be considered as erroneous. Most, if not all, hitherto described species of Bollmania occur in semi-arid habitats, only exceptionally has the genus been found in caves (cf. Lindberg 1961Lindberg , 1962. The new species is the first true Figure 19. Distribution of the genus Bollmania: 1, beroni; 2, gracilis; 3, kohlana; 4, nematogona; 5, nodifrons; 6, oblonga; 7, orientalis; 8, serrata; 9, Bollmania spp. troglo-and hygrophile (s.l.) to be described, dwelling in a large, humid cave with a permanent stream. The new record extends the current range of Bollmania by 2500 km towards the south-east, to within ca 1700 km south-west of the only other Chinese record, from near Nanjing.
We also provide descriptive notes on hitherto undescribed specimens of Bollmania belonging to already described, but as yet poorly known species, as well as the female specimens recorded from Afghanistan by Lindberg (1961Lindberg ( , 1962. An updated version of the key to species published by Golovatch (1983) is also given.
Finally, we present a general review of the morphology of the female second leg-pair in Bollmania, and in Palaearctic genera of the order as a whole. These legs are strongly reduced in many species and, although this character has largely been ignored in previous descriptions, the morphology of the reduced legs offers useful characters for species separation.

Material and methods
The description of the new species is based upon material collected by Dr Petar Beron in the caves of Jianshui County, Yunnan. All specimens are preserved in 70% ethanol. The drawings were made with the aid of a camera lucida. The holotype and two paratypes are preserved in the collection of the National Museum of Natural History, Sofia (NMNHS); a male paratype is deposited in the Zoological Museum, University of Copenhagen (ZMUC). In addition to the Chinese material, Lindberg's millipede collection from Afghanistan (preserved in the Natural History Museum of Gö teborg), containing some female and juvenile specimens of Bollmania, was examined. Further material from Central Asia was obtained from the Zoological Museum of Moscow University (ZMMU, courtesy S. Golovatch and A. Schileyko). The spelling of the locality names follows Kö nemann's Geographica: The Complete Illustrated Atlas of the World (1999).

Description of locality
The cave is situated in Jianshui County, Yunnan. It is spacious, with at least two levels, and a stream about 40-50 cm deep. During heavy rains the floor is flooded. There are many

Etymology
The species honours Dr Petar Beron who collected the material.

Description
Length: 35-40 mm, width 1.9-2.0 mm, 63-65 pleurotergites. Dimensions of the largest pleurotergite in male paratype: prozonite width 1.7 mm; height 1.6 mm; metazonite width 2.0 mm; height 1.8 mm; width of metazonite including the basal crests 2.3 mm; width of metazonite between the largest (sixth) crests 1.88 mm. Body colour brown-yellowish. Dorsum with two paramedian light brown stripes and a broad median yellow stripe along the whole body length. Head and legs yellowish. Posterior part of head marbled brown-yellowish. Ocellaria in a rhomboid form composed of 35-40 black ocelli in seven rows. Organ of Tömö sváry of same size as ocelli, easily seen between ocellaria and base of antennae. Head in males slightly concave frontally, covered with minute setae, and bearing a well-expressed frontal knob (Figures 4,5); in female ovoid, evenly rounded. Labrum light brown, a little darker in contrast to the yellowishbrown forehead. Labral edge covered with larger setae in an irregular row. Antennae yellowish-white, densely covered with minute setae, reaching the posterior margin of sixth pleurotergite when folded backward. First antennomere almost one-quarter of second; second and third almost equal in size; fourth antennomere four-fifths length of third. Fifth and sixth antennomeres enlarged distally, seventh cone-shaped ( Figure 4).
Male pleurotergites 1-5 visibly narrower than 6-8 and just a little narrower than 9-11. Each hemipleurite of pleurotergite 7 (the widest of all) with about 18 crests. Size of crests on pleurotergite 7: 6.10.85254.153555759. Female second and third pleurotergites strongly enlarged. Ozopores visible from sixth to penultimate pleurotergite, placed on top of the sixth, the most pronounced crest of all. Table I shows the chaetotaxy of the anterior pleurotergites.
First and second leg-pair in males shorter than following legs, with prefemur, femur, postfemur and tibia densely covered with setae that are missing in the subsequent legs. Male leg-pairs 2, and 4-7 with coxal projections ( Figure 7); pairs 1 and 3 without. Gonopore on posterior side of the coxa of leg 2. Prefemur of male leg-pair 7 much stouter than femur, its ventral side covered with a field of fine setae. A long seta emerging on the postero-ventral side of coxa, prefemur and femur ( Figure 7). Tarsus divided into a long basitarsus and a very short distitarsus, the latter ending with a claw. Tarsal pads present from leg-pair 3, larger on anterior legs. Coxae 9 and 10 normal. Female second leg-pair strongly reduced ( Figure 11). Hypoproct tripartite, median sclerite largest. Anal valves with two paramedian macrosetae. Spinnerets long and slender ( Figure 6). and thin, pointing caudad. Basal part of solenomere with ovoid, porous plate (k) pointing meso-caudal (Figures 9, 10). Solenomeres with long, sharp and S-shaped basal processes (p), crossing each other in situ (Figure 8). Posterior part of solenomere ending with two branches, the upper one a little shorter and bearing a well-pronounced dorsal tooth (z) and a small but visible spine at its base (j). Another tiny spine (ha) emerging at the posterior end of the main branch. Seminal groove (sg) beginning from the base of the femoroid following its main stem and ending between the branches.

Remarks
Bollmania beroni sp. n. differs from its congeners by the following characters: antennae white-yellowish; coxae of male leg-pairs 2, 4-7 with projections; gonopods with a wellpronounced porous plate (k), dorsal tooth (z) and S-shaped process (p); female second legpair bipartite, with characteristic shape. Although found in a cave, there are no characters of troglomorphism, except probably for slightly longer legs (compared to the examined specimens from Afghanistan, Turkmenistan and Tajikistan, see below) and white-yellowish body and antennae (the other Bollmania species are usually dark brown, especially the antennae). Bollmania kohalana was, so far, the easternmost species described in the genus. The locality of B. beroni extends its range about 2500 km in a south-eastern direction, being the southernmost of all known localities and lying ca 1700 km south southwest of the only other (dubious, cf. above) Chinese record of Bollmania, near Nanjing (Golovatch 1981). The new species is the first true troglo-and hygrophile (s.l.) described in the genus, living in a large cave system supporting a permanent stream.

Remarks
The examined specimens correspond well with the original description of the species, which was probably based on a not fully mature male. Having further material at our disposal we can improve the species diagnosis with the following characters: adult males with 58-60 pleurotergites+telson; females composed of 60 pleurotergites+telson; subadult males without a knob on the head; inner gonopodal coxal process (ip) longer than that illustrated by Lohmander (1933), sharpened, and apically curved as in B. oblonga. Female second leg-pair reduced ( Figure 14).

Remarks
This species is close to B. nodifrons, both species being characterized by the absence of a basal process of the solenomere, and in having a similar shape to the anterior part of the gonopod (compare Figures 13-15 in Golovatch 1979with Figures 45-47 in Lohmander 1933. However, B. oblonga was distinguished by Golovatch by the absence of a knob on the head, the long antennae in males, comparatively small gonopods, a much longer distal process of the solenomere (e in Golovatch 1979, Figures 13-15), a much longer, S-shaped and apically swollen ip (hs in Golovatch 1979, Figure 13), and the existence of small swellings on the coxae of leg-pair 9 (Golovatch 1979). Although the subadult B. nodifrons males are without a knob on the head, and the ip in adults is longer than that described by Lohmander (1933), both species are well distinguished by the size of the gonopods, the length of the distal process, the shape of the apical part of the gonofemur (with two small denticles in B. nodifrons), and the shape of ip. The female second leg-pair is modified ( Figure 15). This species was hitherto known only from its type locality near Kondary Gorge, north of Dushanbe. Our material comes from Gazi-Malek, a mountain located about 150 km further south and very close to the known range of B. nodifrons.

Remarks
This species is confined to the region of Kopetdagh Mts, Turkmenistan. The new locality at Kara Kala is situated ca 190 km north-west of Ashgabat, thus extending the species range some 80-100 km to the north-east, but still within the limits of the mountain.

Bollmania females from Afghanistan
Lindberg's collection from Afghanistan contains two Bollmania species, both unfortunately represented only by females. To facilitate future work we give below a brief description of the examined material.

Description
Length (adult female): 41-42 mm; 64-66 pleurotergites+telson. Antennae short, reaching the end of third or the anterior part of fourth pleurotergite; brown, somewhat lighter laterally. Head convex, covered with fine, dense setae. Vertex with two light spots. Ocelli ca 36 in six to seven rows. Prozonites pale blue-greyish anteriorly, dark brown posteriorly. Metazonites dark brown with lighter yellowish spots beginning from sixth crests downwards; crests 1-5 dark brown, 6 yellow-brownish, bearing ozopore on the top; crests 7-10 brownish, laterally with large yellowish spots. Size of crests: 6.8510.254. The lighter medial band on the dorsum, usually present in Bollmania, is missing. The median dorsal pleurotergite suture is pale brown-yellowish contrasting to brown proand metazonites. Hypoproct divided into three sclerites, with four stout setae. Legs pale yellowish; tibiae and tarsalia darker. Second leg-pair of adult females reduced ( Figure 12).

Remarks
This species resembles B. oblonga, having a similar shape of the second female leg-pair (compare Figure 12 with Figure 15). It was found ca 230 km east of the Babatag Mt, the type locality of B. oblonga.

B. nodifrons Lohmander
Remarks on the reduction of the second leg-pair in female Callipodida Some female callipodidans have long been known to show the second leg-pair strongly reduced. This condition occurs in various suborders, families, genera, and species.  B. armatum Verhoeff, 1926, B. beskovi Strasser, 1973, B. bulgaricum Stoev and Enghoff, 2003, B. graecum Stoev and Enghoff, 2003, B. petrovi Stoev and Enghoff, 2003, B. rhodopinum Verhoeff, 1937Eurygyrus N Hoffman and Lohmander 1964Hoffman 1972;Glaubrecht and Spelda 1993, p Wang and Zhang 1993, Figures 5, 12, 13, 17, 18, 22, 23, 27, 28, 30, 31;Stoev 2004, p 5, Figure 11  summarizes the situation for all Palaearctic callipodidan genera. Concerning the North American genera, the published information (Loomis 1937;Buckett and Gardner 1969;Hoffman 1972Hoffman , 1982 is far from exhaustive and partly contradictory. We have examined females of Abacion magnum (Loomis, 1943) and can confirm that the second leg-pair is indeed strongly reduced in adult females. Rowland Shelley has kindly studied a number of North American callipodidans at our request and informs (in litt.) that adult females of Abacion tesselatum Rafinesque, 1820, A. lactarium (Say, 1821), A. texense (Loomis, 1937), and Delophon georgianum Chamberlin, 1943 (all belonging to the family Abacionidae) have indeed reduced second legs. In the North American ''schizopetalids'' (Shelley doubts that they are really confamilial with the European ones), he found adult females of Tynomma mutans (Chamberlin, 1910) to have reduced second legs; the females he examined of Idrionaria dineh Shelley, 1996, Colactis utorum (Chamberlin, 1925 and C. protenta Loomis, 1937 all had well-developed second legs, but all these females had no obvious ovipositor and thus may be subadult. At present it is not possible to say if the character is of value for analysing the suprageneric relationships of the Callipodida. A more complete study, involving more genera, is necessary before this can be assessed, as well as a comprehensive phylogenetic analysis performed. Intuitively, one would presume that normal, non-reduced legs represent the plesiomorphic state, which is also supported by the absence of modification in Sinocallipus simplipodicus Zhang, 1993, the most primitive callipodidan hitherto described (Zhang 1993;Shear 2000;Shear et al. 2003). On the other hand, reduced second female legs have been found among species of both of the other suborders (see Table II), thus showing that the modification has appeared several times independently. It is worth mentioning that in some Callipodella and Dorypetalum species, we found the third pair of legs to be reduced instead of the second.
In Bollmania, the reduction of the second female legs apparently only happens in some of the species. Thus, female B. nematogona and B. sp. 2 from Afghanistan have normal legs. A possible explanation for this could be that the studied females of these species are not fully mature. Thus, in Callipus foetidissimus (Savi, 1819), the reduction of the second legs takes place at the last moult; females in the second-last stadium have fully developed second legs at the base of which the vulvae are placed instead of being retracted into the body as in the adults (Nguyen Duy-Jacquemin 1976). Similarly, it is only the larger females of Paracortina wangi Stoev, 2004 (Paracortinidae) which have reduced second legs (Stoev 2004), cf. also Shelley's findings on North American material, referred to above.

The second female legs as a species-specific character
In Bollmania the reduced second female legs are of a different shape in each species and hence are useful for species distinction. The same is true in Callipus (Strasser 1974) and Paracortina (Wang and Zhang 1993;Stoev 2004). There is an interesting parallel to this situation in the order Julida where females of Nopoiulus subgenus Paranopoiulus (Blaniulidae) have reduced second legs, the shape of which is species-specific (Enghoff 1984). localities in Tajikistan and for commenting on the final version of the manuscript, and to R. M. Shelley (Raleigh, NC, USA) for studying female North American callipodids on our request. Dr Jean-Jacques Geoffroy (Paris) helped in obtaining some obscure literature. Dr Petar Beron (NMNHS) shared unpublished information on the fauna of the Yan Dong Cave. Fani Bozarova (NMNHS) inked the illustrations and G. Brovad (ZMUC) provided photographs. Part of the work was undertaken with support from the European Commission's programme ''Transnational Access to Major Research Infrastructures'' to P.S. for a month's stay at COBICE (Copenhagen Biosystematics Centre).