Research Article |
Corresponding author: Boyan Vagalinski ( boyanv84@gmail.com ) Academic editor: Oana Teodora Moldovan
© 2018 Boyan Vagalinski, Kaibaryer Meng, Darina Bachvarova, Pavel Stoev.
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.
Citation:
Vagalinski B, Meng K, Bachvarova D, Stoev P (2018) A redescription of the poorly known cave millipede Skleroprotopus membranipedalis Zhang, 1985 (Diplopoda, Julida, Mongoliulidae), with an overview of the genus Skleroprotopus Attems, 1901. Subterranean Biology 26: 55-66. https://doi.org/10.3897/subtbiol.26.26225
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We redescribe the poorly known Chinese millipede Skleroprotopus membranipedalis Zhang, 1985 recorded from Shi-Hua (Stone Flower) Cave, Fangshan County, Beijing. The species’ original description is in Chinese in an obscure outlet which significantly hampers its recognition from its congeners. Here, based on newly collected material, we provide the first scanning electron micrographs of important taxonomic traits. In addition to its type locality, we report the species also from Yun-Shui (Cloud Water) Cave, situated in the same county, some 18 km away. We propose the genus Senbutudoiulus Miyosi, 1957 to be a junior subjective synonym of Skleroprotopus Attems, 1901, syn. n., and introduce the following new combination: Skleroprotopus platypodus (Miyosi, 1957), comb. n. (former Senbutudoiulus).
China, new record, new synonymy, troglobiomorphism
The eastern Asian julidan family Mongoliulidae is currently known to comprise 8 genera and 36 species, as recently reviewed by
Summarized distribution map of species of Skleroprotopus. Numbers: 1 Skleroprotopus chichibuensis Shinohara, 1960 2 S. chollus Mikhaljova & Korsós 2003 3 S. confucius Attems, 1901 4 S. coreanus (Pocock, 1895) 5 S. costatus Mikhaljova & Korsós, 2003 6 S. hakui Takakuwa, 1940 7 S. ikedai Takakuwa, 1941 8 S. inferus Verhoeff, 1939 9 S. insularum Verhoeff, 1939 10 S. laticoxalis Takakuwa, 1942 11 S. membranipedalis Zhang, 1985 12 S. montanus Takakuwa, 1942 13 S. okiensis Takakuwa, 1941 14 S. osedoensis Miyosi, 1957 15 S. platypodus (Miyosi, 1957) 16 S. ramuliferus Lim & Mikhaljova, 2000 17 S. schmidti Golovatch, 1979 18 S. serratus Takakuwa & Takashima, 1949 19 S. sidegatakedensis Miyosi 1957 20 S. simplex Takakuwa, 1941 21 S. toriii Takakuwa, 1940.
We here provide an emended description of S. membranipedalis based on both recently collected topotypic material and specimens from the Cloud Water Cave (new record), and present a brief overview of the genus Skleroprotopus.
Shi-Hua Cave, also known as Qian-Zhen Cave and Shi-Fo Cave, is located on the south bank of Da-Shi River in Fang-Shan Mountain, Fang-Shan World Geological park, approximately 50 km southwest of Beijing. It is the largest limestone cave in northern China, and the one with the richest deposits of secondary carbonate sediments. The cave is locally important in both touristic and scientific aspects. It is part of the Shi-Hua Karst system formed by several caves, namely Ji-Mao, Yin-Hu, Shi-Hua, Qing-Feng and Kong-Shui, connected by an underground river (
Shi-Hua is a multilayer limestone cave consisting of 7 levels interconnected by numerous passages and chambers, measuring a total length of about 5640 m. The cave’s highest point measured from the entrance is 14 m and the lowest is 158 m (
Yun-Shui Cave is also situated in Fang-Shan World Geological park, 75 km from Beijing and some 18 km in a straight line from Shi-Hua Cave. Yun-Shui comprises several halls with a total length of about 610 m. Despite the proximity to Shi-Hua, Yun-Shui, along with the caves San-Qing, Long-Xian-Gong and Xian-Xia, is part of a different karst system – the Tanghsien Karst system located on the northern bank of Ju-Ma River. The two systems – Tanghsien and Shi-Hua – are not connected by underground rivers or terrestrial channels.
The stratum of Yun-Shui was developed from epicontinental sea deposits 1000 MYA, and, similar to Shi-Hua, the cave itself was shaped during the Neogene (
The material was collected in November 2013 by Pavel Stoev, Christo Deltshev and Shuqiang Li. It is deposited in the Myriapod collection of the National Museum of Natural History, Sofia (NMNHS). The scanning electron micrographs were obtained with the aid of a JEOL JSM-5510 at the Faculty of Chemistry, Sofia University. The examined body parts were mounted on cover glasses equipped with a sticky tape, and sputter-coated with gold-palladium. The states of the taxonomic characters presented in Table
Main diagnostic characters of species of Skleroprotopus. Symbols: * - divided apically; ** - completely undivided.
Number of articles of male leg-pair 1 | Claws on male leg-pair 1 | Number of articles of telopodites of male leg-pair 7 | Coxites of male leg-pair 7 | Promerital telopodites | Flagellum apically | Opisthomerite deeply divided into 2 branches | Sources | |
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S. chichibuensis | 5 | absent | 3 | massive, stout | ~ 1/2 as long as coxites | bifurcated | yes |
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S. chollus | 5 | absent | 1 | very short and stout | ~ 1/2 as long as coxites | bifurcated | yes |
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S. confucius | 5 | absent | 3 | rather slender | ~ 2/3 as long as coxites | bifurcated | yes |
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S. coreanus | 5 | absent | 3 | long and slender | ~ 3/4 as long as coxites | non-branched | yes |
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S. costatus | 5 | absent | 1 | rather slender | ~ 2/3 as long as coxites | non-branched | no* |
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S. hakui | 6 | absent | 1–2 | long and slender | ~ 3/4 as long as coxites | bifurcated | yes |
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S. ikedai | 7 | absent | 2 | somewhat elongated | ~ 2/3 as long as coxites | bifurcated | yes |
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S. inferus | 5 | present | 2 | massive, stout | ~ 2/3 as long as coxites | bifurcated | yes |
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S. insularum | 3 | absent | 1 | massive, stout | ~ 2/3 as long as coxites | ? | ? |
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S. laticoxalis | 5 | absent | 3 | very short and stout | ~ 1/2 as long as coxites | bifurcated | yes |
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S. membranipedalis | 6 | absent | 2, the 2nd one minute | long and slender | ~ 1/2 as long as coxites | non-branched | yes |
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S. montanus | 5 | absent | 3 | rather short and stout | almost as long as coxites | ? | yes |
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S. okiensis | 5 | absent | 2 | massive, stout | ~ 2/3 as long as coxites | bifurcated | yes |
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S. osedoensis | 5 | absent | 1 | short and stout | ~ 1/4 as long as coxites | bifurcated | yes |
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S. platypodus | 5 | absent | 2 | short and stout | ~ 1/4 as long as coxites | bifurcated | yes |
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S. ramuliferus | 5 | absent | 2 | massive, somewhat elongated | ~ 2/3 as long as coxites | non-branched | yes |
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S. schmidti | 5 | present | 2 | somewhat elongated | ~ 3/4 as long as coxites | non-branched | yes |
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S. serratus | 5 | absent | 1–3 | long and slender | almost as long as coxites | non-branched | yes |
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S. sidegatakedensis | 5 | present | 2, both very large | short and stout | ~ 1/2 as long as coxites | bifurcated | ? |
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S. simplex | 5 | absent | 2, the 2nd one minute | somewhat elongated | ~ 2/3 as long as coxites | non-branched | no** |
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S. toriii | 5 | absent | 2, both very short | massive, rather short | ~ 2/3 as long as coxites | bifurcated | yes |
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Genus Skleroprotopus Attems, 1901
Mongoliulus Pocock, 1903
Paraprotopus Verhoeff, 1939
Nesoprotopus Verhoeff, 1939
A genus of Mongoliulidae, most similar to the genus Ansiulus Takakuwa, both sharing a number of characters such as: ozopores in all body-rings, an anterior gonopod with an unsegmented telopodite (except for S. schmidti) and a slightly to considerably higher coxite carrying a well-developed flagellum, and a bifid (except for S. simplex) posterior gonopod consisting of a slender solenomerital process and a broader, shield-like, apically setose, caudal process. Differs from Ansiulus mostly by the complete absence of telopodites on posterior gonopods and by the strongly reduced telopodites of male leg-pair 7 (except for S. sidegatakedensis).
Skleroprotopus membranipedalis Zhang, 1985: 154–156, figs 1–8.
3 males, 7 females & 16 juv., China, Beijing, Fangshan Distr., Shi-Hua (Stone Flower/ Stone Buddha) Cave (type locality), 39°47'36.7"N, 115°56'32.1"E, 12.XI.2013, P. Stoev, Ch. Delchev & S. Li leg. (NMNHS); 7 females & 14 juv., same Distr., Mt. Shangfang, Yun-Shui (Cloud Water) Cave, the touristic part, 39°40'29"N, 115°48'35"E, 3.XI.2013, under stones, creeping on walls, humid clay, some 100 m from the entrance, same collectors (NMNHS).
Differs from congeners mostly by the flattened, blade-like, basolateral process on the caudal face of the anterior gonopod, and by the completely pigmentless ocelli.
Measurements: males 49–51 mm in length, 2.5–2.6 mm in height at mid-body, body ring formula 62+(1–2)+T; females 49–60 mm, 2.4–2.8 mm, and (61–67)+(1–2)+T, respectively.
Colouration in life (Fig.
General morphology: Adults with 25–40 very small and completely pigmentless ocelli arranged in a narrow triangular field; eye rows unclear. Vertigial setae and pits absent; 4 supralabral and 22–28 labral setae. Antennae (Fig.
Skleroprotopus membranipedalis, external morphology: 3 male antenna 4 female head, ventral view 5 male gnathochilarium, ventral view 6 left male leg 1, latero-dorsal view 7 male leg-pair 2 with penis, caudal view 8 penis in situ, lateral view 9 left male leg 3, caudal view 10 male leg-pair 7, caudal view 11 telopodite of male leg 7, caudal view. Symbols: pn: penis, ta: tarsal remnant with apical claw, te: telopodite.
Collum with ca. 10 shallow striae on each side. Body rings considerably vaulted, this becoming increasingly pronounced towards telson. Prozonites with several shallow, somewhat undulating, transverse striae encircling them (striae being more pronounced dorsally), and dense, short and shallow, longitudinal striation on dorsum near the pro-metazonital suture. Metazonites with rather sparse and shallow (deeper ventrally) longitudinal striae, these disappearing above the ozopore level; without setae on hind margins. Ozopores relatively small, set far behind the pro-metazonital suture, at ca. metazonital mid-length.
Epiproct very short and blunt in both sexes, marginally with one to several setae. Hypoproct broad and short, nearly semi-elliptic, edentate, tightly fitting under the paraprocts; its margin slightly more strongly vaulted in males. Paraprocts with only 2–3 setae each situated near the caudal margins. Walking legs slender; tarsi of mid-body legs 2–2.3 times longer than tibiae, and 3.3–3.7 times longer than the apical claw.
Male sexual characters: Male mandibular stipites enlarged, ventrally incised, forming two nearly equal, subconical lobes. Promentum (pr in Fig.
Gonopods (Figs
Skleroprotopus membranipedalis, gonopods and vulva: 12 left anterior gonopods, caudal, slightly lateral view 13 left anterior gonopod, lateral view 14 left posterior gonopod, lateral view 15 right posterior gonopod, antero-mesal view 16 same, mesal view 17 left vulva, lateral view. Symbols: a: anterior process, b: axe blade-like process, f: flagellum, op: operculum, p: posterior process, r: remnant of a podomere; rs: receptaculum seminis, , sp: basal spine, te: telopodite. Scale bar (17): 0.2 mm.
Anterior gonopod (Figs
Posterior gonopod (Figs
Female sexual characters: Leg-pair 1 somewhat thicker and shorter, leg-pair 2 also shorter, but not thicker than the following legs. Vulva (Fig.
With its light coloration, slender legs and antennae, and pigmentless ocelli S. membranipedalis seems to be the most troglobiomorphic species within the genus (see e.g.
However, the presence of ocelli in S. membranipedalis suggests a still ongoing adaptation towards troglobiism, meaning that the species has entered the underground relatively recently, possibly in the Pleistocene, in response to the increasingly cooler and drier climate and the gradual replacement of forests by grasslands in the temperate zones – the so called “climatic relict hypothesis” as a model of subterranean colonization (
Apart from its troglobiomorphic alterations, S. membranipedalis is morphologically most similar to S. coreanus and S. serratus, with whom it shares the lack of claws in the male first legs, the elongated coxites of male 7th legs, the apically non-branched flagellum, and the well-divided posterior gonopod. On the other hand, its six-segmented male first legs suggest a proximity to S. hakui, but this is in contradiction with the apically bifurcated flagellum in the latter species.
1. Considering the great interspecific variations of the male leg-pair 1 in Skleroprotopus, including important features such as the number of podomeres or presence vs. absence of apical claws, their shape observed in the sole species of Senbutudoiulus – S. platypodus Miyosi, 1957 – is not sufficiently unusual to justify a separate genus.
2. With the exception of S. montanus, the number of the mandibular pectinate lamellae exceeds 6 also in those species of Skleroprotopus for which this character is known, namely in S. confucius (the type species), S. membranipedalis, S. schmidti, S. hakui, and S. toriii, all showing 7 lamellae.
3. A similar oblong oval shape of the gnathochilarium is also observed in members of Skleroprotopus, such as S. coreanus.
4. The slightly unusual shape of the male leg-pair 2 is too weak for a main generic diagnostic character.
It is also noteworthy that the opisthomerite in Senbutudoiulus platypodus is conspicuosly similar to that in Skleroprotopus osedoensis Miyosi, 1957, described from a cave in the same Japanese prefecture as the former species (
Thus, we here propose a new synonymy: Senbutudoiulus Miyosi, 1957 = Skleroprotopus Attems, 1901, syn. n., and a new combination: Skleroprotopus platypodus (Miyosi, 1957), comb. n.
Of the remaining mongoliulid genera, Ansiulus Takakuwa, 1940 is conspicuously similar to Skleroprotopus, and is a possible synonym of the latter, as already pointed out by
In general, the distribution of the main taxonomic characters within Skleroprotopus is mosaic-like, as it can be traced in Table
PS is grateful to Shuqiang Li for hosting him at the Institute of Zoology, CAS in November 2013, and for arranging the field trips to the caves Shi-Hua and Yun-Shui. The study is part of the project “Speciation and conservation of cave invertebrate animals”, financially supported by the bilateral exchange program of the Chinese and Bulgarian academies of sciences. The study was partly funded by the University of Shumen, project RD-08-167/09.02.2018.
Part of the results of this study were presented at the 17th International Congress of Myriapodology in Krabi, Thailand, 23–26 July 2017.