Research Article |
Corresponding author: Sopark Jantarit ( fugthong_dajj@yahoo.com ) Academic editor: Didier Vanden Spiegel
© 2021 Natdanai Likhitrakarn, Sergei I Golovatch, Sopark Jantarit.
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:
Likhitrakarn N, Golovatch SI, Jantarit S (2021) Two new species of the millipede genus Glyphiulus Gervais, 1847 (Diplopoda, Spirostreptida, Cambalopsidae) from caves in northern Thailand. ZooKeys 1056: 173-189. https://doi.org/10.3897/zookeys.1056.71395
|
Two new species of the genus Glyphiulus Gervais, 1847 are described and illustrated. The first species, G. longus sp. nov., is the second species of the javanicus-group to be found in Thailand. It resembles G. guangnanensis Jiang, Guo, Chen & Xie, 2018, from southern China, but is distinguished by a smaller size and the carinotaxic formula of the collum, combined with ♂ legs 1 bearing very strongly reduced telopodites, the anterior gonopods showing a pair of very long and slender apicomesal processes, and the denser plumose and stout flagella of the posterior gonopods. The second species, G. promdami sp. nov., the fifth member of the granulatus-group in Thailand, seems to be particularly similar to G. subbedosae Likhitrakarn, Golovatch & Panha, 2017, from Laos. However, it can be distinguished from the latter species mainly by showing a uniformly yellow collum and the posterior gonopod coxite bearing several strong setae in median and lateral views, coupled with the anterior gonopod coxosternum being microsetose in the anterior and medial parts in caudal view. An identification key to, and a distribution map of, all seven Glyphiulus species currently known to occur in Thailand are also provided.
Cave, diplopod fauna, granulatus-group, javanicus-group, key, map, subterranean habitat
The millipede family Cambalopsidae Cook, 1895 is very common, abundant and widespread in subterranean habitats of Thailand. Within this family, three genera are well-represented in Thai caves: Glyphiulus Gervais, 1847 (4 species), Plusioglyphiulus Silvestri, 1923 (14 species) and Trachyjulus Peters, 1864 (5 species) (
Two distinct species groups are currently recognized in Glyphiulus, based on the conformation of ♂ legs 1 (
Five Glyphiulus species have hitherto been described from Thailand. The first species recorded was G. siamensis Mauriès, 1983, an epigean millipede from Doi Suthep, Chiang Mai (
In the present study, we describe two additional new species of Glyphiulus from northern Thailand. Furthermore, we provide a distributional map of, and a key to, all seven species of the genus currently known to occur in Thailand.
New material was collected in northern Thailand, in particular in limestone mountain and cave habitats. They were searched for and hand-collected using forceps. All populations were found to be sufficiently large and associated with bat guano in the twilight to deep and dark zones of the caves. The specimens taken were euthanized using a two-step method following AVMA Guidelines for the Euthanasia of Animals (
Specimens were then preserved in 95% ethanol for morphological and future molecular studies. All specimens were examined, measured, and photographed under a Nikon SMZ 745T trinocular stereo microscope, equipped with a Canon EOS 5DS R digital SLR camera. Digital images obtained were processed and edited with Adobe Photoshop CS6. Line drawings were based on photographs and examined under the stereo microscope equipped with a digital SLR camera.
Collecting sites were located by GPS using the WGS84 datum using a Garmin GPSMAP 60 CSx, and all coordinates and elevations were checked with Google Earth. The distribution maps of all Glyphiulus species recorded from Thailand were prepared using QGIS 3.18.0 (
The terminology used and the carinotaxic formulae in the descriptions follow those in
The holotypes, as well as most of the paratypes are housed in the Museum of Zoology, Chulalongkorn University (
Family Cambalopsidae Cook, 1895
Holotype
♂: Thailand, Nan Province, Pon, Thung Chang District, Tham Nam Lod, 19°25'13"N, 101°04'15"E, ca 1420 m a.s.l., 30.05.2018, S. Jantarit leg.;
The species is so named to emphasize the long medial processes of the anterior and posterior gonopods; adjective.
This new species seems to be particularly similar to G. guangnanensis Jiang, Guo, Chen & Xie, 2018, from Yunnan Province, China (
Length of holotype ♂, 23.5 mm; that of paratypes, 22.8–26.5 mm (♀); midbody segments round in cross-section (Fig.
Coloration in alcohol (Fig.
Body with 56p+2a+T rings/segments (♂ holotype); ♀ paratypes with 50–57p+2(1)a+T rings. Eye patches transversely ovoid, each composed of 2–5 rather flat ocelli in a single longitudinal row (Fig.
In width, head = ring 2 < collum = midbody rings (close to 13th to 15th) < ring 4 = 5 < 7 = 3 < 8 = 10; body abruptly tapering towards telson on a few posteriormost rings (Fig.
Collum nearly smooth, carinotaxic formula 1+2a+3c+4–5+6c+7a+pc+ma (Fig.
Following metaterga very strongly crested (Fig.
Tegument rather smooth, shining throughout (Fig.
Ventral flaps behind gonopod aperture on ♂ ring 7 barely distinguishable as low swellings forming no marked transverse ridge.
Legs short, on midbody rings about 2/3 length of body height (Figs
♂ legs 1 highly characteristic (Fig.
♂ legs 2 nearly normal (Fig.
♂ legs 3 missing, lost.
Anterior gonopods (Fig.
Posterior gonopods (Fig.
This new species belongs to the javanicus-group which currently encompasses 32 described species (
Glyphiulus longus sp. nov., ♂ holotype A antenna, lateral view B gnathochilarium, ventral view C, D legs 1, oral and caudal views, respectively E legs 2, caudal view F midbody leg G, H anterior gonopods, caudal and oral views, respectively I, J posterior gonopods, oral and caudal views, respectively. Abbreviations: d apicomesal processes, s subsecuriform process, f flagellum process, l lamelliform lobe. Scale bar: 0.1 mm.
Comparison of all seven Glyphiulus species known to occur in Thailand; n/a = no information.
Characters/Species | G. duangdee | G. longus sp. nov. | G. maidtreejit | G. mongkon | G. promdami sp. nov. | G. sattaa | G. siamensis |
---|---|---|---|---|---|---|---|
Group | granulatus | javanicus | granulatus | granulatus | granulatus | granulatus | javanicus |
Length (mm) | |||||||
♂ | 14–22 | 23.5 | 22–24 | 12–20 | 14.5–18.4 | 23–40 | 23 |
♀ | 14–22 | 22.8–26.5 | n/a | n/a | 14.2–24.3 | 23–40 | n/a |
colour | uniformly brown to dark brown | uniformly red-brownish or dark castaneous brown to grey-brown, dorsal crests and porosteles usually dark brownish | dark grey-brown to dark brown, most of tergal crests/tubercles and ozopoiferous cones very dark brown | uniformly light yellow-brown | uniformly red-yellownish to grey-brown, dorsal crests and porosteles usually dark brownish | uniform light brown or brown, with tergal crests/tubercles and ozoporiferous cones dark brown | reddish brown |
Eyes | 8–13, blackish | 2–5, blackish to brownish | 14–16, blackish | 6–8, light greyish | 8–13, blackish to brownish | 9–13, brown | n/a |
Antennae | Long and moderately clavate; extending beyond segment 4 laterally | short and clavate, extending past ring 3 laterally | short and moderately clavate; extending beyond segment 3 laterally | short and moderately clavate; extending beyond segment 3 laterally | short and clavate, extending past ring 3 laterally | Long and moderately clavate; extending beyond segment 4 laterally | n/a |
Body | |||||||
Holotype | 52p+2a+T | 56p+2a+T | 52p+2a+T | 31p+2a+T | 58p+1a+T | 58p+1a+T | 53+2a+T |
♂ | 40-56p+4-2a+T | n/a | 46p+2a+T | 31-43p+2a+T | 35-58p+1–2a+T | 44–72p+5-1a+T | n/a |
♀ | 40-56p+4-2a+T | 50–57p+2(1)a+T | n/a | 31-43p+2a+T | 39–51p+1-3a+T | 44-72p+5-1a+T | n/a |
Carinotaxy formula of collum | 1a+2-5+pc+ma | 1+2a+3c+4-5+6c+7a+pc+ma | 1-6+7a+pc+ma | 1-4+5a+pc+ma | 1–6+7a+pc+ma | 1-4+5a+6a+pc+ma | 6/6+ma |
Carinotaxy formula of midbody rings | 3/3+I/i+4//3+I/i+3/3 | 2/2+I/i+3/3+I/i+2/2 | (2)3/(2)3+I/i+4//3+I/i+3/3 | 3/3+I/i+4//3+I/i+3/ | 3/3+I/i+4/3+I/i+3/3 | 2/2+I/i+4/3(2)/3+I/i+2/2 | 3/3+I/i+3/3I/i+3/3 |
Ratio of leg length comparing to their ring height | 0.7–0.8 | 0.67 | 0.9–1.0 | 1.1–1.2 | 0.5 | 1.0–1.1 | n/a |
Habitat | caves | caves | caves | caves | caves | caves | epigean |
Locality | Tong Saen Khan District, Uttaradit | Thung Chang District, Nan | Lom Sak District, Phetchabun | Ban Non Hin District, Loei | Na Noi District and Na Muen District, Nan; Rong Kwang District, Phrae | Mae Sai District, Chiang Rai | Doi Suthep, Chiang Mai |
Holotype
♂: Thailand, Nan Province, Na Noi District, Tham Chetawan, 18°16'26"N, 100°34'43"E; 520 m a.s.l., 18.05.2018, S. Jantarit leg.;
The species is so named to honour Mr. Rueangrit Promdam, a carcinologist and researcher at the Princess Maha Chakri Sirindhorn Natural History Museum of Prince of Songkla University (
This new species seems to be particularly similar to G. subbedosae Likhitrakarn, Golovatch & Panha, 2017, from Laos (
Length of holotype, 21.8 mm; adult paratypes 14.5–18.4 (♂) or 14.2–24.3 mm long (♀), juveniles 6.5–12.3 mm long; midbody rings round in cross-section (Fig.
Coloration in alcohol (Fig.
Body with 58p+1a+T rings (♂ holotype); paratypes with 35–58p+1–2a+T (♂), 39–51p+1–3a+T (♀) or 25–35+2–5a+T (juveniles). Eye patches transversely ovoid, each composed of 8–13 blackish, rather flat ocelli in three or four irregular longitudinal rows (Fig.
In width, head = ring 4 = 5 < 6 < 7 < 3 < midbody rings (close to 8th to 10th) < 2 < collum; body abruptly tapering towards telson on a few posteriormost rings (Fig.
Collum nearly smooth, carinotaxic formula 1–6+7a+pc+ma (Fig.
Following metaterga similarly strongly crested (Fig.
Tegument rather smooth, dull throughout (Fig.
Ventral flaps behind gonopod aperture on ♂ ring 7 distinguishable as low swellings forming a bare transverse ridge.
Legs rather short, on midbody rings about half the length of ring height (Figs
♂ legs 1 highly characteristic (Fig.
♂ legs 2 nearly normal (Figs
♂ legs 3 modified in having coxa especially slender and elongate (Fig.
Anterior gonopods (Fig.
Posterior gonopods (Fig.
The granulatus-group currently encompasses 36 described species, including our new species (
Three populations have been collected inside caves, with the longest distance of about 25 air-km between the collecting localities, and all show similar morphological characters as described above. Glyphiulus promdami sp. nov. fails to show any morphological adaptations to cave life and is considered here as a troglophilic species. It appears to have a rather narrow distribution, but has been found in a wide range of cave environments from the twilight (Tham Chetawan) to the dark and deep zones of the caves (all three caves). The temperature in the caves where the species was collected ranged between 24.2 and 29.8 °C, while the relative humidity was 70–94%. All populations were found to be quite large and associated with bat guano.
Glyphiulus promdami sp. nov., ♂ holotype A antenna, lateral view B gnathochilarium, ventral view C, D legs 1, oral and caudal views, respectively E legs 2, caudal view F leg 3, caudal view G midbody leg H, I anterior gonopods, caudal and oral views, respectively J, K posterior gonopods, oral and caudal views, respectively. Abbreviations: d apicomesal processes, f flagellum process, l lamelliform lobe. Scale bar: 0.1 mm.
1 | First male legs either normal or reduced in size, but with a pair of paramedian coxal processes (Fig. |
2 (the javanicus-group) |
– | First male legs very strongly reduced, completely lacking any median structures (Fig. |
3 (the granulatus-group) |
2 | Carinotaxic formula of collum, 6+6, all complete crests. Each anterior gonopod with a typical, digitiform, apicomesal process (d) (Fig. |
G. siamensis |
– | Carinotaxic formula of collum, 1+2a+3c+4–5+6c+7a+pc+ma (Fig. |
G. longus sp. nov. |
3 | Body usually larger: length 23–40 mm. Carinotaxic formula of midbody rings, 2/2+I/i+4/3+I/i+2/2 | G. sattaa |
– | Body usually smaller: length 14–24 mm. Carinotaxic formula of midbody rings, 3/3+I/i+4/3+I/i+3/3 | 4 |
4 | Carinotaxic formula of collum, 1–4+5+6c+7a+pc+ma. Ocelli unpigmented, mostly invisible, only sometimes traceable as light greyish, with 6–8 translucid ocelli. Legs long, about 1.1–1.2 the length of ring height | G. mongkon |
– | Carinotaxic formula of collum different. Ocelli pigmented, with 8–16 blackish ocelli either side of head. Legs short, about 0.5–1.0 the length of ring height | 5 |
5 | Carinotaxic formula of collum, 1a+2–5+pc+ma. Telopodites of first male leg-pair two-segmented | G. duangdee |
– | Carinotaxic formula of collum, 1–6+7a+pc+ma (Fig. |
6 |
6 | 14–16 ocelli in three or four irregular transverse rows. Each anterior gonopod with a very short apicomesal process (d), the latter as high as telopodites | G. maidtreejit |
– | 8–13 ocelli in three or four irregular transverse rows, always black. Each anterior gonopod with an elongated apicomesal process (d), the latter obviously higher than telopodites (Fig. |
G. promdami sp. nov. |
The millipede family Cambalopsidae is known to be the most common, highly abundant and species-rich group dominating the cave diplopod faunas of Southeast Asia and China (
Only five Glyphiulus species have been found, and four described from caves, in Thailand: G. duangdee Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011b, G. maidtreejit Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011b, G. mongkon Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011b, and G. sattaa Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011b (Table
Most species of Glyphiulus in Thailand are known from caves or surrounding karst areas, except for G. siamensis Mauriès, 1983 which has been recorded from Kontathan (= Montha Than) waterfall area, Doi Suthep National Park, Chiang Mai Province (
Distribution of Glyphiulus species in Thailand (seven species): Open diamond: Glyphiulus sattaa Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011; Inverted filled triangle: Glyphiulus longus sp. nov.; Filled triangle: Glyphiulus siamensis Mauriès, 1983; Open circle: Glyphiulus promdami sp. nov.; Inverted open triangle: Glyphiulus duangdee Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011; Filled circle: Glyphiulus mongkon Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011; Filled square: Glyphiulus maidtreejit Golovatch, Geoffroy, Mauriès & VandenSpiegel, 2011.
We would like to thank Areeruk Nilsai, Marttrakarn Jitpalo, Katthaleeya Surakhamhaeng and Kanchana Jantapaso for offering their help in the field. This work was supported by the National Science and Technology Development Agency (FDA-CO-2563-11031-TH), and the Thailand Research Fund (RSA6280063) for SJ. Special thanks are due to Liu Weixin, the reviewer whose constructive criticism has allowed us to improve the paper. One of us (SIG) was partly supported by the Presidium of the Russian Academy of Sciences, Programme No. 41 “Biodiversity of Natural Systems and Biological Resources of Russia”.