Research Article |
Corresponding author: Sopark Jantarit ( fugthong_dajj@yahoo.com ) Academic editor: Wanda M. Weiner
© 2019 Sopark Jantarit, Chutamas Satasook, Louis Deharveng.
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:
Jantarit S, Satasook C, Deharveng L (2019) Coecobrya sirindhornae sp. n., the most highly troglomorphic Collembola in Southeast Asia (Collembola, Entomobryidae). ZooKeys 824: 21-44. https://doi.org/10.3897/zookeys.824.31635
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The most highly troglomorphic Collembola of Southeast Asia, Coecobrya sirindhornae sp. n., is described from a cave in Satun province, Thai Peninsula. It is characterised by its large size, extremely elongated antennae, relatively long legs and furca, reduced macrochaetotaxy, very long and slender claw, pointed tenent hair, four sublobal hairs on outer maxillary lobe, and the absence of eyes and pigmentation. A checklist of Thai Coecobrya species and a key to the troglomorphic species of Thailand are provided. Troglomorphy and conservation of cave habitats in the area are discussed.
new species, peninsular Thailand, subterranean environment, taxonomy, troglomorphy
The genus Coecobrya Yosii, 1956 is characterised by polymacrochaetotic chaetotaxy, absence or reduced eye number, absence of or weak pigmentation, four antennal segments, falcate mucro with a basal spine, and absence of body scales, labral papillae, and dental spines (
Troglomorphic features in Collembola are large body size, elongated appendages (antennae, and to a lesser degree legs and furca), multiplication of antennal chaetae, elongated and slender claw complex, pointed tenent hair, blindness and depigmentation (
In the present study, we describe an extremely troglomorphic new species of Collembola discovered in a cave in Satun province, Thailand. We discuss its level of troglomorphy, by far the highest for Collembola of continental Southeast Asia. A key to Thai troglomorphic species is provided.
We sampled at least 130 caves throughout Thailand to date. Collembola were collected by an aspirator or extracted on Berlese funnel from organic debris. The highly troglomorphic Coecobrya was found in a single cave, located in Satun province. Specimens were stored in 95% ethanol and were mounted on slides in Marc Andre II medium after clearing in Nesbitt solution. Morphological characters were examined using Leica DM1000 LED microscope with phase-contrast. Drawings were made using a drawing tube, and figures were improved with Illustrator CC (Adobe Inc). Specimens were brought alive to the laboratory, where photos were taken using a Leica M80 with Leica MC170 HD, and enhanced by LAS V4.12 software. Scanning Electron Micrographs were taken by Apreo SEM/FEI from the Scientific Equipment Center, Prince of Songkla University (Thailand).
Abbreviations used in the description:
Morphological structures:
Ant. antennal segment,
Abd. abdominal segment,
psp pseudopore(s),
Th. thoracic segment,
Gr. group,
tita tibiotarsus,
mac macrochaeta(e),
mes mesochaeta(e),
mic microchaeta(e),
ms S-microchaeta(e)/microsensillum(a),
tric trichobothrium(ia),
s ordinary S-chaeta(e)/sens
Institutions:
NJAU Department of Entomology, College of Plant Protection, Nanjing Agricultural University, China.
Terminology
Dorsal body chaetotaxy follows
Holotype: male on slide, Thailand: Satun province: Manang district, Tham Rusri, altitude 58 m, nine specimens (one male, one female and three subadults in slides, three in ethanol), dark zone of cave, by aspirator, S Jantarit and A Nilsai leg. (sample # THA_SJ_STN09), 30/04/2016 (A Nilsai), six specimens (three subadults in slides, three in ethanol); 03/05/2016 (S Jantarit and A Nilsai), five specimens in ethanol; 25/07/2017 (S Jantarit and A Nilsai), three specimens in ethanol; 17/03/2018 (S Jantarit and A Nilsai), three specimens in ethanol. Holotype and 13 paratypes in slides deposited in
Habitus (Fig.
Coecobrya sirindhornae sp. n. A–D Habitus E–F Two morphological types of cave Coecobrya in Thailand E Coecobrya phanthuratensis Zhang & Jantarit, 2018; normal form with short antennae, appendages and small size F Coecobrya polychaeta Zhang & Nilsai, 2017; troglomorphic form with long antennae and appendages with large body size and G Coecobrya sirindhornae sp. n., highly troglomorphic characters with extremely long antennae and appendages and also large body size.
Pseudopores (Figs
Coecobrya sirindhornae sp. n. continued. A Distal part of Ant. II dorsally of left antenna BAnt. III organ of left side C Distal part of Ant. IV with subapical organite D Ratio of antennal length E Clypeal chaetae F Prelabral and labral chaetae G Labial palp H Outer maxillary lobe I Mandibles J Ventro-distal complex of labrum K Chaetae of labial basis and ventral chaetotaxy of head.
Mouthparts and ventral head chaetotaxy (Figs
Coecobrya sirindhornae sp. n. continued with SEM. AAnt. I dorsally with three mac (arrows) BAnt. I latero-dorsally with a row of spear-like chaetae (arrows) C Distal part of Ant. II dorsally with a group of paddle-like chaetae (arrows) D–EAnt. III organ of right side F Labral chaetae and maxillary outer lobe G Ventral chaetotaxy of head H Pseudopore and mac on Th. III I Claw III morphology J Mucro K Labial palp with its notation after
Antennae (Figs
Dorsal head chaetotaxy (Fig.
Tergites (Fig.
Legs (Figs
Ventral tube (Fig.
Furcal complex (Figs
Genital plate (Fig.
Coecobrya sirindhornae sp. n. is restricted to the dark zone of the cave where it has been found, in the oligotrophic environment of a small chamber, on muddy ground and wet rock walls. The chamber is connected to a narrow steep hole. Small puddles are present in the chamber and water is dripping from the ceiling. Muddy ground surface is flooded during rainy season. Some individuals were found feeding on a cricket corpse. They were quick jumping and moved rapidly. The species is found only in that chamber where humidity is at saturation, and temperature is constant (23‒24 degrees Celsius). The population seems rather limited (only 26 specimens were collected from five attempts, each time one hour collecting by 2 people). Small (young) individuals were less numerous and not collected.
This species is named to honour Her Royal Highness Princess Maha Chakri Sirindhorn, who is passionately interested in natural history and plays an important role in promoting the conservation of biodiversity and the environment of Thailand.
Coecobrya sirindhornae sp. n. differs at first from all other species of the genus by its highly troglomorphic characters. Diagnostic morphological characters of the new species and related troglomorphic Coecobrya are listed in Table
Comparison of troglomorphic Coecobrya: C. chumphonensis Zhang & Nilsai, 2017, C. cavicta Nilsai & Zhang, 2017, C. polychaeta Zhang & Nilsai, 2017, C. sirindhornae sp. n., and C. nupa Christiansen & Bellinger, 1992. Key: c = ciliated chaetae, s = smooth chaetae, ? = not given in literature description. Characters indicated in parentheses are rarely observed.
Characters | C. chumphonensis | C. cavicta | C. polychaeta | C. sirindhornae sp. n. | C. nupa |
---|---|---|---|---|---|
Body length | up to 2.82 mm | 1.72 mm | up to 2.58 mm | up to 2.6 mm | 2.0 mm |
Ant. /head | 3.70–4.48 | 2.67 | 5.91–7.12 | 8.0‒12.3 | 6.5 |
Long smooth straight chaetae on antennae | absent | present | absent | present | ? |
Number of paddle-like chaetae on Ant. II | 2‒4 | ? | 1 | 10‒12 | ? |
Clypeus | |||||
prefrontal | 3s | ? | 3s | 3s | ? |
facial | 8s | ? | 2s7‒10c | 2s7‒10c | ? |
Dorsal head | |||||
An | 2 | 4 | 4 | 1 | ? |
A0 | mac | mac | mic | mes | ? |
M | 4 | 3 | 3 | 0 | ? |
Gr. II | 6(7) | 4 | 3 | 1 | ? |
Sublobal hairs on maxillary outer lobe | 3 | 3 | 4 | 4 | 3 |
Lateral process of labial palp | short | short | long | long | short |
Labial chaetae | mRel1l2 | mrel1l2 | M1m2rel1l2 | m1m2rel1l2 | M1m2rel1l2 |
Postlabial chaeta X | minute | minute | normal | normal | ? |
Chaetae along cephalic groove | 4s5‒7c | 3‒4s7‒8c | 6‒7s5‒10c | 7‒9s3‒7c | ? |
Chaetotaxy of Th. II | |||||
medio-medial mac | 4–6 | 3 | 7(6) | 3 | 2 |
medio-sublateral mac | 3 | 4 | 3 | 2 | ? |
Posterior macTh. II | 25–32 | 30–31 | 29–40 | 15–18 | ? |
Mac on Th. III | 32–35 | 35 | 35–43 | 32–35 | 15? |
Mac on Abd. I | 6–7 | 6–7 | 8–9 | 6 | 4 |
Central macAbd. II | 3 | 3 | 4(3) | 2 | 2 |
Chaetotaxy of Abd. III | |||||
central mac | 2 | 1 | 1 | 1 | 1 |
lateral mac | 3 | 3 | 3 | 3 | 2? |
ms | not seen | not seen | present | not seen | ? |
Chaetotaxy of Abd. IV | |||||
central mac | 7 | 7‒9 | 6 | 6 | 4 |
lateral mac | 10–12 | 11 | 9 | 8 | ? |
Tenent hair | usually pointed | pointed | pointed | pointed | pointed |
Ungual inner teeth | 3 | 2 | 3 | 3 | 3 |
Unguiculus outer edge | serrate | serrate | serrate | 2–3 teeth | ? |
Ventral tube | |||||
anterior face | 9‒12 | ? | 12 | 10 | ? |
posterior face | 13 | ? | 20–31 | 20–30 | 7 |
lateral flap | 7(10) | ? | 9–12 | 7–8s(5c) | 6 |
Smooth chaetae trochanteral organ | 12–22 | 15–16 | 15–25 | 12–18 | 16 |
Chaetae on manubrial plaque | 4‒7 | 4 | 4‒10 | 3 | 5 |
Chaetae on ventro-distal part of manubrium | 11–15c | 13c | 15–25c | 8–10c | ? |
Mucronal spine | nearly reaching mucronal apex | nearly reaching mucronal apex | nearly reaching mucronal apex | nearly reaching mucronal apex | beyond mucronal apex |
Locality | Chumphon, Thailand | Satun, Thailand | Satun, Thailand | Satun, Thailand | Maui, Hawaii |
Coecobrya cf. hoefti (Schäffer, 1896)
Sources.
Altitude. > 2,000 m a.s.l. in Doi Inthanon, Chiang Mai province (
Habitat. No ecological data in Chiang Mai province; soil sample in mixed dry deciduous forest and deforested area in Chaiyaphum province.
Distribution. Doi Inthanon, Chiang Mai province, northern Thailand and Khon San district, Chaiyaphum province, northeastern Thailand.
Distribution outside Thailand. Europe.
Coecobrya guanophila Deharveng, 1990
Sources.
Type deposition.
Altitude. 458 m a.s.l.
Coordinates. 19°23.6386'N; 98°55.6864'E
Habitat. Dark zone of cave (Tham Chiang Dao) on bat guano.
Distribution. Chiang Dao district, Chiang Mai province, northern Thailand (only known from the type locality).
Coecobrya similis Deharveng, 1990
Sources.
Type deposition:
Altitude. 500 m a.s.l.
Coordinates. around Tham Chiang Dao (19°23.6386'N; 98°55.6864'E)
Habitat. Near the entrance of Tham Chiang Dao, litter and soil.
Distribution. Chiang Dao district, Chiang Mai province, northern Thailand (only known from the type locality).
Coecobrya lanna Zhang, Deharveng & Chen, 2009
Sources.
Type deposition. MNHM and NJAU.
Altitude. 1,720 m a.s.l.
Coordinates. 19°23.5213'N; 98°52.4899'E
Habitat. Forest litter at Doi Chiang Dao.
Distribution. Chiang Dao district, Chiang Mai province, northern Thailand (only known from the type locality).
Coecobrya cavicta Nilsai & Zhang, 2017
Source.
Type deposition.
Altitude. 115 m a.s.l.
Coordinates. 6°43.5816'N; 100°9.7494'E
Habitat. Dark zone of cave (Tham Ton Din) in wet and humid environment, near a stream bank, without bat guano.
Distribution. Khuan Don district, Satun province, southern Thailand (only known from the type locality).
Coecobrya chumphonensis Zhang & Nilsai, 2017
Source.
Type deposition.
Altitude. 70 m a.s.l.
Coordinates. 10°26.7841'N; 99°2.1018'E
Habitat. Dark zone of cave (Tham Chang Puak) on wet ground and rocks near a puddle; wet and humid environment, in an oligotrophic habitat without bat guano.
Distribution. Mueang district, Chumphon province, southern Thailand (only known from the type locality).
Coecobrya polychaeta Zhang & Nilsai, 2017
Source.
Type deposition.
Altitude. 23 m a.s.l.
Coordinates. 6°46.5246'N; 100°2.4966'E
Habitat. Dark zone of cave (Tham Phraya Bangsa) in a small chamber of muddy ground, wet and humid environment, in an oligotrophic habitat without bat guano.
Distribution. Mueang district, Satun province, southern Thailand (only known from the type locality).
Coecobrya cf. polychaeta Zhang & Nilsai, 2017
Source.
Altitude. 115 m a.s.l.
Coordinates. 6°43.5816'N; 100°9.7494'E
Habitat. Dark zone of cave (Tham Ton Din) along a stream bank, on stalagmites, muddy and clay substrate, gravels and rocks in wet and humid environment, without bat guano.
Distribution. Khuan Don district, Satun province, southern Thailand (only known from this cave).
Coecobrya donyoa Zhang & Jantarit, 2018
Source.
Type deposition.
Altitude. 65 m a.s.l.
Coordinates. 9°54.238'N; 99°2.685'E
Habitat. Dark zone of cave (Tham Don Yoa) on bat guano.
Distribution. Lang Suan district, Chumphon province, southern Thailand (only known from the type locality).
Coecobrya khaopaela Zhang & Jantarit, 2018
Source.
Type deposition.
Altitude. 300 m a.s.l.
Coordinates. 9°33.5599'N; 98°58.9364'E
Habitat. Dark zone of cave (Tham Khao Paela) on bat guano.
Distribution. Tha Chana district, Surat Thani province, southern Thailand (only known from the type locality).
Coecobrya khromwanaramica Zhang, 2018
Source.
Type deposition.
Altitude. 77 m a.s.l.
Coordinates. 8°46.194'N; 99°22.106'E
Habitat. Twilight to dark zone of a rather dry cave (Tham Khromwanaram) on bat guano.
Distribution. Ban Na San district, Surat Thani province, southern Thailand (only known from the type locality).
Coecobrya phanthuratensis Zhang & Jantarit, 2018
Source.
Type deposition.
Altitude. 82 m a.s.l.
Coordinates. 8°54.028'N; 98°31.498'E
Habitat. Twilight to dark zone of cave (Tham Phanthurat) on bat guano.
Distribution. Phanom district, Surat Thani province, southern Thailand (only known from the type locality).
Coecobrya promdami Zhang & Jantarit, 2018
Source.
Type deposition.
Altitude. 78 m a.s.l.
Coordinates. 9°12.293'N; 99°46.47'E
Habitat. Dark zone of humid cave (Tham Khao Wang Thong) on bat guano.
Distribution. Khanom district, Nakhon Si Thammarat province, southern Thailand (only known from the type locality).
Coecobrya ranongica Nilsai & Zhang, 2018
Source.
Type deposition.
Altitude. 52 m a.s.l.
Coordinates. 10°19.5745'N; 98°45.9012'E
Habitat. Twilight to dark zone of cave (Tham Phra Khayang) on bat guano.
Distribution. Kra Buri district, Ranong province, southern Thailand (only known from the type locality).
Coecobrya specusincola Zhang & Nilsai, 2018.
Source.
Type deposition.
Altitude. 160 m a.s.l.
Coordinates. 8°59.996'N; 99°46.692'E
Habitat. Dark zone of cave (Tham Khao Phab Pha) on scattered bat guano.
Distribution. Sichon district, Nakhon Si Thammarat province, southern Thailand (only known from the type locality).
This key includes C. sirindhornae sp. n. and all other species of Thailand which have long antennae (more than 2.5 times as long as the cephalic diagonal). All are cave restricted.
1 | Outer maxillary lobe with 3 sublobal hairs; a single chaeta m on labium | 2 |
– | Outer maxillary lobe with 4 sublobal hairs; two chaetae m on labium; claw with unpaired inner tooth | 3 |
2 | Labial chaetae as mrel1l2; claw without unpaired inner tooth | C. cavicta Nilsai & Zhang, 2017 |
– | Labial chaetae as mRel1l2, claw with unpaired inner tooth | C. chumphonensis Zhang & Nilsai, 2017 |
3 | Labial chaetae as M1m2rel1l2; antennae 5–7 times as long as cephalic diagonal; tita without a dorso-distal smooth chaeta in addition to the tenent hair; claw moderately slender | 4 |
– | Labial chaetae as m1m2rel1l2, ; antennae >8 times as long as cephalic diagonal; tita with a dorso-distal smooth chaeta in addition to the tenent hair; claw very slender | C. sirindhornae sp. n. |
4 | Postlabial chaeta X4 ciliate; mac a1 present on Abd. I | C. polychaeta Zhang & Nilsai, 2017 |
– | Postlabial chaeta X4 smooth; mac a1 absent on Abd. I | C. cf. polychaeta Zhang & Nilsai, 2017 |
Coecobrya is, among Collembola, one of the genera that exhibit most frequently morphological modifications considered to be linked to subterranean environments (
The first highly troglomorphic Coecobrya, C. nupa, was described by Christiansen and Bellinger in 1992 from Hawaii. Later on,
As Thailand is under tropical climate, cave temperature in the dark zone of lowland Thai peninsula is warm. It ranges from 23 to 30 degree Celsius (an average of 25‒26 degree Celsius for the caves studied so far) while humidity is approx. 70–93% (unpublished observations). The new highly troglomorphic species described here is restricted to a single small chamber (0.8 × 3‒4 m) without organic resources, where humidity is very high (> 90%), but temperature is only 23‒24 degree Celsius, a value very low in caves of the region. The karst where the cave is developed is a small outcrop of low elevation, that cannot account for the low temperature observed. The other troglomorphic species of southern Thailand were also often collected in relatively low temperature microhabitats. These rough ecological data suggest that highly troglomorphic Collembola may require a specific environment in tropical caves, not only oligotrophic habitats. This remains to be investigated in more detail.
Three of the four most troglomorphic Coecobrya known in Thailand (C. sirindhornae sp. n., C. polychaeta, and C. cavicta) are limited to Satun caves. The fourth one is C. chumphonensis, from the province of Chumphon, 380 km to the north. The karst of Satun highlights the region’s most complete Palaeozoic geological history and outstanding features of karst landscape that have developed during long geological periods (
This exceptional richness in troglomorphic species of the karst of Satun highlights that the country’s first UNESCO Global Geopark (Satun Geopark) is also a spot of major biological importance. Regarding C. sirindhornae sp. n. itself, its area of occurrence is extremely reduced to a small chamber in a small cave of a small isolated hill. The hill is approx. 110 × 250 m and distant of approximately 400 m from the closest neighbouring limestone hill, which is approx. 500 × 2500 m The cave is occupied by a temple and surrounded by agricultural lands. Two caves of the same small hill were surveyed but did not provide any specimen of the new species. All this makes C. sirindhornae sp. n. highly vulnerable in the face of growing anthropic disturbance which are spreading over Thailand karsts, especially in lowland. The survey of neighbouring hill caves is on the way to better evaluate the fine distribution and vulnerability of this remarkable species. In a broader context, this discovery underlines a need higher than expected for rapid evaluation and assessment of the cave fauna of the numerous karstic outcrops spread on the plain of southern Thailand, and of the current threats affecting these karsts.
We would like to thank Areeruk Nilsai and Katthaleeya Surakhamhaeng for their kind assistance in the fieldwork and improving some figures. Anne Bedos is thanked for her review of the initial draft, and Mark Judson for style improvement of part of the manuscript. This work was supported by Prince of Songkla University (PSU-15443: SCI580885S) and the Thailand Research Fund (TRG-5880189 and MRG-6080287) for the first author.