BIODIVERSITY AND BIOGEOGRAPHY
J. Limnol., 2013; 72(s2): 327-344
DOI: 10.4081/jlimnol.2013.s2.e16
The groundwater-dwelling fauna of South East Asia
STYGOBIONTS
Anton BRANCELJ,1,2* Chaichat BOONYANUSITH,3 Santi WATIROYRAM,4 La-orsri SANOAMUANG3,5
National Institute of Biology, Večna pot 111, 1000 Ljubljana; 2Faculty for Environmental Sciences, University of Nova Gorica, Vipavska
c. 13, 5000 Nova Gorica, Slovenia; 3Applied Taxonomic Research Center, Faculty of Science, Khon Kaen University, Khon Kaen
40002; 4Division of Science, Faculty of Liberal Arts and Science, Nakhon Phanom University, Nakhon Phanom 48000; 5Faculty of
Science, Mahasarakham University, Maha Sarakham 44150, Thailand
*Corresponding author: anton.brancelj@nib.si
1
INTRODUCTION
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Received: February 2013. Accepted: September 2013.
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Key words: Caves, groundwater fauna, karst, Southeast Asia, stygobionts.
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More than half of the stygobionts (i.e. obligate
groundwater dwellers) reported globally are known from
Europe. In total, there are about 3800 known stygobionts
worldwide and about 2000 taxa are reported from groundwater in Europe (Gibert and Culver, 2009). This is the result of long-term research in fissured (i.e. karstic) and
porous (i.e. alluvium, interstitial) aquifers in Europe.
The first information related to stygobionts arose from
caves and karstic springs, because animals there are relatively larger, more noticeable and easier to collect than
animals in porous aquifers. Records were made sporadically as a result of occasional visits to caves or investigation of wells and were focussed mainly on larger
body-sized groups like Isopoda, Amphipoda, Decapoda
and Pisces. Some rare records on micro-crustacea from
caves or wells have been existing for a long time as well
[Tab. 1; after Botosaneanu (1986)]. Among the first
records of groundwater fauna were those of Copepoda
from the drinking water system of St. Petersburg from
1866 (although specimens recorded there were actually
stygophiles) and of Bathynellaceae from a similar environment in Prague (in 1882) (Botosaneanu, 1986; Camacho, 1992).
Among the first described stygobionts (some of them
were actually stygophiles) were amphibians (Proteus anguinus Laurenti, 1768), fish [Monopterus albus (Zuiew,
1793)] and amphipods [Gammarus minus (Say, 1818),
Niphargus puteanus (C.L. Koch, 1836)], followed by
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ABSTRACT
Groundwater fauna consists of organisms that are adapted to live their whole life-time in different types of groundwater (=aquifers):
with fissured (karstic) and porous (alluvium) types as the most common. About 3800 species of obligate groundwater species (stygobionts) have been recorded worldwide and 2000 of them from groundwater in Europe. Before 1970, 19 species of stygobionts were known
from Southeast Asia. After 1980, the number of stygobionts from this region started to increase, and, at present, 122 stygobionts are
known here. Most of them are crustaceans, with the Copepoda, Isopoda, Amphipoda and Decapoda as the most abundant groups. Intensification of research on groundwater fauna can considerably increase the total number of stygobionts known from the region, which
could rises up to several times the current tally if the intensity of research was comparable with that in Europe.
crabs and shrimps [Orconeces pellucidus (Tellkampf,
1844), Troglocaris anophthalmus (Kollar, 1848)]. In contrast, stygobiotic Calanoida, also present in Southeast
(SE) Asia, have been found just recently [Microdiaptomus
cokeri (Osorio Tafall, 1942)] (Tab. 1). The main reason
for their late discovery, is the generally rather low numbers of freshwater stygobiotic Calanoida (Brancelj and
Dumont, 2007).
The intensity of research related to groundwater fauna
increased after the First World War and since then it has
been increasing, not only in Europe but worldwide. Most
recently, among the most intensive projects on groundwater and its fauna, which included both types of aquifers,
was the project Protocol for the Assessment and Conservation of Aquatic Life in the Subsurface (PASCALIS;
available from: http://pascalis-project.com/) that was conducted in Europe during the period 2002-2005 (Deharveng et al., 2009; Stoch and Galassi, 2010). The project
revealed that even in areas with intensive and continuous
research of groundwater fauna there was still a big potential for discovering new species. In six European regions
with a total area of 11,777 km2, 217 species were known
before project PASCALIS, and after the project the number increased to 379, with 109 new species for those six
regions, including some that were new to science (Deharveng et al., 2009; Dole-Olivier et al., 2009). For example,
intensive and systematic sampling of porous aquifers
along the rivers, which were included in the PASCALIS
project, resulted in a discovery of rich population of two
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Tab. 1. List of the first three stygobiotic species of each higher taxonomic group described and present elsewhere in the world. Representatives of higher taxonomic groups are also present in Southeast Asia but with different species [data from Botosaneanu (1986)].
Ostracoda
4
Pseudocandona eremita
(Vejdovsky, 1880)
Central and South Europe
Copepoda
Calanoida
5
Microdiaptomus cokeri
Osorio Tafall, 1942
Mexico
11
12
13
14
Sphaeromicola topsenti
Paris, 1916
France
Pseudocandona zschokkei
(Wolf, 1919)
West and Central Europe
Speodiaptomus birsteini
Borutsky, 1962
Krim peninsula (Ukraine)
Ridgewayia marki
(Esterly, 1911) - anchialine,
Bermuda islands
Nitocrella hirta
Chappuis, 1923
Europe
Anaspides tasmaniae
(Thomson, 1893)
Tasmania (Australia)
Bathynella chappuisi
Delachaux, 1920
Europe
Spahaeromides raymondi
Dollfus, 1897
France
Faucheria faucheri
(Dolphus and Virè, 1900)
France
Caecosphaeroma virei
Dollfus, 1896
France
Caecosphaeroma burgundum
Dollfus, 1896
France
Cyanthura curassavica
Stork, 1940
Central America
Cyanthura milloti
Chappuis, Delamare Deboutteville and Paulian, 1956
Reunion island
Caecidotea nickajackensis
Packard, 1881
Tennessee (USA)
Asellus hilgendorfi
Bovallius, 1886
Japan
Microcerberus remanei
Chappuis and Delamare, 1952
Mediterranean area
Microcerberus delamarei
Remane and Siewing, 1953
Brazil
Neophreatoicus assimilis
Chilton, 1884
New Zealand
Phreatoicoides gracilis
Sayce, 1900
Australia
To be continued on next page.
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Anthuridea
Cruregens fontanus
Chilton, 1881
New Zealand
Asellota
Caecidotea stygia
Packard, 1871
Central part of USA
Microcerberidae
Microcerberus stygius
Karaman, 1933
Macedonia
Phreatoicidea
Phreatoicus typicus
Chilton, 1882
New Zealand
Eucyclops terras
(Graeter, 1907)
Switzerland
Bryocamptus pyrenaicus
(Chappuis, 1923)
France, Slovenia
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Sphaeromatidae
Monolistra caeca
Gerstaecker, 1856
Slovenia
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Isopoda
Cirolanidae
9
Cirolanides texensis
Benedict, 1896
Texas (USA)
10
Trichodrilus cantabrigensis
Beddard, 1908
United Kingdom
Acanthocyclops venustus
(Norman and Scott, 1906)
Europe
Harpacticoida
Parastenocaris fontinalis
Schnitter and Chappuis, 1915
Europe
Syncarida
8
Bathynella natans
Vejdovsky, 1882
Europe
Trichodrilus intermedius
Fauvel, 1903
France
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7
Cyclopoida
Diacyclops languidoides
(Lilljeborg, 1901)
Europe
Criconema minor
(Scheider, 1940)
Slovenia
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6
Thalassoalamus aquaedulcis
Schneider, 1940
Slovenia
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Oligochaeta
3
Trichodrilus pragensis
Vejdovsky, 1875
Czech lands
Phagocata olivacea
(Schmidt, 1862)
Southeast Adriatic coast
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Nematoda
2
Pseudorhablolaimus limnophilus
Soos, 1937
Hungary, Austria
Dendrocoelum nausicae
Schmidt, 1861
South Europe and Anatolia
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Turbellaria
1
Phagocata vitta
(Duges, 1830)
Europe, the Alps, Balkan
Groundwater-dwelling fauna of SE Asia
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Tab. 1. Continued from previous page.
17
18
Melitidae
Eriopsia elongata
(Bruzelius, 1859)
Europe, USA
Niphargidae
Niphargus puteanus
(C.L. Koch, 1836)
Germany, Switzerland
Crangonyctidae
Crangonyx subterraneus
Bate, 1859
West and Central Europe
Thermosbaenacea
19
Thermosbaena mirabilis
Monod, 1924
Tunisia
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Coleoptera
24
Siettitia balsetensis
Abielle de Perrin, 1904
France
Pisces
25
Taenioides anguillaris
(Linnè, 1758)
China
Niphargus longicaudatus
A. Costa, 1851
Italy
Stygobromus tenuis
(Smith, 1874)
East coast of USA
Bactrurus mucronatus
(Forbes, 1876)
Central part of USA
Monodella argentarii
Stella, 1951
Italy
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Caridina japonica
De Man, 1892
Japan
Orconeces inermis
Cope, 1872
Kentucky, Indiana (USA)
Cambarus hamulatus
(Cope, 1881)
Alabama, Tennessee (USA)
Sesarmoides jacobsoni
(Ihle, 1912)
Central Java, Indonesia
Sesarmoides verleyi
(Rathbun, 1914)
Jamaica
Frontipodopsis staheli
Walter, 1919
Central and South America
Sczizobates disjunctus
(Walter, 1925)
Argentina
Siettitia avenionensis
Guignot, 1925
France
Uvarus chappuisi
(Peschet, 1932)
Burkina Faso
Monopterus albus
(Zuiew, 1793)
Mjanmar, China, Japan
Trypauchen vagina
(Bloch and Schneider, 1801)
Taiwan, China
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Barbouria cubensis
(Von Martens, 1872)
Cuba
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Acarina
Hydrachnida
23
Wandesia thori
(Schecthel, 1912)
Europe
Niphargus stygius
(Schiödte, 1847)
Slovenia
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Reptantia
Orconeces pellucidus
(Tellkampf, 1844)
Tennessee (USA)
Brachyura
Thelphusula bidiens
(Lanchester, 1900)
Sarawak, Borneo
Pseudoniphargus africanus
Chevereux, 1901
Algeria
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22
Eriopsella sechellensis
(Chevreux, 1901)
Seychelles
Monodella stygicola
Ruffo, 1949
Italy
Decapoda
Natantia
20
Troglocaris anophthalmus
(Kollar, 1848)
Slovenia, Italy
21
Sarathrogammarus guernei
(Chevreux, 1889)
Azores (Portugal)
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16
Rhipidogammarus rhipidophorus
(Catta, 1878)
Mediterranean area
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Amphipoda
Gammaridae
15
Gammarus minus
Say, 1818
Central part of USA
species of stygophilic groundwater dwelling cladocerans.
In the past, both species were considered to be very rare,
but the many specimens collected during the project enabled a new genus – Phreatalona, to be established (Van
Damme et al., 2008).
Other parts of the world remained rather cold spots for
a long time. Until 1964, information on relatively rich
troglobiotic/stygobiotic fauna existed only for Europe and
the SE USA. Other parts of the world, including SE Asia,
remained very poorly known, even three decades later
(Holsinger, 1993). Actually, most of the information on
cave-dwelling fauna from SE Asia was limited to terrestrial species (Deharveng, 2004). Among stygobiotic
fauna, at least one representative from each main group
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A. Brancelj et al.
Historical overview and present status of stygobionts
in Southeast Asia
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At the beginning of the 20th century only six stygobionts
were known from SE Asia; this increased to 20 species in
1970 and reached 22 species in 1986, when the first list of
global and regional stygobiotic fauna was compiled (Tab.
3; Botosaneanu, 1986). In the period between 1986 and
2001 the number of newly recorded species increased by
57 species (Juberthie and Decu, 2001) and in 2012 reached
a total number of 122 species included in 74 genera (Fig.
1). In this number are also species from anchialine caves
and some species which probably belong to the stygophiles.
Most of the newly recorded species were also new to science and thus described in adequate taxonomic papers.
The highest number of stygobionts so far recorded is
from Thailand (36 species) and the Philippines (35
species), followed by Indonesia and Malaysia (20 and 19
species, respectively), Vietnam (9 species), Cambodia (3
species), Laos (2 species) and Myanmar (1 species) (Tabs.
3 and 4).
Most of the species are recorded from a single location
or, less frequently, from several in close proximity to each
other (usually several kilometres). So far, only three
species from SE Asia are known from more than one
country (Attheyella vietnamica Borutzky, 1967: Vietnam
and Thailand; Theosbaena cambodjiana Cals and Boutin,
1985: Cambodia and Thailand; Parhippolyte uveae Borradaile, 1899: Indonesia and Philippines).
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Southeast Asia includes the countries of Cambodia,
Laos, Burma (Myanmar), Thailand, Vietnam and peninsular Malaysia. It also includes the maritime areas of SE
Asia: Brunei, East Malaysia, East Timor, Indonesia, the
Philippines and Singapore (Wikipedia, 2013). Total land
area is about 4,300,000 km2, 408,000 km2 (9.7%) of
which is karstic (Day and Urich, 2000; Tab. 2). Apart from
the karstic areas, there are also vast alluvial areas, with an
array of potential habitats for stygobiotic organisms (Gibert et al., 1990).
Data on stygobiotic fauna from the countries of SE Asia
was collected from various literature sources. For the period
up to 1986, the source was Stygofauna Mundi (Botosaneanu, 1986), where all relevant literature on groundwater fauna worldwide is presented till 1986. For the period
between 1986 and 2001 the source was Encyclopaedia
RESULTS
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METHODS
Biospeleologica (Juberthie and Decu, 2001). After 2001,
individual papers on fauna from SE Asia were used.
To present the intensity of research on stygofauna in
SE Asia, a cumulative curve over time was constructed
by adding each record of a new stygobiotic species in the
region to the previous, already recorded taxa.
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of stygobionts so far recorded in SE Asia had already been
known from elsewhere before the beginning of the 20th
century (Tab. 1). This is an additional indication that stygobiotic fauna in SE Asia was not adequately sampled
since relatively recently, i.e. after the 1970s.
More recent inventories revealed that about 160 stygobiotic taxa are known from SE Asia and the Indian subcontinent combined (Gibert and Culver, 2009). From the
Indian sub-continent, about 50 stygobionts are known;
there, several new stygobionts – especially among the
micro-crustaceans (Copepoda and Syncarida) – were recently found to live in porous aquifers (Ranga Reddy and
Defaye, 2008; Ranga Reddy et al., 2008; Ranga Reddy
and Schminke, 2009).
In the present paper a more detailed analysis of stygobiotic fauna in SE Asia is presented, with special emphasis
on the most recent investigation of epikarst in Thailand
and Vietnam.
Tab. 2. Extent of karstic area per country in Southeast Asia [after
Day and Urich (2000)].
Country
Cambodia
Indonesia
Laos
Malaysia
Myanmar
Philippines
Thailand
Vietnam
Total
Country area
(km2)
181,035
1,904,569
236,800
131,598
676,578
300,000
513,120
331,689
4,275,389
Karstic area
(km2)
(%)
20,000
145,000
30,000
18,000
80,000
35,000
20,000
60,000
408,000
11.0
7.6
12.7
13.7
11.8
11.7
3.9
18.1
9.7
Fig. 1. Cumulative number of stygobiotic taxa recorded in
Southeast Asia from 1820 up to 2012.
Elaphoidella jaesornenis Watiroyram, Brancelj and
Sanoamuang, 2013
Elaphoidella margaritae Pesce and Apostolov, 1985
(Pesce and Apostolov, 1985)
Elaphoidella namnaoensis Brancelj, Watiroyram and
Sanoamuang, 2010
Elaphoidella thailadensis Watiroyram, Brancelj and
Sanoamuang, 2013
Elaphoidella vietnamica Borutzky 1967
Epactophanes philippinus Bruno and Cottarelli, 1999
(Bruno and Cottarelli, 1999)
Fierscyclops solaris Boonyanusith, Brancelj and
Sanoamuang, 2013
Fierscyclops tanasosriensis Boonyanusith, Brancelj and
Sanoamuang, 2013
Boholina crasicephala Fosshagen, 1989
Boholina purgata Fosshagen, 1989
Bryocyclops maewaensis Watiroyram, Brancelj and
Sanoamuang, 2012
Elaphoidella bidens decorata (Sars, 1904)
Copepoda (22 taxa)
Asiacaris dispar Cottarelli, Bruno and Berera, 2010
(Cottarelli et al., 2010)
Attheyella (Canthosella) vietnamica Borutzky, 1967
Ostracoda (2 taxa)
Batucypretta paradoxa Victor and Fernando, 1980
Candonopsis putealis Klie, 1932
Oligochaeta (1 taxon)
Haplotaxis glandularis Yamaguchi, 1953
Nematoda (1 taxon)
Dorylaiumus selengorensis De Man, ?
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x
Location
Batu caves near Kuala Lumpur, Gombak district
Batu caves near Kuala Lumpur, Gombak district
Well, Bogor island
x
Cave
Spring
To be continued on next page.
Wat Yang Kao temple, Sangkhlaburi district,
Kanchanaburi province
Kaeo Sawan Badan cave, Sangkhlaburi district,
Kanchanaburi province
Tham Yai Nam Nao cave, Nam Nao National Park,
Nam Nao district, Phetchabun province
Cave
Tham Khun cave, Noen Maprang district, Phitsanulok
province
Cave Cave in North Vietnam, Lac Thuy district, Hoa Bin province
Interstitial
Phreatic, Matitunao river, Cebu island
Cave
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Than Sadet river, Pha-ngan island,
Surat Thani province
x
Cave
Cave in NorthVietnam, Lac Thuy district,
Hoa Bin province; Tham Bot Wangna cave,
Noen Maprang district, Phitsanulok province
Anchialine cave
San Vicent cave, San Vicente
Anchialine cave
San Vicent cave, San Vicente
Cave
Tham Nam Phar Ngam cave, Mae Wa National Park,
Mae Phrik district, Lampang province
Cave
Pauh Cave, Bukttinggi; Vijer cave near botanic garden;
several caves in Kanchanaburi province
Cave Tham Phar Ngam cave, Jaesorn National Park, Wang Nuea
district, Lampang province
Well
Wells on Phuket island, Phuket province
Hyporheic
Cave
Spring
Cave Tham Kubio cave, Chum Phae district, Khon Kaen province
Cave
Cave
Batu cave near Kuala Lumpur, Gombak district
Cave Tham Kubio cave, Chum Phae district, Khon Kaen province
Tham Phulu cave, Muang district, Phang Nga province
Cave
Gua Tanette cave, Maros island, Sulawesi
Cave
Water Polo cave, Gunung Mulu National Park,
Sarawak, Borneo
Country
Habitat
Cambodia Indonesia Laos Malaysia Myanmar Philippines Thailand Vietnam
Dugesia leclerci Kawakatsu and Mitchell, 1995
Mitchellia sarawakana Kawakatsu and Chapman, 1983
Turbellaria (4 taxa)
Dugesia batuensis Ball, 1970
Dugesia deharvengi Kawakatsu and Mitchell, 1989
Taxa
Tab. 3. List of stygobiotic taxa for Southeast Asia, locations of records and habitats.
Groundwater-dwelling fauna of SE Asia
331
Stenasellus foresti Magniez, 2002
Stenasellus covillae Magniez, 1987
Stenasellus deharvengi Magniez, 1991
Stenasellus boutini Magniez, 1991
Stenasellus brignolii Pesce and Argano, 1981
Stenasellus cambodianus Boutin and Magniez, 1985
Stenasellus chapmani Magniez, 1982
x
x
x
x
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N
x
x
x
x
x
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x
x
x
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x
Cave
Cave
Cave
Cave
Spring
Cave
Cave
Cave
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Interstitial
Cave
Interstitial
Cave
Cave
Cave
To be continued on next page.
Interstitial 1.3 m deep, Bambu river,
Papua New Guinea, Lae Morobe province
Tham Phanthurat cave in Khao Sok National Park,
Phanom district, Surat Thani province
Caves in Batammbang province
Spring, Phuket island, Phuket province
Cave near Kampong Trach district, Kampot province,
Snake cave, Water Polo cave,
New High Level cave, Sarawak, Borneo
Bat Quarry cave, Aceh Besar, Sumatra
Tham Keao cave near Nong Bua Daeng,
Phakdi Chumphon district, Chaiyaphum province
Ngalau Surat cave, Ngalu Pelayangan cave, Sumatra
Sungai Masalong river, Sabah, Borneo
Tham Yai Nam Nao cave, Nam Nao National Park,
Nam Nao district, Phetchabun province
Cave, Rom island
Batu caves near Kuala Lumpur, Gombak district
Hang Trinh Nu cave, Bo Hon island
Shore of lake Wisdom, New Guinea
Cave
Tham Rusi cave, Muang district, Phang Nga province
Anchialine
Cave on islet north of Koron island
cave
Anchialine cave
Cave, Palau islands, Republic of Palau
Cave Gua Air Jernih cave, Gunung Mulu National Park; Borneo
Cave, spring
Caesar’s cave, well, Batuan, Bohol island
x
x
Interstitial
Interstitial
Phreatic, Mindoro island
Location
Cave
Dang Water cave, Cuc Phuong National Park, Ha Noi
Therm. spring
Salt thermal spring, Kuripan, Java
x Anchialine
Cave, Ninh Binh province
cave
x Anchialine
Cave, Ninh Binh province
cave
Cave
Batu caves near Kuala Lumpur, Gombak district
Interstitial
Phreatic near Talipanan village, Mindoro island
x
Country
Habitat
Cambodia Indonesia Laos Malaysia Myanmar Philippines Thailand Vietnam
Isopoda (21 taxa)
Annina fustis (Bowman and Iliffe, 1991)
Anopsilana conditoria Bruce and Iliffe, 1992
(Bruce and Iliffe, 1992)
Anopsilana lingua Bowman and Iliffe, 1987
Cyathura (Stygocyathura) chapmani Andreev, 1982
Cyathura (Stygocyathura) filipinica Botosaneanu and
Sket, 1999 (Botosaneanu and Sket, 1999)
Cyathura (Stygocyathura) papuae Weagle, Coleman and
Hosse, 1987 (Weagle et al., 1987)
Stenasellus bedosae Magniez, 1991
Syncarida (5 taxa)
Batubathynella malaya (Sars, 1929)
Paraeobathynella vietnamensis Camacho, 2005
(Camacho, 2005)
Sabahbathynella wongi Schminke, 1988
Siambathynella laorsriae Camacho, Watiroyram and
Brancelj, 2011
Sketinella trontelji Camacho, 2005 (Camacho, 2005)
Parastenocaris arganoi Cottarelli and Mura, 1982
Parastenocaris mangyans Bruno and Cottarelli, 1999
(Bruno and Cottarelli, 1999)
Parastenocaris distincta Cottarelli, Bruno and
Berera, 2006 (Cottarelli et al., 2006)
Phyllognathopus bassoti Rouch, 1972
Nitocra vietnamensis Tran and Chang, 2012
Hadodiaptomus dumonti Brancelj, 2005
Halicyclops thermophilus Kiefer, 1929
Microarthridion thanhi Tran and Chang, 2012
Taxa
Tab. 3. Continued from previous page.
332
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Tab. 3. Continued from previous page.
Adelana chapmani (Holthuis, 1979)
Arachnothelphusa rhadamanthysi (Ng and Goh, 1978)
Archipelothelphusa cavernicola Takeda, 1983
Decapoda (Natantia, Reptatntia and Brachyura) (33 taxa)
Thermosbaenacea (2 taxa)
Theosbaena cambodjiana Cals and Boutin, 1985
Thermosbaena sp.
Flagitopsia fluviatilis (Stock, 1991)
Paraniphargus ruttneri Schellenberg, 1931
Psammogammarus fluviatilis Stock, 1991
Seborgia vietnamica Jaume, Sket and Boxshall, 2009
(Jaume et al., 2009)
Tegano barnadi Sawicki and Holsinger, 2005
Eriopsia philippensis (Chilton, 1921)
Cottarellia minima Ruffo, 1994
Bollegidia sootai (Coineau and Rao, 1972)
Bogidiella thai Botosaneanu and & Noteboom, 1988
Bogidiella deharvengi Stock and Botosaneanu, 1988
Bogidiella (Medigidiella) sarawacensis Stock, 1983
Bogidiella daccordii Ruffo, 1994
Amphipoda (13 taxa)
Aequigidiella aquilifera Botosaneanu and Stock, 1989
Stenasellus javanicus Magniez and Rahmadi, 2006
(Magniez and Rahmadi, 2006)
Stenasellus mongnatei Magniez and Pantivong, 2005
(Magniez and Pantivong, 2005)
Stenasellus monodi Magniez, 2000
Stenasellus rigali Magniez, 1991
Stenasellus stocki Magniez, 2001
Stenasellus strinatii Magniez, 1991
Thalandoniscus annae Dalens, 1989
Taxa
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x
x
x
x
x
Interstitial
Interstitial
Cave
Cave
Cave
Interstitial
Cave
Airport well cave, Peleliu island
Tham Phulu cave, Muang district, Phang Nga province;
Tham Keao cave, Phakdi Chumphon district,
Chaiyaphum province
Phreatic on Palawan island, St. Paul subterranean
river Nat Park, Western Visayas
Batu Lubang cave, Halmashera island
Niah Great cave, Batu Niah National Park, Sarawak,
Borneo; Deer cave, Gunung Mulu National Park,
Sarawak, Borneo
Tham Poung Chang cave, Muang district,
Phang Nga province
Interstitial, Sabang beach, eastern Mindoro,
Palawan islands
Interstitial, Sabang beach, eastern Mindoro,
Palawan islands
Well near Los Baños, southern shore of Laguna de Bay,
Luzon island
Pagsanjan falls, Laguna province, Luzon island
Batu Lubang cave, Halmahera, east Java
Gravel bar near Pagsanjan falls, laguna
Cave Dong Duc Tie, Dao Van Gio island
Cave
Cave
Cave
To be continued on next page.
Niah Great cave, near Miri, Borneo
Simud Puteh cave, Sabah, Borneo
Quinapon-an cave, Antequera, Bohol island
Cave
Cave near Kampong Trach district, Kompot province
Cave Tham Kubio cave, Chum Phae district, Khon Kaen province
Cave
Interstitial
Cave
Interstitial
Cave
Well
on
ly
x
Tham Nam cave, Kaeng Khoi district, Saraburi province
Cikaray cave, Leuwi Kares island
Location
Cave
Ngalau Lagung cave, Sumatra
Cave Tham Kubio cave, Chum Phae district, Khon Kaen province
Cave
Ngalau Indah cave, Sumatra
Cave
Ngalu Baso cave, Ngalau Kamang cave, Sumatra
Cave
Springs near the Tham Tapan cave, Muang district,
Phang Nga province
Cave
Cave
Country
Habitat
Cambodia Indonesia Laos Malaysia Myanmar Philippines Thailand Vietnam
Groundwater-dwelling fauna of SE Asia
333
x
x
x
Phricothelphusa deharvengi Ng, 1988
Samarplax principe Husana, Tan and Kase, 2011
(Husana et al., 2011)
Sesarmoides cerberus (Holthuis, 1964)
Sesarmoides emdi Ng and Whitten, 1994
Sesarmoides jacobsoni (Ihle, 1912)
Stygothelphusa bidiensis (Lanchester, 1900)
Sundathelphusa cavernicola Takeda, 1983
Sundathelphusa boex Ng and Sket, 1996
(Ng and Sket, 1996)
Sundathelphusa hades Takeda and Ng, 2001
(Takeda and Ng, 2001)
Sundathelphusa lobo Husana, Naruse and Kase, 2009
Sundathelphusa sottoae Ng and Sket, 1996
(Ng and Sket, 1996)
Phaibulamon stilipes Ng, 1992
x
x
on
N
x
x
x
co
m
x
x
x
x
x
x
x
x
x
x
x
e
us
x
Bantakay cave, Luzon island
Marulas caves, Luzon island
Bautakay cave, Atimonau, Quezon province, Luzon island
Gua Tanette cave, Lubang Batu Neraka cave,
cave in Maros, Maros, Sulawesi
Deer cave, Green cave, Clearwater cave,
Gunung Mulu National Park, Sarawak, Borneo
Clearwater cave, cave of Winds, Wonder cave, Gunung
Api masiff, Gunung Mulu National Park, Sarawak, Borneo
Subterranean river near Santiago, Isabela province,
Luzon island; cave near Sitio Disiluad, Aglipay Quirino
province, Luzon island
Bantakay cave, Luzon island
Location
Cave, Nusa Lain island
Gua Paon cave, Nusa Penida island
Guwa Djamblang cave, Guwa Ningrng caves,
Bedojo district, Gunung Sewu, Java
Bau caves in the region of Bau and Sarawak, Borneo
Quinaponan cave, Ughob cave, Antequera, Bohol island
Castigio cave, Capiro springs and rivers near Batuan,
Bohol island
Latay cave, Agusan del Sur, Surigao del Sur, Mindanao
To be continued on next page.
Cave
Lobo cave, Samar, Jiabong
Cave, well Ughob cave, Bonugan cave, well, Batuan, Bohol island
Cave
Cave
Cave
Cave
on
ly
Cave
Cave
Cave
Cave Tham Tê cave, Thakhek district, Khammouane province
Anchialine Bat cave, Boracay island; Tagbaobo cave, Samal island
cave
Cave
Several caves, probably only in Gunung Sewu Karst
x
Cave
Cave in Phong Nha, Hang Toi, Quang Binh province
Cave
Tiniguaban cave, Gimaras, Tinigualban island;
Holmahera, Maluccas
Cave
Tham Nam Phrah Khoan cave, Sangkhlaburi district,
Kanchanaburi province
Cave Tham Poung Chang cave, Muang district, Phang Nga province
Anchialine cave
Principe cave, Eastern Visayas, Samar
Cave
x
ia
l
er
c
m
Cave
Cave
Cave
Cave
Cave
Cave
Cave
x
x
x
x
Country
Habitat
Cambodia Indonesia Laos Malaysia Myanmar Philippines Thailand Vietnam
Edoneus erwini Cai and Husana, 2009
(Cai and Husana, 2009)
Edoneus marulas Cai and Husana, 2009
(Cai and Husana, 2009)
Edoneus sketi Cai and Husana, 2009
(Cai and Husana, 2009)
Erebusa calobates Yeo and Ng, 1999
Karstarma philippinarum Husana, Naruse and Kase, 2010
(Husana et al., 2010)
Macrobrachium poeti Holthuis, 1984
Nemoron nomas Ng, 1996
Parhippolyte uveae Borradaile, 1899
Edoneus atheatus Holthuis, 1978
Cerberusa tipula Holthuis, 1979
Cerberusa coeca Holthuis, 1979
Archipelothelphusa longipes Balss, 1937
Cancrocaeca xenomorpha Ng, 1991 (Ng, 1991)
Taxa
Tab. 3. Continued from previous page.
334
A. Brancelj et al.
3
20
x
x
on
2
x
19
x
x
co
m
x
x
1
x
35
x
ia
l
er
c
m
x
Names of species and genera are as published in original papers; no taxonomic revisions are included in this analysis.
Total: 122 species
Silurus furnessi = Pterocryptis furnessi (Fowler, 1905)
Troglocyclocheilus khammouaensis Kottelat and
Bréhier, 1999
Schistura spekuli Kottelat, 2004
Schistura spiesi Vidthayanon and Kottelat, 2003
Schistura jarutanini Kottelat, 1990
Neolissochilus subterraneus Vidthayanon and
Kottelat, 2003
Pterocryptis buccata Ng and Kottelat, 1998
Puntius microps (Günther, 1868)
Schistura deansmarti Vidthayanon and Kottelat, 2003
Monopterus albus (Zuiew, 1793) (rice-field eel)
Nemacheilus oedipus Kottelat, 1988
Nemacheilus troglocatarctus Kottelat and Géry, 1989
Caecogobius cryptophthalmus Berti and Ercolini, 1991
Cryptotora thamicola (Kottelat, 1988)
Clarias nieuhofii Valenciennes, 1840
Pisces (15 taxa)
Barbus speleops Roberts, 1991
Coleoptera (1 taxon)
Siamoporus deharvengi Spangler, 1996
Acari/Hydrachnida (1 taxon)
Soldanellonyx monardi sarangensis Viets, 1929
Thelphusula styx Ng, 1989
N
x
x
36
x
x
x
x
x
x
x
e
us
x
x
x
10
x
Cave
Cave
Cave
Cave
Cave
Cave
Cave
Cave
Bikahan cave, Antequera, Bohol island
Quilas cave, Batuan, Bohol island
Location
Tham Phu Khieo cave, Nong Bua Daeng district,
Chaiyaphum province
Cave on Samar island
Susa cave, Pang Ma Pha district, Mae Hong Son province
Clearwater cave, Snake cave, Gunung Mulu National Park,
Sarawak, Borneo
Several caves along the country
Several caves in Pang Mapha district, Mae Hong Son province
Tham Wang Badan cave, Sai Yok district,
Kanchanaburi province
Tham Phra Wang Daeng cave, Noen Maprang district,
Phitsanulok province
Sai Yok Noi cave, Sai Yok district, Kanchanaburi province
Djamblang cave, Bedojo district, Gunung Sewu, Java
Tham Phra Sai Ngam cave, Noen Maprang district,
Phitsanulok province
Sao Hin cave, Thong Pha Phum district,
Kanchanaburi province
Tam Duong cave, Lai Chau province
Tham Phra Wang Daeng cave, Noen Maprang district,
Phitsanulok province
Logan’s cave, Sarawak, Borneo
Spring Nam Dôn, Thakhek district, Khammouane province
Tham Pulu cave, Muang district, Phang Nga province;
Tham Kubio cave, Chum Phae district, Khon Kaen province
Java
Langun cave, Samar, Calbiga
Caves at Bidi, Posih cave, Jambusan cave, Fairy cave,
near Bau
Bat cave, Gunung Mulu National Park, Sarawak, Borneo
on
ly
Cave
Cave
Cave
Cave
Cave
Cave
Cave
Cave
Cave
Spring
Cave
Cave
Cave
Cave
Cave
Country
Habitat
Cambodia Indonesia Laos Malaysia Myanmar Philippines Thailand Vietnam
Sundathelphusa urichie Ng and Sket, 1996 (Ng and
Sket, 1996)
Sundathelphusa vedeniki Ng and Sket, 1996 (Ng and
Sket, 1996)
Sundathelphusa waray Husana, Naruse and Kase, 2009
Thelphusula bidiens (Lanchaster, 1900)
Taxa
Tab. 3. Continued from previous page.
Groundwater-dwelling fauna of SE Asia
335
336
A. Brancelj et al.
on
ly
Structure of stygobiotic fauna in Southeast Asia
e
Thirteen higher taxonomic groups have been recorded
so far in SE Asia (including vertebrates, i.e. fish; Tab. 3).
The most abundant groups so far are the Decapoda
(Natantia, Reptantia and Brachyura), represented by 33
taxa (6+3+24 species, respectively), followed by Copepoda (22 species), Isopoda (20 species), Amphipoda (13
species), Pisces (10 species) and Syncarida (5 species).
Other groups (Turbellia, Nematoda, Oligochaeta, Ostracoda, Thermosbaenacea, Acari/Hydrachnida and
Coleoptera) are represented only with one to four species
each. Out of 74 genera with stygobionts, there are 56 genera where only one stygobiotic representative is known.
The number of species per certain group within a particular country varies considerably – from 1 to 17 (Tabs. 3
and 4). The group with the highest number of species per
country is the Decapoda in the Philippines, where 17
species are known, followed by ten species of Copepoda
from Thailand. Groups with seven species each per county
are the Amphipoda from the Philippines, the Decapoda
from Malaysia and the Isopoda from Thailand. Four groups
have six representatives per country: Copepoda in the
Philippines, Isopoda in Indonesia, Decapoda in Indonesia
and the Pisces in Thailand. The group with five species is
Copepoda in Vietnam, while Isopoda has four species in
the Philippines. There are 29 groups with only one or two
species known for each group and for each country.
The time series of stygobiotic records indicates that
there are 41 papers, where 48 authors (alone or as co-authors) contributed one single record on stygobiotic fauna;
17 of the records were published before 1980. The rest of
the records were contributions by 30 authors who
recorded/described two or more new species (Tab. 5).
Among those, two records by the same author were done
in 1900 (Lanchester, Decapoda) and additional two in
1967 (Borutzky, Copepoda). Up to 1986, 15 more records
N
on
co
m
m
er
c
Revision of biospeleological studies and the cavedwelling fauna of Thailand has been previously done by
Deharveng and Bedos (2001) and more recently the terrestrial cave-dwelling fauna was reviewed by Ellis (2006,
2012). Investigations on cave-dwelling fauna have been
carried out since the early 20th century but focussed only
on terrestrial fauna from some caves in southernmost Thailand (Annandale et al., 1913). Stenasellus brignoli Pesce
and Argano, 1981 was the first stygobiotic species described for Thailand. It was collected from freshwater wells
in Phuket province in 1980 (Pesce and Argano, 1981).
After 1983, the number of biospeleological studies increased as French researchers from the Association
Pyrénéenne de Spéléologie started their caving activities
in Thailand. In 2001, when Deharveng and Bedos (2001)
provided the list of aquatic cave-dwelling fauna from
Thailand, the list included 21 invertebrate and vertebrate
species belonging to 9 higher taxonomic groups (Tab. 3).
The ecology and biology of more than half of those
species were not known (Deharveng and Bedos, 2000).
The most abundant on the list were Isopoda (5 species)
and the Pisces (6 species). In addition, there were two
species of Amphipoda and two of Decapoda. Several
groups (flatworms, oligochaetes, copepods, syncarids,
thermosbaenaceans and coleopterans) were represented
with only one species and all of them were endemic to
Thailand (Tab. 3).
After 2000, 14 new stygobiont species were discovered, among them four new species of fish (Vidthayanon
and Kottelat, 2003; Kottelat, 2004), which increased the
number of stygobiotic fishes in Thailand from six to ten
species. In the last 10 years significant progress has been
made in research on the groundwater Copepoda (Fig. 2A
and 2B). Before then, only one stygobiotic species was
known from the freshwater interstitial habitat
(Elaphoidella margaritae, Pesce and Apostolov, 1985)
(Tab. 3). The first cave-dwelling species found in Thailand was Elaphoidella namnaoensis Brancelj, Watiroyram
us
Historical overview and present status in Thailand
and Sanoamuang, 2010 from a cave in Nam Nao National
Park (Phetchabun province) (Brancelj et al., 2010) and
the most recently described species are Bryocyclops maewaensis Watiroyram, Brancelj and Sanoamuang, 2012
(Watiroyram et. al., 2012) and two species from the genus
Fierscyclops published in this volume (Boonyanusith et.
al., 2013). Three papers with descriptions of six new
species (but not included in this analysis) have been already submitted to journals (Boonyanusith, personal communication; Watiroyram, personal communication).
Intensive research on cave environments, especially on
epikarst, conducted during the PhD studies of two of the
co-authors (CB and SW), revealed that stygobiotic fauna
is very rich and not only present in Thailand but also in
nearby countries (Vietnam and Laos) (Fig. 2C-G). It includes, apart from the Copepoda also Ostracoda, Syncarida, Isopoda and Amphipoda.
ia
l
One-hundred and one species from the list of stygobionts in SE Asia living in karstic habitats are recorded
from caves (8 of them from anchialine caves), four species
are recorded from karstic springs and one from a thermal
spring. Two species were found both in caves and wells,
while only one was found from a well. In addition, 13
species were recorded only from porous aquifers (i.e. interstitial/hyporheic environment), where micro-crustaceans (body size ≤1 mm) prevailed. In contrast to
porous environments, in karstic caves and springs a wide
array of body size could be found – from small-body sized
Nematoda and Copepoda (body size <1 mm) to largebody sized organisms like Decapoda and Pisces (body
size >10 cm).
337
Groundwater-dwelling fauna of SE Asia
Tab. 4. Number of stygobiotic species per higher taxonomic group per country.
Cambodia
Species (n)
Groups (n)
Turbellaria
Nematoda
Oligochaeta
Ostracoda
Copepoda
Syncarida
Isopoda
Amphipoda
Thermosbaenacea
Decapoda
Acari/Hydrachnida
Coleoptera
Pisces
3
2
Indonesia
Laos
20
8
1
2
2
Malaysia
19
9
2
1
1
2
2
6
2
1
6
1
1
1
Philippines
1
1
2
2
1
1
6
4
7
7
1
35
6
17
2
1
1
Thailand
36
10
1
Vietnam
1
10
1
7
2
2
2
1
9
on
ly
1
Myanmar
10
4
5
2
1
1
1
Decapoda, Pisces
Isopoda
Pisces
Syncarida, Copepoda
Decapoda
Copepoda
Decapoda
Decapoda, Ampipoda, Isopoda
Amphipoda, Isopoda
Copepoda
Syncarida, Copepoda
Amhipoda
Copepoda
Decapoda
Decapoda
Syncarida
Isopoda
Turbellaria
Decapoda
Decapoda
Pisces
Copepoda
Thermosbaeanaceae, Isopoda
Isopoda
Copepoda
Copepoda
Turbellaria
Isopoda, Copepoda
Amphipoda
Copepoda
Turbellaria
Turbellaria
Nematoda
Oligochaeta
Ostracoda
Ostracoda
Ostracoda
Copepoda
Copepoda
er
c
m
co
m
on
N
Ng - 13
Magniez - 12
Kottelat - 10
Brancelj - 7
Husana - 7
Cottarelli - 6
Holthuis - 6
Sket - 6
Botosaneanu - 5
Sanoamuang - 5
Watiroyram - 5
Stock - 5
Bruno - 4
Kase - 4
Cai - 3
Camacho - 3
Ilife - 3
Kawakatsu - 3
Naruse - 3
Takeda - 3
Vidthayanon - 3
Borutzky - 2
Boutin - 2
Bowman - 2
Chang - 2
Fosshagen - 2
Mitchell - 2
Pesce - 2
Ruffo - 2
Tran - 2
Ball - 1
Chapman - 1
De Man - 1
Yamaguchi - 1
Fernando - 1
Klie - 1
Victor - 1
Apostolov - 1
Kiefer - 1
Group(s) studied
Author - no. of taxa recorded
Mura - 1
Rouch - 1
Schminke - 1
Andreev - 1
Argano - 1
Bruce - 1
Coleman - 1
Hosse - 1
Pantivong - 1
Rahmadi - 1
Weagle - 1
Boxshall - 1
Chilton - 1
Coineau - 1
Holsinger - 1
Jaume - 1
Noteboom - 1
Rao - 1
Sawicki - 1
Schellenberg - 1
Cals - 1
Balss - 1
Borradaile - 1
Goh - 1
Ihle - 1
Tan - 1
Whitten - 1
Yeo - 1
Viets - 1
Spangler - 1
Berti - 1
Bréhier - 1
Ercolini - 1
Fowler - 1
Géry - 1
Günther - 1
Roberts - 1
Valenciennes - 1
Zuiew - 1
ia
l
Author - no. of taxa recorded
us
e
Tab. 5. Authors who published papers on stygofauna from Southeast Asia and their contribution to the knowledge of a particular group
(most of them as author or co-author of taxonomic papers) (for details on recorded taxa see Tab. 3).
Group(s) studied
Copepoda
Copepoda
Syncarida
Isopoda
Isopoda
Isopoda
Isopoda
Isopoda
Isopoda
Isopoda
Isopoda
Amphipoda
Amphipoda
Amphipoda
Amphipoda
Amphipoda
Amphipoda
Amphipoda
Amphipoda
Amphipoda
Thermosbaeanaceae
Decapoda
Decapoda
Decapoda
Decapoda
Decapoda
Decapoda
Decapoda
Acari
Coleoptera
Pisces
Pisces
Pisces
Pisces
Pisces
Pisces
Pisces
Pisces
Pisces
338
N
on
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m
m
er
c
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l
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A. Brancelj et al.
Fig. 2. Epikarst stygobionts and habitats in Southeast Asia. A) Scanning electron microscopy image of a female representative of
epikarst copepods, from the order Cyclopoida - Bryocyclops maewaensis Watiroyram, Brancelj and Sanoamuang, 2012 (photo by Santi
Watiroyram); B) light microscopy image of a female representative of the epikarst copepods, from the order Harpacticoida – Paramorariopsis irenae Brancelj, 2006 (photo by Anton Brancelj); C) entrance into a karstic cave (view from outside) in Thailand (photo by Santi
Watiroyram); D) entrance into a karstic cave (view from inside) from Laos (photo by Anton Brancelj); E,F,G) sampling of the epikarstic
fauna from the pools filled by percolating water in caves in Thailand (photo by Santi Watiroyram); H) a detail from a comparable
ecosystem (karstic cave) in Slovenia (photo by Anton Brancelj).
339
Groundwater-dwelling fauna of SE Asia
were recorded by 7 authors. After 1986, 67 new species
were added by authors, who contributed more than two
descriptions of a new species. The greatest contributions
were by Ng and Martinez – 13 and 12 descriptions, respectively – on Decapoda, Pisces and Isopoda.
co
m
e
us
m
er
c
ia
l
The first exploration of the freshwater cave fauna in
SE Asia started at the end of the 19th century and was
mainly limited to terrestrial habitats (Price, 2004). Actually, even today, most work is still focussed on terrestrial
fauna (=troglobionts) (Juberthie and Decu, 2001). Some
limited exploration was done also on aquatic fauna in the
caves. Among the first explorations were those in the
Philippines (in 1820), followed by Myanmar (in 1888),
Vietnam (in 1906), Indonesia (in 1910), Thailand (in
1913) and Laos (in 1919) (Botosaneanu, 1986). Research
on cave fauna in Cambodia and Malaysia started later, in
1960/1961 (Annandale et al., 1913; Botosaneanu, 1986).
Tropical and subtropical karstic areas worldwide were
for a long time neglected as suitable places for collecting
and studying stygobionts. When comparing Europe (an
area of 10,180,000 km2 and about 2000 stygobionts) and
SE Asia (an area of about 4,304,000 km2 and 122 stygobionts), it is obvious that there is a big potential for more
stygobionts to be found in SE Asia. A comparison of the
number of stygobionts in SE Asia vs the rest of the world,
on
ly
DISCUSSION
and vs the total number of members of particular groups
in freshwater, revealed that the number of stygobionts in
SE Asia compared with the rest of the world is (still) relatively low (Tab. 6). The only exception is Brachyura (Decapoda), for which the number of stygobionts has
significantly increased in the last 25 years. Comparing the
area of SE Asia and the rest of the world and number of
stygobionts from interstitial and karstic aquifers already
known in the rest of the world, at least 800 stygobionts
could be expected in SE Asia. The actual numbers of stygobionts recorded for Europe and SE Asia are a combination of stygobionts in fissured (i.e. karstic) as well as
porous (i.e. alluvium; interstitial) aquifers. As both types
are common in SE Asia, the estimated number of 800 stygobionts is quite probable and could even be exceeded.
In addition to exclusively freshwater caves, there are also
numerous anchialine caves along the coasts, which are
rich in freshwater, brackish and marine stygobionts (Fosshagen and Ilife, 1989; Husana et al., 2009; Tran and
Chang, 2012).
A high potential for discovery of new stygobionts is
also indicated by the cumulative curve of stygobiotic taxa
over time, which is still very steep and where, in the last
40 years (after 1970), the number of stygobionts increased
almost six-fold (from 19 to 122 species) (Fig. 1). The increase of species within a particular group is uneven and
reflects mainly the interests and intensity of work by individual authors on the specific group. Currently, the most
Tab. 6. List of the main groups of crustaceans and fish, with the number of known taxa in subterranean habitats in Southeast Asia,
worldwide and in all inland surface habitats.
Crustaceans
and fish fauna
Copepoda
Calanoida
Harpacticoida
Cyclopoida
Gelyelloida
on
Ostracoda
N
Cladocera
Southeast Asia*
Syncarida
0
Amphipoda
2
References
620
Forró et al. (2008)
1936
20
1
17
2
0
607
11
441
153
2
2774
552
1124
1096
2
21
553
994
154
1+1?
Decapoda
Anomura
Brachyura
Natantia
Reptantia
World inland water bodies#
119
13
Thermosbaenaceae
Worldwide°
5
5
Isopoda
Pisces
Stygobionts
16
Camacho and Valdecasas (2008)
665
1870
Väinölä et al. (2008)
121
2
15
42 (69§)
31
2844
63
1476
655
640
Bond-Backup et al. (2008)
Yeo et al. (2008)
De Grave et al. (2008)
Crandall and Buhay (2008)
92
18
12,470
Data from this paper; data from Botosaneanu, 1986; see references in right column; after De Grave et al. (2008).
*
°
#
Boxshall and Defaye (2008)
240
10
33
0
24
6
3
Martens et al. (2008)
§
Wilson (2008)
Jaume (2008)
Lêvêque et al. (2008)
340
A. Brancelj et al.
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on
ly
entrances of the caves, where litter or drift can accumulate. For this reason, Decapoda, especially Brachyura,
were frequently reported from those zones in the past as
stygobionts when in fact some of them were stygoxenes
or stygophiles (Leclerc et al., 2001). However, they contributed to the overall biodiversity of subterranean habitats. For that reason, the distinction between stygophiles
and stygobionts is more blurred in the tropical zones when
compared to that in temperate zones.
Due to the low intensity of research on fauna in many
aquifers worldwide, the distribution of the majority of
taxa is still very poorly known. As most stygobionts were
found in one or a few sampling campaigns and/or in one
or a few locations only, most of them are considered as
endemics while in reality they might not be. Scarcity of
data on their distribution can lead to the wrong conclusion
that all stygobionts are endemic on a small scale (i.e. narrow endemics) (Deharveng et al., 2009). Some data about
a few species from SE Asia indicates that their range of
distribution can be extended at least over two countries
(examples in groups of Copepoda, Thermosbaenacea and
Decapoda). An example of misinterpretation of endemism
can be found in the Copepoda from epikarst in Thailand.
After five years of intensive sampling it appears that rare
and endemic taxa are actually quite common – but limited
to specific habitats (Brancelj et al., 2010; Watiroyram,
2012; Watiroyram et al., 2012). This supports the idea to
put more effort into searching for representatives of some
aquatic groups, which are common in surface water bodies but still rare in groundwater, either in porous or karstic
aquifers. The most appropriate candidates are groups of
Cladocera and Calanoida. Both groups have many representatives in epigean water bodies, while in groundwater
they are represented by only a few species (Brancelj and
Dumont, 2007). So far, there is only one known stygobiotic species of Calanoida from SE Asia (Brancelj, 2005).
Cladocera are represented with representatives from the
genus Nicsmirnovius, which lives in rheic and hyporheic
conditions, much like Phreatalona, yet it is not a stygobiont (Van Damme et al., 2003).
For that reason, more intensive and systematic sampling programmes should be prepared for different habitats in interstitial as well as karstic aquifers. Special
attention should be put on sampling techniques and equipment. In principle, all sampling methods already known
and used in caves and alluvium in Europe and North
America (hand-nets, drift nets, plankton nets, baited traps,
Bou-Rouch pump and Karaman-Chappuis method) (for
details see: PASCALIS protocol) can be applied in the
caves and gravel bars of SE Asia. In the past incorrect
sampling devices (especially nets with too coarse mesh
size) resulted in a loss of many smaller stygobionts. When
new techniques were introduced, the number of collected
species/specimens increased significantly (Brancelj,
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intensively studied groups are the Copepoda, Isopoda,
Amphipoda, Decapoda and Pisces, while some other
groups, which are well studied elsewhere, are underestimated in SE Asia. Among those groups are the
Oligochaeta, Ostracoda and Hydrachnida, represented by
only a few species (Tabs. 3 and 5). The effect of highly
motivated taxonomists can be seen, for example, in the
case of the Indian stygofauna, where a significant increase
in the knowledge of micro-crustaceans was achieved in
relatively short period by only a few specialists (Ranga
Reddy and Defaye, 2008; Ranga Reddy et al., 2008;
Ranga Reddy and Schminke, 2009). The same is valid for
China, where research on karst systems resulted in the description of several new stygobionts (Sket and Fišer,
2009) (Tab. 5). Although both countries, India and China,
have high potential for groundwater fauna, there is a slight
possibility of sharing common fauna with SE Asia on the
species level, except on a very local scale. Based on the
present knowledge of the distribution of groundwater
fauna in SE Asia, distribution of particular species is
rather limited and is usually confined to a region. Only
some exceptionally species have trans-border distributions over several provinces or countries.
Recent intensive inventory of fauna from relatively
unknown environments (i.e. epikarst) in Thai caves, has
resulted in the discovery of one species of bathynellid and
six species of copepods as well as several species of
Harpacticoida and Cyclopoida that are not yet described
(Brancelj et al., 2010; Camacho et al., 2011; Watiroyram
et al., 2012; Boonyanusith et al., 2013; Watiroyram et al.,
2013). Along with the true stygobionts from epikarst,
many species of Copepoda were collected from pools or
streams, but the majority were stygoxenes or stygophiles
transported into the caves during floods or as regular drift
(Boonyanusith, personal communication; Watiroyram,
personal communication). The problem of identifying the
correct ecological position of species found in the caves
is that specimens can become pale after some time in subterranean environments, which leads to misinterpretation
of the stygobiotic nature of collected specimens. Such an
example was Argyrodiaptomus cavernicolax Shen and
Tai, 1965, from a cave in Southern China, which recently
appeared to actually be two closely related species of Sinodiaptomus, which freely move in and out of the cave
(Dumont, personal communication). Another example is
Mesocyclops francisci Hołyńska, 2000, which was collected from a cave in Northern Thailand (Watiroyram,
2012) but was previously recorded in Malacca, Malaysia,
Sumatra and Cambodia from surface water habitats
(Hołyńska, 2000; Chaicharoen, 2011). Food in subterranean habitats is an important element that determines
population size and biodiversity in temperate zones (Culver et al., 2006). As primary production in tropical zones
is more intense, more food is available, especially at the
Groundwater-dwelling fauna of SE Asia
2003). One of the new techniques, specific for SE Asia,
is sampling epikarst fauna from Buddha pots (Brancelj et
al., 2010). They are actually plastic or metal buckets,
placed near Buddha statues in the caves to collect dripping
water from the ceiling. They appeared as very efficient
sampling devices for sampling epikarst fauna and where
several new species of Copepoda had been already collected (Brancelj et al., 2010; Watiroyram et al., 2012;
2013).
CONCLUSIONS
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ACKNOWLEDGMENTS
We thank Martin Ellis who supplied the list of organisms found in karstic areas and subterranean habitats in
Thailand. This work was partly supported by the National
Research University Project of Thailand, Office of the
Higher Education Commission, through the Holistic Watershed Management Cluster of Khon Kaen University. The
senior author (AB) would like to thank to the organisers of
the FISA conference for invitation to the meeting. The authors wish to thank Dr. Jolyon Dodgson for his help with
the English corrections and two anonymous reviewers for
their useful comments on the earlier version of the paper.
Brancelj A, 2005. Hadodiaptomus dumonti n. gen., n. sp., a new
freshwater stygobiotic calanoid (Crustacea: Copepoda:
Calanoida) from Vietnam (South Asia) and a new member
of the subfamily Speodiaptominae Borutzky, 1962. Hydrobiologia 534:57-70.
Brancelj A, Dumont HJ, 2007. A review of diversity, adaptations
and groundwater colonization pathways in Cladocera and
Calanoida (Crustacea), two rare and contrasting groups of
stygobionts. Fund. Appl. Limnol. 168:3-17.
Brancelj A, Watiroyram S, Sanoamuang L, 2010. The first
record of cave-dwelling Copepoda from Thailand and description of a new species: Elaphoidella namnaoensis n. sp.
(Copepoda, Harpacticoida). Crustaceana 83:779-793.
Bruce NL, Iliffe TM, 1992. Anopsilana conditoria, a new
species of anchialine troglobitic cirolanid isopod (Crustacea)
from the Philippines. Stygologia 7:225-230.
Bruno MC, Cottarelli V, 1999. Harpacticoids from groundwaters
in the Philippines: Parastenocaris mangyans, new species,
Epactophanes philippinus, new species, and redescription
of Phyllognathopus bassoti (Copepoda). J. Crustacean Biol.
19:510-529.
Cai YX, Husana DEM, 2009. Cave shrimps of the genus
Edoneus Holthuis, 1978, from Luzon, the Philippines, with
description of three new species (Crustacea: Decapoda:
Atyidae). Raffles B. Zool. 57:51-63.
Camacho AI, 1992. The natural history of biospeleology. Museo
Nacional de Cicencas Naturales ed., Madrid: 374 pp.
Camacho AI, 2005. Disentangling an Asian puzzle: two new bathynellid (Crustácea, Syncarida, Parabathynellidae) genera
from Vietnam. J. Nat. Hist. 39:2861-2886.
Camacho AI, Valdecasas AG, 2008. Global diversity of Syncarids (Syncarida; Crustacea) in freshwater. Hydrobiologia
595:257-266.
Camacho AI, Watiroyram S, Brancelj A, 2011. The first record
of Bathynellacea from Thailand: a new genus and species
of Parabathynellidae (Crustacea: Syncarida). J. Nat. Hist.
45:45-46.
Chaicharoen R, 2011. Diversity and distribution of freshwater
calanoid and cyclopoid copepods in seven provinces of
Cambodia. PhD Thesis. Khon Kaen University ed., Khon
Kaen: 216 pp.
Cottarelli V, Bruno MC, Berera R, 2006. A new species of
Parastenocaris from Mindoro Island, Philippines: Parastenocaris distincta n. sp. (Crustacea: Copepoda: Harpacticoida: Parastenocarididae). Zootaxa 1368:57-68.
Cottarelli V, Bruno MC, Berera R, 2010. First record of Parastenocarididae from Thailand and description of a new genus
(Copepoda: Harpacticoida). J. Crustacean Biol. 30: 478-494.
Crandall KA, Buhay JE, 2008. Global diversity of crayfish
(Astacidae, Cambaridae, and Parastacidae- Decapoda) in
freshwater. Hydrobiologia 595:295-301.
Culver DC, Deharveng L, Bedos A, Lewis JJ, Maden M, Raddell, JR, Sket B, Trontelj P, White DJ, 2006. The mid-latitude biodiversity ridge in terrestrial cave fauna. Ecography
29:120-128.
Day MJ, Urich PB, 2000. An assessment of protected karst landscapes in Southeast Asia. Cave Karst Sci. 27:61-70.
De Grave S, Cai Y, Anker A, 2008. Global diversity of crabs
(Crustacea: Decapoda: Caridea) in freshwater. Hydrobiologia 595:287-292.
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In conclusion, faunistic inventories and taxonomic
work done on subterranean fauna in SE Asia in the last
two decades have revealed that stygobionts are much
more common than was thought before. Their number
will increase considerably when greater efforts are oriented towards subterranean aquifers.
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