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Journal of Fish Biology (2011) 79, 1545–1562
doi:10.1111/j.1095-8649.2011.03066.x, available online at wileyonlinelibrary.com
Out of sight out of mind: current knowledge of Chinese
cave fishes
Y.-H. Zhao*†, R. E. Gozlan‡and C.-G. Zhang*
*Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese
Academy of Sciences, 100101 Beijing, China and ‡Centre for Conservation Ecology &
Environmental Change, School of Applied Sciences, Bournemouth University, BH12 5BB
Dorset, U.K.
Caves and karsts are among the most threatened ecosystems in the world. They are very fragile,
balanced habitats with high levels of endemic species that are extremely sensitive to environmental
changes. In recent decades, however, threats from rapid economic growth have increased the need
for conservation efforts for cave-dwelling communities. In addition, difficulties in accessing and
sampling these habitats mean that they remain as one of the least known ecosystems in the world
with modern studies of cave fishes only starting in China during the 1980s. Here, the current status
of cave fishes in China is reviewed. China is host to the highest number of cave fish species in
the world, with 48 troglobite species out of a total of 101 cave fish species. All of these cave
fish species (one order and three families) and half of the genera are endemic to China with
Sinocyclocheilus being the most speciose cave fish genus. Species from this genus possess horns and
humpbacks resulting from processes of parallel evolution, but the function of these features remains
unknown. With the exception of Onychostoma macrolepis distributed in north China, all other
species are found in the karst environment of the Yunnan-Guizhou Plateau. Sympatric distribution
is common, and sometimes several different cave fish species can be found in the same cave
or subterranean river. For this reason, Chinese cave fishes represent an important evolutionary
framework. ©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles
Key words: conservation; endemic; karst; red list; Sinocyclocheilus; troglobite.
INTRODUCTION
China’s complex topography and diversity of freshwater habitats make it one of the
richest countries in terms of freshwater biodiversity with c. 1254 native freshwa-
ter fish species (Xing, 2011). This is particularly true for cave fishes (also known
as hypogean fishes) as China is host to the largest taxonomic diversity with >90
currently described species across three families (Romero et al., 2009). Similar to
the allegory of the Cave in Plato’s Republic, cave fishes are compelled to gaze
at a simple but fragile ecosystem link to the outside world through limited biotic
input and as such are very vulnerable to environmental changes. The diversity of
animals, from invertebrates to mammals, concealed in caves is increasingly attract-
ing interest among the scientific community. Before c. 1980 there was almost no
scientific information on cave fishes. The discoveries of blind fishes in the early
1980s (Zheng, 1981; Chu & Chen, 1982) marked the beginning of modern cave-fish
†Author to whom correspondence should be addressed. Tel.: +86 10 64807076; email: zhaoyh@ioz.ac.cn
1545
©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles
1546 Y.-H. ZHAO ET AL.
study in China. Since then, an extensive network of underground passages has been
explored and many cave-fish species were discovered and scientifically described
(Proudlove, 2010). Most of this research, however, has been published in Chinese
journals which makes it difficult to access by the international community. Here the
current knowledge of Chinese cave fishes is reviewed, in order to support future
conservation programmes of these highly diverse and highly threatened species.
DEFINITION OF TERMS
KARST
Kras is a Slovenian word meaning ‘stony ground’ and describes an area located
in south-western Slovenia extending into north-eastern Italy of typical limestone
landscape. Karst, the German name for kras, has been expanded as a global term
for landscape containing caves and extensive underground water systems that has
developed within particularly soluble rocks such as limestone (Gunn, 2004; Ford &
Williams, 2007).
CAVE
This paper is restricted to freshwater caves, which have a natural opening in
solid rock with areas of complete darkness and are larger than a few millimetres in
diameter (Culver & Pipan, 2009). In most cases, caves are formed by dissolution of
rocks, and are strongly influenced by subterranean water.
CAVE FISHES (HYPOGEAN FISHES)
The ecological definition refers to those species restricted to the cave (subterranean
river) environment, at least for part of their life history, and as such they could not
survive without this environment (Zhao & Zhang, 2006).
TROGLOMORPHISM
Cave-dwelling animals will always present some morphological characters adapted
to the cave environment known as troglomorphism (Fig. 1). There are a range of
adaptations according to the type of cave animal. Romero & Green (2005) listed
characters considered as troglomorphism for cave fishes, e.g. reduction or loss of
eyes, pigmentation, scales or swimbladder. Conversely, chemo- and mechanorecep-
tors (olfactory organs and the lateral-line system) or appendages (fins) are enlarged
or enhanced (Romero & Green, 2005). Here, a horn-like character on the nape and
a humpback profile (Fig. 2) are also treated as troglomorphic characteristics. Both
characters are found among some cave cyprinid fish species of the Sinocyclocheilus
genus, but their functionality remains speculative (Zhao & Zhang, 2006; Romero
et al., 2009).
TROGLOBITE AND TROGLOPHILE
Troglobites are defined as cave-fish species that display specific adaptations (trog-
lomorphism) to subterranean life. Troglophiles are defined as cave-fish species which
©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles, Journal of Fish Biology 2011, 79, 1545– 1562
CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1547
Fig.1. Sinocyclocheilus furcodorsalis, showing troglomorphism of the cave fish.
do not display signs of troglomorphism (Zhao & Zhang, 2006). In other words
troglobite–trogophile could also be called typical– atypical cave fish.
DATA SOURCE
This review covers all available articles on Chinese cave fishes published up to
2011 using a range of bibliographical sources, including the Zoological Record, the
China Knowledge Resource Integrated Database, VIP Database for Chinese Tech-
nical Periodicals, as well as some other Chinese scientific journal databases. In
addition, some data and observations collected during fieldwork from 1982 to 2011
are provided.
THE HISTORICAL RECORDS OF CHINESE CAVE FISHES
China hosts the earliest written records for both troglobite and troglophile fishes in
the world (Zhao & Zhang, 2009). In 1436, a local doctor, Lan, recorded the following
in his medical book Materia Medica of South Yunnan, ‘a very famous golden line
fish always found in stone cave with water of the Yunnan Province, and in particular
from Lake Dianchi near Jinning, a city located in south of lake’. Today this fish has
been named the Dianchi golden-line barb Sinocyclocheilus grahami (Regan 1904),
a troglophile species. The next record of a cave fish came 100 years later, through
the report of Yingjing Xie, the local Governor of Luxi County. When he travelled
to the Alu Cave located in Luxi County, Yunnan Province, he wrote in his article
Records on Alu Cave in 1540, ‘I heard there was a kind of transparent fish coming
out when the subterranean river flooded’. This was the first record of a troglobite
©2011 The Authors
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1548 Y.-H. ZHAO ET AL.
(a)
(b)
Fig. 2. Specific features of troglomorphism (head horn and humpback) in Chinese cave fishes in the genus
Sinocyclocheilus: (a) Sinocyclocheilus microphthalmus and (b) Sinocyclocheilus tileihornes.
©2011 The Authors
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CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1549
fish. This fish, the transparent golden-line barb Sinocyclocheilus hyalinus Chen &
Yang 1993, can still be found today in the same cave and was described by modern
taxonomists in 1993 and 1994 (Chen & Yang, 1993; Chen et al., 1994).
In 1839, Guangzu Zheng, a naturalist, published One Spot Record, a type of
encyclopaedia on nature and society. In Miscellany II, one chapter of the book, the
author wrote, ‘Muzhu Cave, located in the west of the Guiding County (Guizhou
Province), is very deep and connected to a huge subterranean river where some fish
lives. The fish have lost their eyes due to the dark environment of the cave’. In
another chapter, Reasons of things, the author speculates on the reasons why ‘fish
living in the cave do not have eyes’. In the same book, Zheng also recorded another
transparent fish distributed in Lake Dianchi (Qian & Li, 2002).
TAXONOMIC DIVERSITY
On the basis of recent statistics (until the end of 2010), with 1254 species, China
hosts one of the largest diversities of freshwater fishes, including 827 endemic species
(Xing, 2011). A large number of these freshwater species, however, are threatened
(n=245) highlighting the need to consider China as a hotspot for freshwater fish
conservation (V¨
or¨
osmarty et al., 2010; Xing, 2011). China also has the highest num-
ber of cave-fish species (8% of overall diversity) with currently c. 101 valid species
(Table I) including 48 species of troglobite. Despite this high species diversity, Chi-
nese cave fishes originate from a single order (Cypriniformes) comprising only three
families; Cyprinidae (56% of all cave fishes), Cobitidae (2%) and Balitoridae (42%).
This is in contrast, for example, to Brazilian cave fishes with 25 species from three
orders and six families, Mexican cave fishes where 11 species belong to five orders
and six families and cave fishes in Thailand where nine species belong to two orders
and four families (Proudlove, 2010).
CYPRINIDAE
Chinese cyprinid cave fishes are divided across four genera, Onychostoma (one
troglophile), Sinocrossocheilus (three troglophiles), Sinocyclocheilus (a total of 52
species, including troglophile and troglobite fish species) and Typhlobarbus (one
species, troglobite) (Yue, 2000; Zhao & Zhang, 2009). Currently, there is very little
understanding of cave-fish ecology or even life-history traits but some facultative
species only access cave habitats to hibernate during the winter. This is, for example,
the case of Onychostoma macrolepis (Bleeker 1871) which accesses caves during
winter from November to April. This winter behaviour makes O. macrolepis the
only cave-fish species north of the Changjiang River. Other species of this genus
are distributed south of the Changjiang River without this behaviour (Zhang, 1986).
During spring and summer, Sinocrossocheilus bamaensis (Fang 1981) will swim out
of the cave in the morning and at night to find food but otherwise will always live in
caves during the winter (Su et al., 2003). The belly naked blind barb Typhlobarbus
nudiventris Chu & Chen 1982 is the only species within this genus and found in
Jianshui County, Yunnan Province.
The genus Sinocyclocheilus is a monophyletic group with four clades, called angu-
laris, cyphotergous and tingi, from four representative species respectively (Romero
©2011 The Authors
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1550 Y.-H. ZHAO ET AL.
Table I. List of Chinese cave fishes
Conservation status
Species Authorities Year Troglobite Troglophile
Distribution
(Province) A B C D
Cyprinidae
Onychostoma macrolepis (Bleeker) 1871 +Beijing, Hebei,
Shandong, Shanxi,
Shaanxi, Henan, etc.
Sinocrossocheilus liuchengsensis (Liang) 1987 +Guangxi
Sinocrossocheilus megalophthalmus Chen, Yang & Cui 2006 +Guangxi
Sinocrossocheilus bamaensis (Fang) 1981 +Guangxi, Guizhou
Sinocyclocheilus altishoulderus (Li & Lan) 1992 +Guangxi
Sinocyclocheilus anatirostris Lin & Luo 1986 +Guangxi VU VU
Sinocyclocheilus brevibarbatus Zhao, Lan & Zhang 2009 +Guangxi
Sinocyclocheilus brevis Lan & Chen 1992 +Guangxi
Sinocyclocheilus donglanensis Zhao, Watanabe & Zhang 2006 +Guangxi
Sinocyclocheilus furcodorsalis Chen, Yang & Lan 1997 +Guangxi
Sinocyclocheilus guilinensis Ji 1982 +Guangxi
Sinocyclocheilus huanjiangensis Wu, Gan & Li 2010 +Guangxi
Sinocyclocheilus jii Zhang & Dai 1992 +Guangxi
Sinocyclocheilus jiuxuensis Li & Lan 2003 +Guangxi
Sinocyclocheilus lingyunensis Li, Xiao & Luo 2000 +Guangxi
Sinocyclocheilus longibarbatus Wang & Chen 1989 +Guangxi
Sinocyclocheilus macrophthalmus Zhang & Zhao 2001 +Guangxi
Sinocyclocheilus mashanensis Wu, Liao & Li 2010 +Guangxi
Sinocyclocheilus microphthalmus Li 1989 +Guangxi VU VU
Sinocyclocheilus tianlinensis Zhou, Zhang & He 2003 +Guangxi
Sinocyclocheilus xunleensis Lan, Zhao & Zhang 2004 +Guangxi
Sinocyclocheilus yishanensis Li & Lan 1992 +Guangxi
Sinocyclocheilus macrolepis Wang & Chen 1989 +Guangxi, Guizhou
Sinocyclocheilus multipunctatus (Pellegrin) 1931 +Guangxi, Guizhou
©2011 The Authors
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CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1551
Table I. Continued
Conservation status
Species Authorities Year Troglobite Troglophile
Distribution
(Province) A B C D
Sinocyclocheilus angularis Zheng & Wang 1990 +Guizhou VU VU
Sinocyclocheilus bicornutus Wang & Liao 1997 +Guizhou
Sinocyclocheilus cyphotergous (Dai) 1988 +Guizhou VU
Sinocyclocheilus hugeibarbus Li & Ran 2003 +Guizhou
Sinocyclocheilus robustus Chen & Zhao 1988 +Guizhou
Sinocyclocheilus yaolanensis Zhou, Li & Hou 2009 +Guizhou
Sinocyclocheilus angustiporus Zheng & Xie 1985 +Guizhou, Yunnan
Sinocyclocheilus anophthalmus Chen & Chu 1988 +Yunnan RA EN VU
Sinocyclocheilus aquihornes Li & Yang 2007 +Yunnan
Sinocyclocheilus broadihornes Li & Mao 2007 +Yunnan
Sinocyclocheilus grahami (Regan) 1904 +Yunnan II EN EN EN
Sinocyclocheilus guishanensis Li 2003 +Yunnan
Sinocyclocheilus huaningensis Li 1998 +Yunnan
Sinocyclocheilus hyalinus Chen & Yang 1993 +Yunnan VU VU
Sinocyclocheilus lateristritus Li 1992 +Yunnan
Sinocyclocheilus longifinus Li & Chen 1994 +Yunnan
Sinocyclocheilus luopingensis Li & Tao 1997 +Yunnan
Sinocyclocheilus macrocephalus Li 1985 +Yunnan
Sinocyclocheilus macroscalus Shen et al. 2000 +Yunnan
Sinocyclocheilus maculatus Li 2000 +Yunnan
Sinocyclocheilus maitianheensis Li 1992 +Yunnan
Sinocyclocheilus malacopterus Chu & Cui 1985 +Yunnan
Sinocyclocheilus oxycephalus Li 1985 +Yunnan
Sinocyclocheilus purpureus Li 1985 +Yunnan
Sinocyclocheilus qiubeiensis Li 2002 +Yunnan
Sinocyclocheilus qujingensis Li, Mao & Lu 2002 +Yunnan
Sinocyclocheilus rhinocerous Li & Tao 1994 +Yunnan VU
©2011 The Authors
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1552 Y.-H. ZHAO ET AL.
Table I. Continued
Conservation status
Species Authorities Year Troglobite Troglophile
Distribution
(Province) A B C D
Sinocyclocheilus tileihornes Mao, Lu & Li 2003 +Yunnan
Sinocyclocheilus tingi Fang 1936 +Yunnan
Sinocyclocheilus wumengshanensis Li, Mao & Lu 2003 +Yunnan
Sinocyclocheilus yangzongensis Tsu(=Chu) & Chen 1977 +Yunnan
Sinocyclocheilus yimenensis Li & Xiao 2005 +Yunnan
Typhlobarbus nudiventris Chu & Chen 1982 +Yunnan RA VU VU
Cobitidae
Protocobitis typhlops Yang, Chen & Lan 1993 +Guangxi VU
Protocobitis polylepis Zhu, Lu, Yang & Zhang 2008 +Guangxi
Balitoridae
Heminoemacheilus hyalinus Lan, Yang & Chen 1996 +Guangxi
Heminoemacheilus zhengbaoshani Zhu & Cao 1987 +Guangxi
Oreonectes anophthalmus Zheng 1981 +Guangxi RA VU VU
Oreonectes furcocaudalis Zhu and Cao 1987 +Guangxi DD
Oreonectes luochengensis Yang, Wu, Wei & Yang 2011 +Guangxi
Oreonectes macrolepis Huang, Du, Chen & Yang 2009 +Guangxi
Oreonectes microphthalmus Du, Chen & Yang 2008 +Guangxi
Oreonectes retrodorsalis Lan, Yang & Chen 1995 +Guangxi VU
Oreonectes translucens Zhang, Zhao & Zhang 2006 +Guangxi
Paracobitis posterodarsalus Ran, Li & Chen 2006 +Guangxi
Paracobitis maolanensis Li, Ran & Chen 2006 +Guizhou
Paranemacheilus genilepis Zhu 1983 +Guangxi
Schistura lingyunensis Liao & Luo 1997 +Guangxi
Schistura dabryi microphthalmus Liao & Wang 1997 +Guizhou
Triplophysa nandanensisi Lan, Yang & Chen 1995 +Guangxi
Triplophysa tianeensis Chen, Cui & Yang 2004 +Guangxi
Triplophysa longibarbatus (Chen, Yang, Sket & Aljancic) 1998 +Guizhou VU
©2011 The Authors
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CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1553
Table I. Continued
Conservation status
Species Authorities Year Troglobite Troglophile
Distribution
(Province) A B C D
Triplophysa longipectoralis Zheng, Du, Chen & Yang 2009 +Guangxi
Triplophysa nasobarbatula Wang & Li 2001 +Guizhou
Triplophysa zhenfengensis Wang & Li 2001 +Guizhou
Triplophysa xiangxiensis (Yang, Yuan & Liao) 1986 +Hunan VU
Triplophysa aluensis Li & Zhu 2000 +Yunnan
Triplophysa gejiuensis (Chu & Chen) 1979 +Yunnan RA VU VU
Triplophysa qiubeiensis Li & Yang 2008 +Yunnan
Triplophysa shilinensis (Chu & Yang) 1992 +Yunnan VU
Triplophysa xiangshuingensis Li 2004 +Yunnan
Triplophysa yunnanensis Yang 1990 +Yunnan VU
Triplophysa rosa Chen & Yang 2005 +Chongqing
Yunnanilus pulcherrimus Yang, Chen & Lan 2004 +Guangxi
Yunnanilus bajiangensis Li 2004 +Yunnan
Yunnanilus beipanjiangensis Li, Mao & Sun 1994 +Yunnan
Yunnanilus discoloris Zhou & He 1989 +Yunnan CR
Yunnanilus jingxiensis Zhu, Du & Chen 2009 +Guangxi
Yunnanilus longibarbatus Gan, Chen & Yang 2007 +Guangxi
Yunnanilus longidorsalis Li, Tao & Lu 2000 +Yunnan
Yunnanilus macrogaster Kottelat & Chu 1988 +Yunnan DD
Yunnanilus macrolepis Li, Tao & Mao 2000 +Yunnan
Yunnanilus nanpanjiangensis Li, Mao & Lu 1994 +Yunnan
Yunnanilus niger Kottelat & Chu 1988 +Yunnan VU
Yunnanilus obtusirostris Yang 1995 +Yunnan
Yunnanilus paludosus Kottelat & Chu 1988 +Yunnan
Yunnanilus parvus Kottelat & Chu 1988 +Yunnan DD
A, China key protection, 1988; B, China Red Book, 1998; C, China Red List, 2004; D, IUCN Red List, 2010. DD, data deficient; EN, endangered; II, second class
of protected status in China; RA, rare; VU, vulnerable.
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1554 Y.-H. ZHAO ET AL.
et al., 2009; Zhao & Zhang, 2009). Each clade has its own typical morphology and
distribution with very little overlap (Table II) (Zhao & Zhang,
2009).
COBITIDAE
Cobitidae comprises only two cave-fish species in the world, which are both from
the genus Protocobitis (two troglobites) and are only found in China.
BALITORIDAE
Balitoridae is the second largest family of cave fishes in the world with seven
genera that can be found in China: Heminoemacheilus (one troglobite and one
troglophile), Oreonectes (six troglobites and one troglophile), Paracobitis (two
troglobites), Paranemacheilus (one troglophile), Schistura (two troglobites), Triplo-
physa (eight troglobites and six troglophiles) and Yunnanilus (14 troglophiles).
HABITAT DIVERSITY
China has a large variety of karsts, extending over >907 000 km2of surface
limestone (Yuan, 2002). In particular, south-west China is one of the largest karst
geomorphologic distribution areas in the world. It is estimated that the karst geomor-
phology covers c. 620 000 km2in this region mainly including Guizhou, Guangxi
and Yunnan Provinces (Huang et al., 2008). The south China karst was selected as
one of UNESCO (United Nations, Educational, Scientific and Cultural Organiza-
tion) World Heritage Sites in 2007, due to its karst features and landscapes as well
as rich biodiversity (http://whc.unesco.org). In south-west China, the topography is
dominated by the extensive fengcong (peak-cluster) and fenglin (peak-forest) karsts
(Zhang, 1980; Gunn, 2004). Different karst types may have some corresponding rela-
tions to cave-fish types. Troglobite fish species are more heavily concentrated in the
fengcong area where violent uplifting has produced steep slopes and a complicated
karst environment. Troglophile species tend to be found in the Yunnan Plateau and
West Guangxi which exhibit flatter topologies (Zhao & Zhang, 2009).
A subterranean river includes a number of habitats, categorized into three main
types (Table III). The many branches of subterranean rivers provide diverse habi-
tats including fast sections but also subterranean riffle–pool sequences representing
a perfect stable environment for cave-fish populations particularly in a complex
cave where temperature will remain stable from year to year. In these subter-
ranean environments, however, food is scarce with limited natural enemies. Troglo-
bite fishes are always found in subterranean rivers. For example, the duck-billed
golden-line barb Sinocyclocheilus anatirostris Lin & Luo 1986 is found in the
65·6 km main channel and 11 branches of the Bailang subterranean river (Zhu et al.,
2003).
Openings on top of subterranean rivers are like skylights, and are an example of
a typical cave-fish habitat (Table III). Sinkholes (or dolines) are natural depressions
or holes that are gradually or suddenly formed by karst erosions. They may vary
in size from 1 to 600 m both in diameter and depth with giant sinkholes known
©2011 The Authors
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CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1555
Table II. Evolutionary relationship and main characteristics of four species clades (groups) of the genus Sinocyclocheilus
Distribution
Main characters
Representative
Clade
Relationship
Tingi
Sinocyclocheilus tingi Fang 1936
Most are troglophile;
normal body shape (most);
lateral-line scales >60;
pectoral fin short
Cyphotergous
Sinocyclocheilus cyphotergous (Dai 1988)
All troglobites;
Humpback;
pectoral fin long
Angularis
Sinocyclocheilus angularis Zheng & Wang 1990
Most troglobites;
horn-like characters;
pectoral fin long
Jii
Sinocyclocheilus jii Zhang & Dai 1992
Humpback;
pectoral fin short;
dorsal-fin spine soft
East of distribution range;
Nanpanjiang River system
Middle of distribution range;
Longjiang River system (main)
East and middle of distribution range;
Hongshuihe River sytem (main)
West of distribution range
©2011 The Authors
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1556 Y.-H. ZHAO ET AL.
Table III. Typology of cave-fish habitats
Habitat type Sub-types Source Characteristics Representative
Deep cave or
subterranean river
Subterranean river Natural (1) Dark Always troglobites; e.g.
(2) Environmental variables are stable Oreonectes anophthalmus Zheng 1981
(3) Limited food supply
Intermittent openings
along the subterra-
nean river
Sinkholes Natural (1) Limited light Always troglobites; e.g.
(2) Influenced by surface environmental
factors
Sinocyclocheilus altishoulderus (Li & Lan 1992)
(3) Less influences from human activities
(4) Unstable energy input
Well Artificial (1) Limited light Always troglobites; e.g.
(2) Frequently disturbed by human
activities
Sinocyclocheilus angularis Zheng & Wang 1990
(3) Limited energy input
Entrance or exit of
subterranean river
Simple confluence
with surface river
Natural (1) Limited light Always troglophiles; e.g.
(2) Environmental variables are unstable Sinocyclocheilus guishanensis Li 2003
(3) Limited food supply
Dragon pool Natural (1) Good light Always troglophiles; e.g.
(2) Good food and energy supply Sinocyclocheilus huaningensis Li 1998
Big lake Natural (1) Good light Always troglophiles; e.g.
(2) Highly influenced by human activities Sinocyclocheilus tingi Fang 1936
(3) Good food and energy supply
Dam Artificial (1) Good light Always troglophiles; e.g.
(2) Highly influenced by human activities Sinocyclocheilus yishanensis Li & Lan 1992
(3) Good food and energy supply
©2011 The Authors
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CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1557
as tiankeng. Subterranean rivers always flow though several sinkholes and these
openings make the river more vulnerable to the outside environment. These openings,
however, are also a source of exogenous food and energy which support specific cave-
fish communities. For example, the high shoulder golden-line barb Sinocyclocheilus
altishoulderus (Li & Lan 1992) and the Donglan golden-line barb Sinocyclocheilus
donglanensis Zhao, Watanabe & Zhang 2006 can be found associated with a series of
sinkholes. In south-west China, due to the lack of surface water, this karst landform
is also known as a stone desert. Local people have to draw underground water from
man-made wells. Unlike sinkholes, wells and related subterranean water will be
disturbed frequently by human activity and usually in a regular fashion, e.g. noisy
in daylight and quiet at night. The angle golden-line barb Sinocyclocheilus angularis
Zheng & Wang 1990 was collected from such a well in Panxian County, Guizhou
Province.
The third type of habitat is the end of a subterranean river (i.e. the entrance and
exit, always exit; Table III). Sometimes, the subterranean river will simply come
out from underground and flow directly into the surface river but at other times it
will form a small pond, known as a dragon pool by local people, or may open up
into a large surface lake. Troglophile fishes will always be found associated with
these habitats and will never swim far from the cave exit or entrance. Commonly,
man-made reservoirs and dams utilize subterranean water and form artificial pools
similar to large dragon ponds. The water level of these reservoirs changes frequently
and irregularly, with a potentially direct effect on cave-fish populations. In general,
the population size of cave fishes is determined by the food resources available and
is comparatively greater at the entrance or exit of a subterranean river.
DISTRIBUTION
All cave fishes north of the Changjiang River belong to one species, O. macrolepis
(Fig. 3, north of 30◦N), but as all populations have become isolated due to anthro-
pogenic habitat fragmentation, this species is declining rapidly (Zhang & Xu, 1991).
In the southern and western parts of China, karst environments are spread over large
areas in the Yunnan – Guizhou Plateau including east of Yunnan Province, south of
Guizhou Province, north and north-west of the Guangxi Zhuang Autonomous Region
and provide suitable conditions to support a high diversity of cave-fish populations.
The Xiangxi Plateau loach Triplophysa xiangxiensis (Yang, Yuan & Liao 1986) and
the rose plateau loach Triplophysa rosa Chen & Yang 2005 are found in the Hunan
and Chongqing Provinces, respectively, on the edge of the Yunnan – Guizhou Plateau.
The Guangxi Zhuang Autonomous Region remains the richest in terms of troglobite
fish species (n=24; see Fig. 4).
The Xijiang River, a tributary of the Pearl River is where all Chinese cave fishes
originated from with the exception of O. macrolepis. For example, 10 000 years ago
Lake Dianchi, which is currently part of the Changjiang River and hosts S. grahami,
was three time larger and drained into the Xijiang River. The reduction of the lake
happened during the Holocene due to uplifting of the river basin (Wang & Dou,
1998). There are now six species of cave fishes in the Changjiang River drainage
including O. macrolepis which can be also found in the Yellow and Haihe River
system.
©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles, Journal of Fish Biology 2011, 79, 1545– 1562
1558 Y.-H. ZHAO ET AL.
70°
50°
40°
30°
20°
10°
90°100°110°120°
10°
20°
Pearl River
Changjiang River
Yellow River
Beijing
Haihe River
Amur River
Yalu River
30°
40°
50°
80°90°100°110°120°130°140°
Fig. 3. The distribution of Chinese cave fishes. , locations where cave fishes have been found.
NARROW DISTRIBUTION AND SYMPATRIC DISTRIBUTION
All Chinese cave fishes are endemic and can be found in a karst area from the
Tropic of Cancer to 40◦N and 102– 112◦E (Fig. 3). Most species have a very
narrow distribution. Some species can only be found in one specific cave or sub-
terranean river. For example, the blind mountain loach Oreonectes anophthalmus
Zheng 1981, a troglobite species, is only found in Taiji cave in Wuming County
(Guangxi). In general, troglophile fishes have a larger distribution range compared
to troglobite species. There are a few species, however, which have an extremely
restricted distribution and as such are at a high risk of extinction. Qujing golden-
line barb Sinocyclocheilus qujingensis Li, Mao & Lu 2002, a troglophile species, is
©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles, Journal of Fish Biology 2011, 79, 1545– 1562
CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1559
50
45
40
35
30
25
20
Number of cave fishes
15
10
5
0
Rest Onychostoma macrolepis
Yunnan
Guangxi
Guizhou
Chongqing
Hunan
Beijing
Shandong
Hebei
Shanxi
Henan
Shaanxi
Gansu
Province
Fig. 4. Distribution of the number of troglobite ( ) and troglohile ( ) fishes in the various Chinese provinces.
Data are divided into provinces where only Onychostoma macrolepis is found and where a variety of
cave-fish species is found (rest).
restricted to the small Wujiafen Reservoir built on an exit of a subterranean river in
the Qujing City (Yunnan).
It is also common to find several cave-fish species living in sympatry in caves
or subterranean rivers. For example, the rhinoceros horn golden-line barb Sinocy-
clocheilus rhinocerous Li & Tao 1994 (troglobite), the small gill-open golden-
line barb Sinocyclocheilus angustiporus Zheng & Xie 1985 (troglophile) and the
soft dorsal-spine golden-line barb Sinocyclocheilus malacopterus Chu & Cui 1985
(troglophile) are found in a subterranean river flowing in Xinzhai Village of Luoping
County (Yunnan). Also, the small eye golden-line barb Sinocyclocheilus microphthal-
mus Li 1989 (troglobite), the Lingyun golden-line barb Sinocyclocheilus lingyunensis
Li, Xiao & Luo 2000 (troglobite) and Schistura lingyunensis Liao & Luo 1997
(troglobite) are found in Shadong Cave, Lingyun County (Guangxi). In effect, it is
believed that frequent connection–disconnection of subterranean rivers and cave-fish
behaviour could be the driver of sympatric evolution. In some cases, however, sub-
terranean rivers have recently been artificially connected allowing different species
to be reunited. For example, the construction of the Heilongtan Reservoir, Shilin
City (Yunnan) was achieved by blasting two subterranean rivers and now the big
head golden-line barb Sinocyclocheilus macrocephalus Li 1985 (troglophile) and the
sharp head golden-line barb Sinocyclocheilus oxycephalus Li 1985 (troglophile) can
be found in sympatry.
SOME POSSIBLE EXAMPLES OF CONVERGENT EVOLUTION
Evolution in cave fishes has led to a range of specific morphological adapta-
tions (troglomorphism) to extreme conditions in the dark such as loss of the visual
©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles, Journal of Fish Biology 2011, 79, 1545– 1562
1560 Y.-H. ZHAO ET AL.
apparatus and pigmentation. In addition, in some Sinocyclocheilus species, horns and
humpbacks are present. The horn consists of the frontal and parietal bones (Zhao
& Zhang, 2009), while the humpback is totally free of bone and mainly consists
of adipose tissue (Wang et al., 1995). The shape of the horn varies among different
species: some are small (S. angularis), some show a thin protrusion (S. rhinocerous),
and some show a tile shape (the tile-like horn golden-line barb Sinocyclocheilus
tileihornes Mao, Lu & Li 2003). A slight humpback has been observed in some
species (the short body golden-line barb Sinocyclocheilus brevis Lan & Chen 1992)
and a greater humpback in others (S. altishoulderus). Finally, a horn-like humpback
is present in the humpback golden-line barb Sinocyclocheilus cyphotergous (Dai
1988). On the basis of molecular analyses, these species come from two clades, i.e.
clade angularis and clade cyphotergous. Although head horn and humpback horn
look similar, these two characteristics are derived from different tissues and are
present on species from different clades representing a very interesting phenomenon
of convergent evolution (Zhao & Zhang, 2009).
The functional use of the horn remains unknown but some speculate that the horn
can be used to carry eggs, as in the male of a Kurtid nursery fish Kurtus gulliveri
Castelnau 1878 (Berra & Humphrey, 2002; Romero et al., 2009). In cave fishes,
however, the horn-like character is found within a species on both sexes, and no
evidence of such functionality has been found during field surveys. Another possible
functional explanation is that the horn could protect the brain from shocks from
colliding with rocks (Li et al., 1997). This seems unlikely as a simple structure
would not be enough for protection and it is difficult to imagine, for example, that
the horn derived from the humpback in S. cyphotergous would be enough to protect
its brain. Field observations have shown that when S. tileihornes is kept in a bucket,
the fish uses its horn to hang or hook itself on the edges (pers. obs.). It seems likely
that such behaviour would be used by the fish in its subterranean habitat (which
sometimes have rapid currents) to hang onto hard surfaces and hold position, with
potential energy-saving benefits. This energetic explanation is strengthened within
the context of subterranean habitats where food resources are scarce.
CONSERVATION
Due to the extremely limited distribution of cave-fish species, the fragile balance
of subterranean habitats and human pressure on ground water from an expanding
agricultural sector, cave fishes should be put at the forefront of conservation agen-
das. For example, due to recurrent droughts in the Yunnan – Guizhou Plateau, the
utilization of subterranean water is rapidly increasing (Huang et al., 2008). This has
direct implications from frequent changes of subterranean water levels to increased
noise from pumping mechanisms. In addition, recent development of hydropower
stations driven by subterranean water, exploitation of rocks for road construction,
as well as water pollution (which is greater than that for surface water due to low
flow and weak self-purification capacity in some underground pools) significantly
increase the threat to cave-fish habitat (Zhao & Zhang, 2009). Finally, income from
tourism encourages local people to put more lights in caves, organize frequent cave
explorations and even catch cave fishes to satisfy the tourists’ appetite; all of which
take away the peaceful refuge characteristic of caves.
©2011 The Authors
Journal of Fish Biology ©2011 The Fisheries Society of the British Isles, Journal of Fish Biology 2011, 79, 1545– 1562
CURRENT KNOWLEDGE OF CHINESE CAVE FISHES 1561
Cave fishes are facing increasing threats with some species specifically under high
risk of extinction, yet the protection of cave fishes lags far behind. The current list
of wild animals under China’s key protection was issued in 1988 including just one
troglophile fish (S. grahami ) among the 16 species of fishes. The list is currently
under revision and the updated version should include the genus Sinocyclocheilus and
many other fish species, reflecting the increasing discoveries of cave fishes. Overall,
a total of 22 cave-fish species have been included in different international conserva-
tion lists with limited assessment of their status (Table I) (Yue & Chen, 1998; Wang
& Xie, 2004; IUCN, 2010). In addition, some conservation areas and national parks
aimed at protecting cave fishes or karst environments have recently been established.
For example, the eyeless golden-line barb Sinocyclocheilus anophthalmus Chen &
Chu, 1988, will benefit from the establishment of the Jiuxiang National Park (Zhao
& Zhang, 2009) and in 2008 the Lingyun-Leye cave-fish protected area was estab-
lished in the Guangxi Zhuang Autonomous Region which hosts several troglobite
species such as S. microphthalmus,S. anatirostris and S. lingyunensis. Also, for the
first time, the artificial reproduction of S. grahami has been achieved (Yang et al.,
2007) and could be used to restock some targeted water bodies following a care-
ful restoration programme. More importantly, this will also help understanding of
cave-fish life history, since the shortage of basic research is still restricting cave fish
conservation.
We are most grateful to D. Fenolio for providing the photograph in Fig 1. This work was
supported by grants of the National Natural Science Foundation of China (NSFC-31071884
and 30870285) and National Key Technologies Research and Development Programme (grant
no. 2008BAC39). We would also like to thank the Fisheries Society of the British Isles for
their support.
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©2011 The Authors
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