100

FieldworkFieldworkSAVING ITALY’S VIPERSFASCINATING FAUNA OF SUBTERRANEAN RIVERS

CHINA’SMYSTERIOUSCAVEFISHESField researcher and passionate conservationist Danté Fenolio reports on the little-known, highly adapted and currently endangered fauna of South China’s karstField researcher and passionate conservationist Danté Fenolio reports on the little-known, highly adapted and currently endangered fauna of South China’s karst

CHINA’S MYSTERIOUSCAVEFISHES

HEREGOOGLE EARTH COORDINATES HERE

101

Cone Karst in Guangxi, China. At times the peaks in South China seem to compete for space and are densely bunched together (cone karst or fengling). At othertimes, the peaks are discrete entities and do not touch one another – falling into the tower karst or fengcong category. The two are related in that they representdifferent stages in the same process. Tower karst evolves from cone karst as water undercuts the limestone through time.

102

TEXT BY DANTÉ FENOLIO, PH.D. – VICE PRESIDENT OF CONSERVATION AND RESEARCH, SAN ANTONIO ZOOMATTHEW NIEMILLER, PH.D. – ILLINOIS NATURAL HISTORY MUSEUM

DAPHNE SOARES, PH.D. – NEW JERSEY INSTITUTE OF TECHNOLOGY, FEDERATED DEPARTMENT OF BIOLOGICALSCIENCES

ANDY GLUESENKAMP, PH.D. – DIRECTOR OF CONSERVATION AND RESEARCH, SAN ANTONIO ZOOPROSANTA CHAKRABARTY, PH.D. – LOUISIANA STATE UNIVERSITY MUSEUM OF NATURAL SCIENCE

YAHUI ZHAO, PH.D. – INSTITUTE OF ZOOLOGY, CHINESE ACADEMY OF SCIENCES

PHOTOS BY DANTÉ FENOLIO

The Small-eyed Barbel Sinocyclecheilus microphthalmus photographedin-situ. The same species is featured on the opening page of our story.

e headed into the field at dawn.The drive took us closer and closer to adense cluster of high limestone peaks,ultimately following a road among them.This was an area of South China we hadvisited before. We were all excited – it isexceptionally remote and with fewpeople. The region is riddled with caves.Unbelievably tangled clusters ofvegetation grow on the nearly verticalslopes. Birds, infrequently encounteredelsewhere, are commonplace again andsmall mammals occasionally dash acrossthe road and into the thick roadsidevegetation. As we climbed the steepterrain, the road began to twist back andforth – it was cut from a sheer cliff face andultimately had drop-offs that were 800 to1000 feet above the valley floor. Thewidth of the road was hardly more thanthe width of our vehicle. Any mistakedriving this route would end badly, but wehave gained great confidence in ourdriver during the past five or soexpeditions to South China. He is the realdeal - a professional. After fifteen or somiles, the road turned into a muddy, ruttedmess. A short distance farther and wearrived to an old house made ofweathered adobe. The aged structure wassheltered from the sun by an even olderlooking roof of worn, handmade clay tiles.

We would traverse the rest of the route onfoot. The locals greeted us warmly. A yearago, they had told us that there was apopulation of cavefish in nearby cavestreams. On this visit they provided ourcolleague, Dr. Yhaui Zhao, with a giftupon our arrival: a cavefish preserved inalcohol. We watched as Yahui held up theclear bottle of alcohol and stared at theslender, eyeless fish. He was amazed withthe find and was overwhelmed withexcitement. We prepared for a wet cavetrip and started toward the massive karsttower in front of us. The trail was a steepone that wound its way into a carvedvalley. At the base of the valley, a cavemouth was visible through the vegetationas a dark, circular shadow. Cold airbillowed from the cave mouth and wemade our way down muddy and rockyslopes to a stream below. With anunderwater housing and camera, wewere able to photograph cavefish wherethey live….oh what a rush – to capturethese animals in their element. (As an FYIand before we move on, the acceptedichthyological plural of fish is “fishes”when referring to multiple species).The term “cavefishes” conjures up visualimages of pink and blind animals thatalmost defy reality in appearance andSoutheast Asia has many species. In fact,

W

continued on page 107 ›

103

The Asiatic watersnake Sinonatrix aequifasciata can be found inside of caves, sometimes well beyond the twilight zone.

104

Many roads in China’s karst region traverse steep and difficult terrain. Continued exploration of subterranean habitats in Southeast Asia is critical to protecting thespecies that live there. Documentation of the distribution and diversity of cave species identifies “biodiversity hotspots” which can then be targeted for protection.

105

The Taiji Cave Loach Oreonectes anopthalmus is seriously threatened byovercollection and agricultural runoff at the only known locality.

Oreonectes macrolepis retains vestigial eyes and some skin pigmentation.

106

The Golden Line Barbel Sinocyclocheilus furcodorsalis photographed in-situ.

107

Top, caving skills are required to work in many of the caves the CCWG hasbeen investigating. Bottom, fish traps are often used to collect fish in caves.

defining cavefishes is something thatrequires explanation in a place as diverseas Southeast Asia. Some definitions willhelp here. Animals that live exclusively incaves or groundwater are knownrespectively as troglobites (or troglobionts)and stygobites (or stygobionts).Troglobionts live on the land, stygobiontsin the water. The terms are associatedwith species that are highly adapted forlife in subterranean habitats and are foundno place else. The adaptations of cave-inhabiting species come in a variety offorms that are not expressed the same wayin all species. Think of each character, likeeye size, as a variable on a sliding scale.As a species evolves in conjunction with asubterranean existence, the size anddegree of development of its eyes, forinstance, tends to slide down the scale(again, not observed in every species).These changes happen over time andacross generations, not in individuals. Thesame can be said of other key characterssuch as degree of pigmentation, bodysize, body length and girth, mouth shapeand size, and forehead shape and size.Obligate subterranean fishes in Chinagenerally, but not always, show somemodification in these characters. Whenthese characters are expressed, they areconsidered troglomorphic characters, orcharacters associated with life belowground. Some subterranean speciesdevelop structures not found in theirrelatives that live in surface habitats, andscientists are not always certain of theirfunction. The Chinese Barbels, forexample, inhabit both surface streams andsubterranean waters. The cave-inhabiting

species exhibit varying degrees ofadaptation for that environment, andsome have mysterious structures. Forexample, the Horned Golden LineBarbel, Sinocyclochielus tileihornes, hasa structure protruding from its foreheadthat looks very much like a horn. Othercave-inhabiting species have massivebumps on their foreheads and or aflattened, duck-billed mouth. We assumethat the structures have something to dowith life in the dark, but we do not knowtheir exact function yet. Just as with theother characters mentioned above, thesestructures exist on a continuum; that is,they are expressed more strongly insome species than in others. There aremany cavefishes in China that are onlyfound in groundwater but that havediffering expression of the charactersmentioned above. The blind and pinkfish found in the region are abundantand well represented. Loaches (familiesNemacheilidae and Cobitidae) andbarbels (family Cyprinidae) dominate theichthyofauna of these subterraneanwaters – but there are exceptions. One isa blind and pink catfish, described onlythree years ago, SE Asia’s first“blindcat.” But back to definingcavefishes in SE Asia…the tricky part ishow you describe the rest of the fishesthat inhabit caves for at least part of theirlives. For example, there is anassemblage of species that live in cavestreams during the day but feed inproductive surface waters under thecover of darkness, not unlike the ecologyof cave inhabiting bats. These fishestypically have fully functional eyes and

continued on page 112 ›

Hand netting of fishes is a preferred method when conditions are suitable.

108

109

Above, photography of subterranean species is a big part of the documentation process. The Chinese Cavefish Working Group has put a lot of effort intocapturing images of cave organisms where they occur and in-situ (image by Daphne Soares). Right, cave formations are commonplace in South China’s caves.

110

One of the oddly-shaped groundwater loaches, Triplophysa huanjiangensis, has an elongate head and face.This is Triplophysa huanjiangensis photographed in-situ.

111

The Tile-like Horned Barbel Sinocyclocheilus tileihornes has an interesting structure protruding from its head.No explanation for the function of this structure has been identified.

112

China is a complicated mosaic of ethnic groups with distinctive languages,customs and identities, and many of these groups retain their cultures today.

pigment; however, they depend onsubterranean habitat for their survival.They are as tied to subterranean watersas their blind and depigmented relativesthat never leave permanent darkness.Certainly, both groups qualify ascavefishes. The karst region (area that hasan appropriate geology for caveformation) of SE Asia is larger than thestate of Texas (USA) and boasts thegreatest diversity of obligate subterraneanfishes anywhere in the world. In Chinaalone, there are no fewer than 130species dependent on subterraneanwaters. There are also troglophiles,species that readily inhabit subterraneanwaters when they are available. Thisincludes a host of catfishes and cyprinidsnot typically considered cavefishesbecause they also occur in surface water,far from caves. These species cancomplete their entire life cycles in surfacehabitats but a few might also be able todo so in subterranean habitats. Our drivehome took us past the loud andunmistakable clanging of excavatorsbreaking up limestone to be hauled off toconcrete plants and tile factories. Even inthe most remote corners of China, theharvest of limestone is big business and,in part, fuels the burgeoning developmentseen across the region – one of manysignificant threats to subterranean wildlifeof the area. Other major threats includeoveruse of groundwater for agricultureand contamination from runoff,threatening entire subterraneanecosystems. Additional threats lurk in thecontemporary exploitation of cavefishesin SE Asia. For example, we surveyed a

cave and its river that we had previouslyvisited in 2011. Back then, it was abeautiful cave with few signs of humanvisitation. The river boasted a healthypopulation of one of the cavefishes yousee here, the Golden Line Barbel,Sinocyclocheilus furcodorsalis. Duringour visit this year, we found evidence ofintensive harvest of this species. Localstold us why they had been harvesting thefish (for the aquarium trade) and evenwho they were selling them to. We sawgill nets and nets of every other varietystrewn along the waterway – some inplaces where they could continue to trapfish. Fish captured this way would thensimply die in the unattended nets. Trashnow litters the cave, and there are signsof camps where fishermen burn candlesand prepare food as they wait on theirtraps. The income from harvesting thesefish is just too much of a temptation forlocals and, in all truth, primary blameshould not be placed on them. However,there is no excuse for unsustainablecommercial collection of fish for theaquarium trade. Companies selling fishfor the trade (and buying from theselocals) need to avoid subterraneanspecies – or we will lose this biodiversityin the blink of an eye. Cavefishes areparticularly susceptible to overharvest.We are working on population studiesbut they are difficult to conduct undersuch circumstances. This cave was goingto be one of our study sites. Weencountered no fish on our recent visit.The locals told us that few had been seenin several years but they used to catchthem “all the time and on each visit.” In

113

2011, we observed many dozens. Becauseof their unique ecology and limitedpopulation sizes, the vast majority ofcavefishes worldwide cannot withstandcommercial harvest (Mexican Cave Tetrasare farmed in Florida, USA, for theaquarium trade). Preliminary evidencestrongly suggests that most populations ofcavefishes in China are highly localized,vulnerable to commercial collection, andeasily removed. While it may be technicallylegal to capture and sell some of thesespecies in China, it is not ethical. Toofrequently, abuse of wildlife and wild placeshappens under the guise of “well, it’s legal,”but that does not make it ethical. Anotherexample of contemporary threats to China’scavefishes is the harvest of a host of “OilFish” (Sinocyclocheilus ssp.) that exhibit abat-like ecology. As mentioned above, thesespecies live underground during the dayand exit the cave to feed in productivesurface waters at night. Other speciesmigrate annually into subterranean watersto seek shelter from seasonal changes on thesurface. All of these movements are verypredictable in both space and time, makingfish easy targets for modern fish traps andnets. Unfortunately and predictably, acommercial fishery has developed for thesespecies, considered a delicacy in manyparts of China. Overfishing is rampant andthere are numerous examples of populationsthat have nearly vanished completely underthis harvest pressure. With commercialharvest, environmental contaminants,limestone quarries, and excessivegroundwater extraction, these species facea challenging future. We’d like to make anappeal to everyone: please don’t contributeto the loss of these species by purchasing

them, for any purpose. Regardless of whathas happened in the past, it is ourgeneration that needs to step up, do theright thing, and put conservation of rareand fragile species first. So who are “we.”We are the Chinese Cavefish WorkingGroup (CCWG), a group of concernedbiologists. We conduct surveys in SouthChina to document populations ofcavefishes and other subterranean faunaand to better understand the threats thatthey face. In addition, we are conductingstudies of biomechanics, genetics,systematics, and population ecology. Oneof the most rewarding aspects of this workhas been the opportunity for foreign cavebiologists to interact with Chinesegraduate students and train them incaving and cave biology. We are hopefulthat the next generation of Chinese cavebiologists may benefit from our efforts. Aprimary goal of the CCWG is to providecritically important data to wildlifeauthorities in hopes that some of theseamazing species can be saved. Manyhealthy populations of cavefishes remainand much can be done to ensure theirfuture. The San Antonio Zoo has been akey sponsor of the group and hasdeveloped labs for work with captivepopulations of subterranean species.Conservation breeding programs maywind up being the last stop for a few ofthe groundwater fishes below ruggedSouth China and long-term plans are inplace to develop an institute for theconservation of subterranean specieswithin China. National Geographic –China, has funded field work across thepast several years (grant numbers GEFC-15-13 and GEFC-15-16). .

Top, Frogs of the genus Odorana are troglophiles and some species are onlyknown from caves. Bottom, close-up of a Tile-like Horned BarbelSinocyclocheilus tileihornes.