Non-stygobitic fishes in caves and other subterranean habitats
Introduction
V1.0 14th August 2024
Many species of fishes have been found in caves and other hypogean environments, and they can provide us with plenty of information on the initial stages of cave colonisation, as well as being potentially important members of the non-stygobitic community of a cave. Probably most of these non-stygobitic species are accidental inhabitants, washed into the cave against their will, and doing the best they can until they get far enough downstream to regain daylight and the environment they know. Many will die in the cave through lack of food, though some may be able to feed during their involuntary journey in darkness. Brown trout (see below) are common in British caves and what evidence there is suggests that they do feed underground. The next stage in the process of colonisation is the stygophile stage, where animals can feed and breed underground but where genetic continuity with epigean population(s) is maintained so that genetic isolation does not occur. Proving that a particular species is a stygophile rather than accidental is not always easy, but there must be many species of fishes which are able to feed in darkness, and a good number which can breed.
I do not intend to discuss in detail each and every occurrence of a fish species in a cave. Such a discussion would be long, incomplete and of little value since most of the instances considered would be of accidentals. Rather, I review the evidence in the literature on those fishes which are stygophilic, possibly stygophilic, live in sea caves, or live in some other interesting hypogean habitat. Some of the cases discussed will certainly turn out to be of little value once we know more about them, but if this short contribution encourages someone to investigate them then it will have served its purpose. A list of many non-stygobitic species seen in caves worldwide, compiled by Bill Poly, can be found in Poly 2001.
Similar reviews of North American instances of non-stygobitic fishes in caves have been published recently (Poly and Boucher 1996, Poly 2001), and I have drawn upon them in my consideration of this area.
Fishes are covered in systematic order first and then region by region.
Agnatha in caves
Lampetra planeri in Yorkshire, UK
Cave-divers exploring the submerged course of the River Nidd in Yorkshire, UK (see Monico 1995:189-194 and Hill and Hall 2015:272-277 for details) have seen many small lampreys in the water they swim through. They are the brook lamprey, Lampetra planeri, on their spawning migration. The immature stage of the lamprey is the ammocete larva which spends its whole life (six years) buried in, and obtaining sustenance from, the nutrients in sediment. Upon maturation the adults swim upstream to mate and it is these animals that are noticed by the cave-divers. It seems that the cave environment is irrelevant to these animals since the ammocetes always live in darkness anyway and the adults do not feed. It seems likely that self-sustaining populations could easily live in caves provided there was sufficient sediment of the right type to support the larvae.
Lampetra soljani in the Balkan peninsula
Lampetra sojani is found the Mirna drainage area (Croatia) and the the Neretva drainage area (Bosnia and Croatia) (Tutman et al. 2017, Tutman et al. 2020, Holcic and Mrakovcic 1997, Kottelat and Freyhof 2007). It is reported (Tvrtkovic and Franicevic 2002, Gottstein Matocec et al. 2001) that ir probably lives in caves during the summer when there is little sutface water. In common with Lampetra planeri this species is non-predatory and does not feed as an adult (Tutman, Dulcic and Glamuzina 2009). [Note: Until the studies of Tutman et al. 2017 this species was thought to be Lampetra (also sometimes Lethenteron) zanandreai, and the sources cited here use that name].
Cooper and Iles (1971) observed a specimen of a Lampetra species in Deer Head Cove Cave, DeKalb County, Alabama in 1968.
Reveillet (1986) observed adult Lampetra in a cave in Belgium.
Salmonidae
The Brown Trout, Salmo trutta, in Europe and Australia
This is an essentially European species but it has been introduced into many countries worldwide (Elliott 1994:9-13). It is an unlikely cave fish being much larger than many species found in caves. However it has been recorded from caves in at least the United Kingdom (Proudlove 1979, 1982; Chapman 1993:134-139), Germany (Biese and Pappenheim 1931; Dudich 1932, Kosswig 1937) and Tasmania (Scott 1959; Lake and Coleman 1977). In the UK it is relatively common in vadose streams in caves in Yorkshire where it tends to be very pale in colour, almost white. This is not due to evolutionary pigment loss, as in true cave fishes, but to a physiological reaction to darkness. Melanin pigment resides in cells termed melanophores and it may be distributed throughout the cell, resulting in a dark looking fish, or concentrated into the centre resulting in a pale animal. All brown trout from the UK that have been examined have been in the latter condition. The German sample from the Grosse Tropfsteinhoehle conformed to this pattern (Biese and Pappenheim 1931, Dudich 1932, Kosswig 1937). It has lost all of its red carotenoid pigment and had small, contracted melanophores. The Tasmanian sample (Scott 1959) was “of notable general paleness”.
These animals arrive into the cave primarily by drifting downstream with the current, perhaps during flood conditions (although Guy (1982) argues that this is unlikely and that upstream movements are more likely, see Guy (1982) and Proudlove (1982) for opposing views on this matter). Some will pass through the cave system to emerge back into daylight while some will probably starve to death over a long period. Some however may well continue to live in the cave for a considerable period and it seems likely that they can feed in darkness. A single individual from Lake Avernus in Ingleborough Cave was collected by Glover (1978). The snout of this animal was rather blunt and scarred and its stomach contained small stones as well as the remains of benthic organisms such as Gammarus pulex (Crustacea: Amphipoda). Food in the stomach of a trout is evidence of very recent feeding as food normally passes quickly backward into the intestine (see Elliott 1994:74-75 and references therein for details of this). Since it is impossible that this fish traversed over a mile of cave in the short time that stomach evacuation takes place it must have obtained the food from the cave stream. Trout living in a very turbid river, with very restricted visibility, were shown to feed on the bottom rather than in mid water (Tippets and Moyle 1978), a situation analogous to that in a cave.
Important life history details of Salmo trutta, with pertinent observations on isolated polulations, can be found in Klemetsen et al. (2003) and Griffits et al. (2009). The genetics of isolated populations of brown trout were examined by Campos et al. (2006).
Balon, Crawford and Lelek (1992) report that there is an underground connection between the upper River Danube and tributaries of Lake Konstanz near to Aach, Germany. Kottelat (1997:129) hypothesises that this connection may be significant in the distribution of trout in the area. It is this subterranean conduit which is now known to contain the troglobitic Barbatula underscribed species (Behrmann-Godel et al. 2017).
Kovac et al. (2014) record that Salmo trutta is common in subterranean waters in Slovakia where they are depigmented to a degree. They suggest that this is a result of permanent populations in caves demonstrating ecological and physiological pre-adaptations for the colonistaion of karst waters. The first report of this species in caves in Slovakia was by Buchholtz (1787) and they are also mentions by Gulicka (1986).
The story of a Brown Trout from Ingleborough Cave, Yorkshire.
Brown Trout in Porth yr Ogof, South Wales by Christine Grosart.
The Arctic Char, Salvelinus alpinus, in caves in Iceland
Judson (2022, unpublished Thesis) studied populations of Arctic Charr sampled from 19 lava caves near Lake Mývatn, Iceland to assess the hypotheses that patterns of genetic and phenotypic variation are affected by: (i) colonization history; (ii) genetic drift and gene flow coupled with contemporary landscape features; and (iii) divergent natural selection caused by ecological variation as an agent of selection. He detected significant signatures of colonization history based on the genetic clustering of the cave populations and their relationship to the lake fish. Signatures of genetic bottlenecks and the association of genetic variation with geography and population size suggest that genetic drift has contributed to population divergence. Estimates of gene flow and fish movement are positively related to the geographic proximity of populations. In contrast, he found limited evidence that patterns of genetic and phenotypic variation are related to ecological variation. This work is now published in Judson et al. (2024).
Esocidae
Only a single report of a Pike (Esox lucius) in a cave is known (Anonymous 2022) and nothing at all is currently known about the caves it was seen in.
Cottidae
The Bullhead or Millers Thumb, Cottus gobio, in Europe
The Bullhead, Cottus gobio, is a widespread and common freshwater fish in Britain. In many caves with active vadose streams it is commonly seen lying on the bottom but soon scurries off once disturbed. Unlike the brown trout it does not become pale in colour, retaining its green/brown hues. It seems clear that it either chooses to swim into underground places or, more likely, is carried there by the current. Proudlove (1979, 1982) described its presence in British caves and Wuestemann (1988) studied its ecology in a cave in Germany. Anyone studying this species in caves should consult Tomlinson and Perrow (2003).
The banded sculpin, Cottus carolinae, in the USA
One of the most interesting of all cases of this sort is that of members of the Cottus carolinae species group in several caves in the eastern United States. Williams and Howell (1979) recorded an albino banded sculpin from Buckeye Creek Cave in Greenbriar County, West Virginia (see also Poly and Boucher 1996). In addition to being colourless, it had enlarged cephalic canal pores, fusion of the two post-mandibular pores and a reduced number of pelvic fin rays. They suggest that speciation in the folded limestones of the area may be enhanced and that this animal may be a stray from a true cave-adapted population. Jenkins and Burkhead (1994) consider that this should be considered as a new species, though Poly and Boucher (1996) wisely suggest that further specimens should be examined before this is accepted.
Cottus bairdii and Cottus carolinae are both found in caves in Georgia (Cope and Packard 1881, Dearolf 1956, Poly and Boucher 1996, Poly 2001, Buhlmann 2001, Huntsman et al. 2011, Venarsky et al. 2012, Niemiller et al. 2006, Niemiller et al. 2016, Zigler et al. 2020).
Sculpins have also been recorded from Sculpin Cave in Kentucky (Bryant, Erisman and Hockersmith 1972).
It seems most likely that one or more of these instances is of incipient cave colonisation and adaptation, with progressive (cephalic lateral line system modifications) and regressive (eye size and pigment reduction) features displayed.
The Yellow Bullhead, Ictalurus natalis, in Florida, USA
Relyea and Sutton (1973) record this species in two caves in Alachua County Florida, Bat Cave and Martin’s Cave, both of which are 12 km from the nearest surface drainage. Adults and juveniles are present in both locations and appear to feed successfully as they are healthy and not emaciated. The presence of juveniles so far from a surface water supply suggests that the animals breed in the cave. There are a number of anatomical abnormalities in the fishes, primarily the absence of any of pelvic, caudal and adipose fins. This may be because of inbreeding in a small, closed population. Relyea and Sutton suggest that this species is preadapted to cave life because it has an elaborate chemo-sensory system. Taking all of these points together there is a very strong suggestion that these populations are stygophilic. Streever (1992) records the death of a large number of yellow bullheads at the Peacock Springs Cave System in Suwanee County, Florida. Whether these animals are also troglophilic is not known.
Trichomycteridae
Trichomycterus straminius in Colombia
Members of this species were observed by Sket (1988) in various caves in Colombia. He reported that some were strongly depigmented and it is possible that truly troglobitic populations of this species exist in some Colombian caves. The evidence for this is not complete and for the moment I retain this species here rather than in the main part of the species accounts. Whatever the status eventually allocated it is clear that these are most interesting animals which are worthy of further study.
Trichomycterus gorgona in Colombia
Fernandez and Schaefer (2005) described this species from a freshwater stream near the northeastern end of Isla Gorgona (2°59'N, 78°11'30"W) off the coast of Colombia. It had obviously reduced eyes and melanin pigmentation. It was collected in a steep and fast flowing epigean stream in 1961 (de Sylva 1963) and the troglomorphisms may be due to similar selective pressures as in in other epigean but troglomorphic fishes. Clearly further searches are required in the area to see if there are any caves in which the species might actually live.
Loricariidae
Chaetostoma microps climbing a wall in a cave in Ecuador
Hoese et al. (2015) recorded an instance of the loricariid fish Chaetostoma microps climbing a flow stone slope and their film of this is fascinating.
Anguillidae
The Atlantic eel, Anguilla anguilla, in Europe
The Atlantic eel (Anguilla anguilla) is common in some caves in the United Kingdom and in Ireland. In Yorkshire they have most often been seen in caves in Dentdale, particularly Tub Hole (see Monico (1995) and Hill and Hall (2015) for details) (Proudlove 1979, 1982). Trombe (1952) reports them from caves in France where they penetrate more than a kilometre into some.
Vilter (1951) examined the retinal structure of Atlantic eels from epigean and hypogean environments.
One of the very earliest accounts of fishes in underground habitats is that of Besson (1569). He said that he has observed small eels living in subterranean waters in France. This seems not unlikely (See also Romero and Lomax 2000).
Eels have proved to be useful in the study of cave hydrology. Wagner (1954) introduced tagged eels into Skocjanske Jama in Yugoslavia and they reappeared 55 days later at the Timavo resurgence near Triest in Italy. This is a 50 km journey so they travelled at about 1 km per day (Bogli 1980). They have also impeded cave study. Trombe (1952) records that an “enorme anguille” attacked l’Abbe H. Breuil in the Toc d’Audoubert, Ariege when it was dazzled by the bright light of his acetylene lamp!
Biological studies in the Frasassi Caves in the northeastern Apennines of Italy revealed many sub-fossil Eurpean eels is a large chamber. This had once been filled with water which was colonised by the eels. Taphonomy and carbon-isotope analysis of the eel remains indicate that the animals periodically entered the cave from the Sentino River that flows outside the cave through the deep Frasassi Gorge. The eels survived in this hypogean environment feeding on sulfur bacteria (Peterson et al. 2013).
The American eel, Anguilla rostrata, in north America
The American eel (Anguilla rostrata) can be found in springs and caves in Florida. Pylka and Warren (1958) observed one in Gerards Cave, Marianna, Jackson County. Helfman (1986) studied a population at Vortex Blue Springs in Holmes County. Larger eels always occurred deeper into the cave. All eels were quiescent during the day and active at night, their activity levels determined by light level.
Cyprinidae
Fishes in the Dinaric Karst
There is no doubt that the fishes of the Dinaric Karst are the most important non-stygobitic fishes in the world. They show many times over the mechanisms of cave coloisation and troglomorphic to troglobitic evolution in action. We can learn a great deal about these mechanisms from detailed studies of their biology.
The Dinaric Karst is doubly famous. First as the source of the word “karst” (from Kras, a region on the Italian-Slovenian border), and second as the home to one of the most diverse subterranean ecosystems on earth (Sket, Paragamian and Trontelj 2004, Sket 2004, 2005, 2012, Hajna 2012, 2019). The first described troglobite, the urodele amphibian Proteus anguinus (see Sket 1997, Goricki et al. 2012, Goricki et al. 2017 and Voros et al. 2017), was noted in this area by Valvasor (1689) and described by Laurenti (1768). Despite (or perhaps because of) the presence of this highly adapted stygobitic vertebrate there are no equally evolved fishes. However the area contains a number of very interesting fishes, some of which are certainly troglophilic, others habitual trogloxenes. It is certainly possible that some are even stygobitic but not proven a such. An important source for this area, and all of the Balkans, is Negm et al. (2020) which described all of the water resources of the area. Also important is Griffiths et al. (2004). Brancelj et al. (2019) describe in detail the major components of the stygophilic fauna. Equally important is the paper by Lukac et al. (2024) on the genus Delminichthys.
Phoxinellus alepidotus Heckel 1843
Delminichthys adspersus (Heckel 1843)
Delminichthys ghetaldii (Steindachner 1882)
Paraphoxinus ghetaldii Steindachner 1882
Paraphoxinus pstrossii Steindachner 1882
Phoxinellus pstrossii (Steindachner 1882)
Delminichthys jadovensis (Zupančič and Bogutskaya 2002)
Delminichthys krbavensis (Zupančič and Bogutskaya 2002)
Telestes croaticus (Steindachner 1866)
Phoxinellus croaticus Steindachner 1866
Telestes fontinalis (Karaman 1972)
Phoxinellus adspersus fontinalis Karaman 1972
Telestes karsticus Marcic and Mrakovicic 2011
Telestes metohiensis (Steindachner 1901)
Paraphoxinus metohiensis Steindachner 1901
Phoxinellus metohiensis (Steindachner 1901)
Telestes polylepis Steindachner 1866
Telestes turskyi (Heckel 1843)
Squalius turskyi Heckel 1843
Leuciscus turskyi (Heckel 1843)
Squalius svallize Heckel and Kner 1857
Phoxinus karsticus Bianco and De Bonis 2015
This taxon was well supported by mitochondrial DNA but has limited supprt from nuclear genes (Palandacic et al. 2017).
Phoxinus likai Bianco and De Bonis 2015
All of these fishes are epigean by choice but in some areas there is no surface water during the summer months and the fishes retreat to the only water available, in limestone caves. When surface water reappears the fishes leave the caves and breeding takes place. This is perhaps the best example among the fishes of an habitual trogloxene. Thines (1969:9) considers them to be troglophiles. Discussed as early as 1895 (Apfelbeck 1895) the classic accounts of “Paraphoxinus” is that of Spandl (1926). Hawes (1938, 1939) considers them during a discussion of flooding as an ecological factor. The best modern treatment are those of Leiner (1980-81), Gulika (1986), Zupancic (1990) and Zupancic and Bogutskaya (2002). The former comments that: “Although about a hundred years have elapsed since these fishes were scientifically described for the first time, we possess just a limited knowledge of the species life and taxonomy. The available data about the species ... are mostly due to the investigations and work undertaken by elder authors.” Some details of “the species life” are provided by Maric (1991) who examined reproduction in P. alepidotus. The chromosomes of the same species were examined by Berberovic, Hadziselimovic and Sofradzika (1969). Sofradzija and Berberovic (1972) studied the chromosomes of all of the above mentioned species. All of these species are endemic to small areas and are threatened (Mrakovcic, Misetic and Povz 1995). Both Cihar (1991:83) and Miller and Loates (1997:114) only mention P. ghetaldii as a cave dweller. The former of these says (p.83):
“P[araphoxinus] ghetaldii is a particularly interesting little fish. Like the others it measures about 10 cm, but it inhabits the water in caves in the karst region of Bosnia and Herzegovina. Living as it does in the dark, it is very characteristically coloured; it has a dingy brown back, yellowish to golden yellow sides and a white belly, while the whole of its body is thinly speckled with small, irregular brownish black spots. It lives mainly on underground aquatic crustaceans.”
Mrakovcic, Misetic and Povz (1995) review information on these species and provide a full reference list including many papers in the local languages. These authors state that little work has been done but that: “Among the most endangered species of the Adriatic catchment in Croatia are all species in the [genus] Paraphoxinus”. It is to be hoped that it will be possible to study these most interesting animals before they are finally lost, though it seems unlikely that this will happen.
Tvrtkovic (1999) records that “As for the ecology of the endemic fish species of the occasionally surface streams, little more is known today than was observed by Trgovcevic (1905), who found that some of the Phoxinellus spp. spawn only underground”.
Franicevic and Oertel (1999) provide some details of Phoxinellus adspersus at one site, Red Lake near Imotski in Croatia.
Zupancic and Bogutskaya (2002) give an account in English of the distribution of Phoxinellus species in Croatia and in Bosnia. This is complemented by the account of Tvrtkovic and Franicevic (2002) which carries a very good reference list to all Croation hypogean species.
Bogutskaya and Zupancic (2003) provide morphological details for all Phoxinellus species in Croatia and Bosnia-Herzegovina.
Jelic and Jelic (2015) report that D. ghetaldii was re-found in Croatia and is in need of urgent consevation attention.
Miller and Loates (1997:104) record that this rare fish is “Found only in the western Balkans. Bottom living, in flowing water, including subterranean reaches of karst rivers; locally common but overall classed as very endangered”. Mrakovcic and Misetic (1990) give its underground distribution as streams and lakes of Livanjsko and Duvanjsko Polje. Vukovic and Ivanovic (1971) say that it migrates into underground streams in winter. This is an interesting contrast to the other cave inhabiting Dinaric fishes, those in the genus Phoxinellus, which retreat into caves in summer as the surface water levels fall. Buj et al (2021) made a detailed study of this species and this paper should be consulted by all with an interest in this species.
See also Buj et al. (2022), Reier et al. (2022).
Soric and Banarescu (1999) record the following:
“Many underwater holes near the shore of the Jaruga River are connected to caves. In autumn, usually October, when the level of the subterranean water becomes lower, the fishes migrate into the underground water. In spring, usually at the end of March or beginning of April; when the level of the subterranean water rises, the fishes return to the Jaruga River ...”
Buj et al. (2022) studied the population genetic structure of Telestes species facilitating their survival in changing environments in Croatia.
Marcic et al. (2022) studied the early development of Delminichthys krbavensis (Leuciscidae, Cypriniformes) from a karstic field in Croatia.
Milanovic (2023) provides an in depth account of the karst area Karst of East Herzegovina and Dubrovnik Littoral
Lukac et al. (2023) studied the evolution of body shape diversification of the endemic Cyprinoidei fishes from the Balkan’s Dinaric karst
“Hybopsis” or “Erimystax” harperi and its subspecies “subterranea” in the USA
Marshall (1947) reported on the cyprinid Erimystax harperi in streams and rivers emerging from the many vauclusian risings (termed spring runs) and from caves in Florida. This species was also studied by Hubbs and Crowe (1956), Relyea and Sutton (1972, 1973) and Brockman and Bortone (1977). Howell (1960, 1961) made a thorough study of the variability and habitats of this species. According to Eschmeyer, (1998) this species is a synonym of Notropis harperi.
“Puntius microps” in Java
Barbus microps was described by Günther (1868) and said to be closely allied to Barbus maculatus but with much smaller eyes. This species was from “Java (?)”. Jacobson (1912) reported on a visit to Java in February and March of 1911 and entitled his article “Iets over blinde visschen” which translates as “About blind fishes”. Specimens he collected were examined by Weber and DeBeaufort (1916) who decided that they were the same as Günther’s microps but they placed this species in the genus Puntius. The provenance of these specimens is given as “Java (subterraneous river in cave Djomblang near Gunung Sewu in Djocja !)”. They make the very significant remark that “some of the specimens from the above named cave, collected by Mr. E. JACOBSON, have lost one or both eyes, probably through mutilation by crustacea”. Thines (1969:88) includes this species as one of his “poissons cavernicoles” but adds no further information. In more recent times British cavers have explored many caves in the Gunung Sewu area of Java. In the same cave as that mentioned by Weber and DeBeaufort (1916), Gua Djomblang, Willis, Boothroyd and Briggs (1984) discovered and collected a number of small light coloured fishes. These were sent to the Natural History Museum in London where Keith Banister identified them as Barbus microps which he described as “quite widespread”. Some of the fishes have reduced eyes, some asymmetrically. Maurice Kottelat has examined these same specimens and is of the opinion that they are actually Puntius binotatus (pers. comm. 1998). The specimens are retained in the collection of Maurice Kottelat (accession number CMK 15108). It is possible that this is an incipient troglobitic population which still retains genetic continuity with epigean Puntius binotatus.
The chub, Leuciscus cephalus, in Slovenia
Kosswig (1937) discovered two young chub in the Grotta Nera near “Postumia” (now Postojna). They were very light in colour and (in translation): “... show such an insignificant production of melanophores on their bodies, that they appeared as white in the living state but particularly when fixed. When the examples were alive the gills glowed weakly reddish through the gill-cover.”
Characidae
Astyanax mexicanus colonising caves in Texas, USA
McGaugh et al. (2019) have studied populations of Astyanax mexicanus which have recently colonised caves in Texas. The abstract of their paper follows: "Cave colonization offers a natural laboratory to study an extreme environmental shift, and diverse cave species from
around the world often have converged on robust morphological, physiological and behavioural traits. The Mexican tetra (Astyanax mexicanus) has repeatedly colonized caves in the Sierra de El Abra and Sierra de Guatemala regions of north-east Mexico ~0.20–1 Mya, indicating an ability to adapt to the cave environment. The time frame for the evolution of these traits in any cave animal, however, is poorly understood. Astyanax mexicanus from the Río Grande in South Texas were brought to Central Texas beginning in the early 1900s and colonized underground environments. Here, we investigate whether phenotypic and behavioural differences have occurred rapidly between a surface population and a geographically proximate cave population, probably of recent origin. Fish from the cave and surface populations differ significantly in morphological traits, including coloration, lateral line expansion and dorsal fin placement. Striking behavioural shifts in aggression, feeding and wall-following have also occurred. Together, our results suggest that morphological and behavioural changes accompanying cave colonization can be established rapidly, and this system offers an exciting and unique opportunity for isolating the genetic and environmental contributions to colonization of extreme environments."
Heptapteridae
Pimelodella transitoria in Brazil
This species is commonly found as a troglophile in caves in the Parque Estadual Turistico do Alto Rebeira (PETAR). It is thought to be the sister species of the stygobitic Pimelodella kronei. Work on P. transitoria has been carried out in association with work on P. kronei by Trajano (1986a, 1987a, 1989a,c, 1994) and these publications provide details of the biology of P. transitoria.
Rhamdia guatemalensis stygeae and Rhamdia guatemalensis decolor are commonly seen in Cenotes in Yucatan, Mexico, and are very probably troglophilic in various subterranean habitats within the Yucatan karst. The subspecies are present at low density in caves and concentrate around cenotes (Horst Wilkens pers. comm.). Details in Hubbs (1936, 1938). See also Monvoisin (1998).
Synbranchidae
The common epigean swamp eel Ophisternon aenigmaticum is reported from the sulphidic cave system Cueva del Azufre in Mexico (Gordon and Rosen 1962, Riesch et al. 2009, Greenway et al. 2014, Riesch et al. 2015).
Cichlidae
Cichlosoma urophthalmus is also reported from similar habitats (Hubbs 1936, 1938). See also Monvoisin (1998).
Poeciliidae
Barona and Espinasa (2004) used molecular methods to study the relationships of Gambusia yucatana in isolated cenotes on the Yucatan peninsula. They showed conclusively that these troglexenic fishes are genetically isolated from one another and that each cenote population does not migrate and reproduce with other cenote populations. This raises the question of how they colonised the various cenotes in the first place. Barona and Espinasa point out that this species gives birth to live young and so the oft-made claim that eggs can be blown by the wind, or carried on birds feet, cannot apply here.
Gobiidae
The Neretva dwarf goby, Knipowitschia croatica, is found in a very small area around the southwestern border of Bosnia and Croatia (Kottelat and Freyhof 2007:569-570). In common with the numerous Cyrinidae which live in similar karst areas it probably migrates into subterranean waters in summer when surface water is rare.
Amblyopsidae in the USA
Of the six species in the family Amblyopsidae four are troglobitic. one (Chologaster cornuta) epigean and one, Chologaster agassizii, is troglophilic. This animal is distributed in springs and caves from south-central Tennessee, south-central Kentucky and southern Illinois, USA (Woods and Inger 1957, Cooper 1980). The most extensive studies of this species are those of Hill (1966, 1968, 1969, 1969). The life history and distribution were studied by Smith and Welch (1978) who also provided population estimates for southern Illinois. Morphological studies
have been made (e.g. McNulty 1978, 1984). Other studies have been made by Palunas (1989, life history), Robinson (1981, presence in Kentucky), McDonald and Pflieger (1979, in south-eastern Missouri) and Weise (1957, in Illinois).
Vertebrate fauna in caves of eastern Tennessee within the Appalachians karst region, USA
Niemiller et al. (2016) recorded eight species of fishes within caves in this region.
Gadidae in a cave on the the River Sim (Southern Urals, Chelyabinsk region)
Abdullin et al. (2015) record a Burbot (Lota lota (Linnaeus 1758) from a cave
“Les poissons souterrain du Sahara”
The Sahara desert is a massive area and much of it has underlying aquifers (Goncalves et al. 2013) which show at the surface as natural oases. The aquifer water is also accessed by many man-made wells. The native peoples of the Sahara will have dug wells since time immemorial, but more and deeper wells were sunk by the French authorities in Algeria in the 19th century (e.g. “Captain Zickel, Director of the artesian borings in the desert”; Desor 1864). It was during these processes that fishes appeared from the wells, and these were of interest to French naturalists and scientists. The following accounts all provide information on this interesting phenomenon: Gunther (1859), Desor (1864, 1864, 1864, 1864, 1871 see also Ramsay 1864), Schroeder (1879), Rolland (1881, 1895), Jus (1886), Girard (1889), Blanc (1895), Hult (1895), Leveque (1990), Heggen (2015). It is clear that further work is required to fully understand the mechanisms underlying the presence of fishes within, and their transportation through, these aquifers. It is clearly time for a re-examination of this in order to understand what is happening.
Fishes were first noticed at Ain-Tala in 1861. They had very short ventral fins and were probably Aphanius apodus. The eyes were well formed and the fishes could apparently see perfectly well.
Barbus figuigensis Pellegrin (AMNH 8820, 2 specimens) reported to be from a subterranean habitat at Fraggard, south of Obansii in the Algerian Sahara (James Atz pers. comm.).
For details of desert environments in general see Hillyard et. al. (2015), Heggen (2015), Laumanns (2017) and Helfmann et al. (2009:410-415).
A trogloxene fish from China
A barbine cyprinid, Varicorhinus macrolepis, is distributed throughout the Chiangjiang River in China. When it is found in karst areas it enters caves in winter, from November till April. During this period the temperature of the cave water is higher than the surface water. In the cave the fishes decrease in condition factor and assimilate fat stored during the summer. On leaving the cave the intestine is empty suggesting that the fishes do not feed within the cave. This is an example of habitual trogloxeny and is analogous to that of bats which hibernate in caves in cold weather and do not feed there. Information from Zhang (1986).
Fishes in Syria ?
A report in the journal Aquariana (volume 1, 1933) mentions possibly hypogean fishes in Syria: “Saleem Makarius, a Syrian, in 1898 described 5 different types of completely blind and abnormal fish, in cave waters of Syria”. This is supported by a statement: “Halliburton also says those observed on his grotto explorations are blind”. (Details from James Atz, pers. comm.). There is no modern information on this area and it is not possible to say whether cave fishes are really to be found in Syria.
A cave in Croatia
During a cave diving expedition to Crveno jezero, near to Imotski in Croatia, four species of fishes were discovered in the very deep lake. They possess eyes and are not thought to be true cave fishes. They may however be endemic to the cave lake (Mladen Gerasic pers. comm. 11/98).
“Blind white fish in Persia”, the qantas of Iran
A classic travel book of the 1950’s was “Blind white fish in Persia” by Anthony Smith (Smith 1953, 1979, 1990). Smith had heard that such fishes had been seen in Qanats of Iran. These are man-made sub-horizontal tunnels which tap into subterranean water supplies. Smith and his colleagues found no blind white fishes and none are known today. The qanats do however have an interesting fish fauna and it has been described in detail by Coad (1996). Anthony Smith was rewarded for his interest many years later when Nemacheilus smithi Greenwood 1976 was named for him.
Fishes in Irish caves
David Drew is an authority on the caves and karst of Ireland. In his time studying these subjects he has come across instances of fishes within the caves. Below is his observations on this:
1. Tratman (1969:31-32) included the following brief notes on animals in the caves of Clare: The caves are subject to frequent flooding. Most of them also lie very shallowly under the surface of the limestone. Though animals have been found in the caves, search for a true cave fauna has so far been unsuccessful. Such a fauna may yet be found in some remoter parts that are not subject to flooding or copious flushing or perhaps in caves such as Vigo Cave, which do not have an active stream running through them.
Recently Spence (1965) has reported on a trout (Salmo trutta) found in the Doolin Cave but it is obviously an introduction from the surface and not a true troglodyte form. Other specimens have been seen in this cave by UBSS and eels (Anguilla anguilla) in G5. In July 1966 a Nottingham University Spelaeological Society expedition to Co Clare specialisecl in collecting fauna. A report has appeared which confirms the previously expressed view that in the main the living fauna in the Clare caves will be largely that of surface streams. Nearly albino frogs, which reacted very sluggishly to light, have been found far down several caves. They seemed to be well nourished.
Tratman (1976) provided the following account: A party of the Cork Speleological Group went down Coolagh River Cave, Co. Clare in July 1975. In the streamway immediately above Balcombe's pot a young salmon (Salmo salar) or peel was found. It was about 25 cm long. It was caught, examined and released. Its presence was vouched for by all the party, which contained several fishermen, and they were emphatic that it was a salmon and not a trout. The salmon could only have got to that position via the inter-tidal resurgence of S5, south of Pollsallagh, about 2.5 km away. It is also reasonably certain that it came up during a flood pulse because before that it would have had to leap at least 2.5 metres to get out of Balcombe's Pot. This is probably too high for a fish of the size given a very low flow over very smooth rock. It can also be inferred that there exist long stretches of open passage along the route to the sea but it does not follow that these passages are passable to man even if they could be located.
2. A pike (Esox lucius) was seen in a well to the west of Loch Corrib (Anonymous 2022). The well well is distant from any known caves or sinking streams. I'm guessing it is a natural collapse to water that has been modified for water supply and only a few metres deep. I suppose it must intersect a cave stream that drains to a spring near the lake but there are no known springs on the lake edge in the area
3. Fish sightings I have had or have been mentioned to me have all been pale, small/medium presumed trout. Certainly in Doolin cave which discharges below high tide into the sea. It is difficult to sea how they got into the cave which has very limited surface headwaters but then I have never understood how the same freshwater fish manage to get into every decent sized river without swimming round to the next estuary via the sea.
4. Much more common in Irish caves are eels ranging from elvers to fully grown. In the Burren in Pollballygoonaun, either side of a steep drop in the streamway, in Galway in the far stream passages of Ballyglunin Cave (boiler suit filled with them on occasions) on most spectacularly in the stream caves which link Lough Mask with Lough Corrib (Galway-Mayo). Eel traps used to be operated on the major sinks and spring and in the estavelles draining many turloughs in the area. In Ireland eels seem to use subterranean passages to migrate upstream from the Atlantic Ocean. David Drew (personal communication July 2022) has suggested the following scenario: The Lough Mask eels are part of a very extensive karst-conduit migratory system for eels. Lough Mask drains underground into Lough Corrib (via channels that are >50m deep = well below sea-level) and Lough Corrib drains into the Atlantic via Galway Bay. The majority of the inflow from the eastern (limestone) side of the 2 lakes is from major karst springs which drain much of the lowlands of east Ga/way, south Mayo and further afield. Thus, migratory eels must use the extensive system of karst channels to reach the inland drainage system.
Brazil
Bichuette and Trajano (2002, 2003) provide details of the epigean and hypogean fishes found in Sao Domingos karst area in Brazil.
India
An intriguing case of a cyprinid from a possibly man-made cave (perhaps a copper mine several thousand years old) near to Udaipur in Rajastan, India is reported by Tehsin, Durve and Kulshreshtha (1988). One specimen was collected from near to the cave entrance and when examined had characteristics intermediate between Schizothorax and Diptychus. The accepted distribution of these species extends in a crescent from Pakistan eastward to Tibet and China and they are restricted to Himalayan and sub-Himalayan drainages. This record is from a site many hundreds of miles from this distribution. The authors speculate that either this is a relict population which had diverged from the ancestral characteristics (hence its intermediate state) or that there is an underground drainage from the Himalayan region to the this area of India. This seems most unlikely but further studies are obviously required.
A cave in Andhra Pradesh, India
In a study of Nelabilum Cave, south-east of Ankireddipalle village, Kurnool District, Andhra Pradesh (15°00'05"N, 78°03'20"E), Ranga Reddy and Sharma (2010) found seven non-troglobitic fishes: Puntius sarana, Puntius ticto, Rasbora daniconius, Garra gotyla stenorhynchus, Mystus cavasius, Mystus bleekeri and Channa orientalis. All were epigean fishes with no modifications to cave life.
Pakistan
Butt (1992) comments on the seasonal migrations and dispersal of fishes in the North West Frontier province of Pakistan. Specimens of Puntius sp., Crossocheilus latius and Barilius vagra (all Cyprinidae) have been collected from wells 25 m deep in the area. The same species are also found in spring fed pools hundreds of metres above the base-level river. Butt (1992) remarks that dispersal of fishes through underground channels is an important mechanism in this area.
USA (California)
Sometime around 1874 a well was dug close to San Buenaventura in California. It was 143 feet deep and was sunk only five feet from the high water mark on a beach. One day it was noticed that young trout (all about 2 inches long) were being ejected from the well in large numbers. They were examined and found to be perfectly normal and had eyes. The nearest river, the Santa Clara, is several miles away from this well and it seems that the trout must have travelled some distance in subterranean conduits to reach the well. This is an interesting example because it suggests that the trout would be making a, perhaps extensive, journey underground. Was this part of a normal migratory pattern or was it in exceptional circumstance intercepted by the well? We do not know, but it is worth bearing in mind when considering cave colonisation. Details from Chase (1874). It seems to parallel the example described from Pakistan by Butt (1992). Caton (1885) reported on blind fish from flowing artesian wells but this has not been confirmed. A supposedly blind fish was found in a cave in Califonia (Anonymous 1950) but this has not been confirmed or seen since.
Elliott et al. (2017) provide details of the known cave fauna of California. There are no known troglobitic fishes which is a surprise given the quantity of karst, the number of caves (c4000 of which c 1000 have been biologically sampled) and the tropical conditions prevaling in the State. See the California entry in the Fishless karst area of the web site.
USA (Florida)
Walsh (2001) provides a useful summary of the biology of Florida caves and springs and see also Brockman and Bortone (1977) and Hale and Streever (1994). See the entry for Florida in the Fishless karst section of the web site.
[More references to add].
Chile
Lataste (1892) reports on fishes which he claims were “vomis par les puits artesiens”. See also Girard (1889).
Australia
Humphreys (1995) examined cave fauna in the limestone area of east Kimberly, Western Australia. Two species of fishes were observed, Neosilurus hyrtlii Steindachner, 1867 (Plotosidae) and Leiopotherapon unicolor (Gunther 1859) (Terapontidae).
Morocco
Gambusia affinis is used in Morocco for control of Anopheles mosquitoes (Bouallam, Badri, Maarouf and Bouzidi 1997).
Fishes in sea caves
Sea caves are of two types: cavities which open at the sea-land boundary and caves which are completely submerged. Moore (1954) discusses the origin and development of sea caves. They have been extensively and intensively studied by a number of workers and the following is a very brief review of some details.
The classic accounts are those of Riedl (1966) and Riedl and Ozretic (1969). The first of these is a most extensive work running to nearly 700 pages. It is in German and there is no English translation available. Other workers have also made studies of sea caves (e.g. Abel 1959, Zander and Heymer 1976, 1977, Zander and Jelinek 1976, Harmelin, Vacelet and Vasseur 1985; Gili, Riera and Zabala 1986, Zander 1976, 1980, 1990, Herler et al. 1999).
Zander and Jelinek (1976) studied various aspects of the biology of fishes in the Grotte de Banjole, Yugoslavia. Of 11 species present in the cave they classified 3 as facultativeley speleophilous and 2 as obligate speleophilous (Blennius (now Lipophrys) nigriceps and Tripterygion melanurus). The breeding system of T. melanurus was studied by Geertjes and Videler (2002). Recently Arko-Pijevac et al. (1999, 2001) have studied a submarine cave near Vrbnik in the Adriatic Sea. They found that the most numerous fish in the cave was Thorogobius ephippiatus (Gobiidae) whereas Gammogobius steinitzi (Gobiidae) was restricted to the cave. See also Bakran-Petricioli and Kruzic (2002) and Gottstein Matocec (2002) for details of sea caves and anchialine caves respectively, in Croatia.
The adaptations of sea cave fishes are, not surprisingly, different to those of true troglobitic fishes. Sea caves are dimly lit rather than totally dark and Lipophrys nigriceps exhibits the following characteristics: reduction in basic melanophore pigmentation, development of clinging organs, enlargement of eyes and lenses combined with an effective ratio of retinal elements and modes of accommodation (Zander 1980). The melanophore reduction is a regressive feature shared with troglobitic fishes but the eye enlargement is a progressive feature.
Uiblein (1995) studied behavioural and morphological plasticity in facultative cave dwellers and secondary deep-sea fishes.
Ragkousis et al. (2021) made an extensive study of rarely reported cryptobenthic fish in marine caves of the eastern Mediterranean Sea, including data on Corcyrogobius liechtensteini, Didogobius splechtnai, Gammogobius steinitzi, Thorogobius ephippiatus, Microlipophrys nigriceps, Tripterygion melanurum, Grammonus ater and Lepadogaster cf. lepadogaster. These species have been rarely reported from the Eastern Mediterranean.
Kovacic et al. (2021) is an important study of qualitative and quantitative aspects of marine cave fish assemblages in intracave cavities.
Fishes in springs and spring runs
A spring is usually thought of as a place where water emerges from below ground. While influenced by light it will in most other factors be rather similar in physical and chemical condition to the underground stream which it previously was. The spring habitat is home to a particular fauna and flora, and as an interface (Botosaneanu (1998) says “Sources: Aux portes du Styx”, Springs: Gates to and from the Styx) between hypogean and epigean habitats is of considerable relevance to the study of cave organisms. The classic studies are those of Culver, Kane and Fong (1995) on the amphipod crustacean Gammarus minus and there are no comparable detailed studies of fishes. The amblyopsid Forbesichthys agassizii is probably the best studied spring fish (Hill 1966, 1968, 1969, 1969; McNulty 1978; Smith and Welch 1978; McDonald and Pflieger 1979; Robinson 1981; Fournie and Overstreet 1985; Metzke, Adams and Adama 2016). Dan Fong has suggested (pers. comm. 1997) that he may study it as a vertebrate analogue of G. minus. Information on these phenomena can be found in Botosaneanu (1998) and Hobbs (1992). Both are very useful sources and included many references to the literature on the subject.