The world's deepest subterranean community - Krubera-Voronja Cave (Western Caucasus)

INTRODUCTION

Since Jules Verne wrote the Journey to the Center of the Earth (1864), the aim to discover and reach the deepest place below surface has been a challenge to generations of explorers. Nowadays, this is possible in the Arabika massif (Western Caucasus), inside the Krubera-Voronja cave that became in 2001 the deepest cave on Earth. The remarkable record of -2191 (±9) meters deep was possible due to explorations that began in the 1960's and resumed in the last years (Klimchouk et al., 2009).

Despite the large potential of Western Caucasus for caves, one of the largest karst massifs in the World, it has been little explored from a biospeleological point of view, especially the deepest cave systems. The main reasons were the political conflicts in the Caucasian area, combined with the difficulty of biological exploration in such deep and cold systems. Sampling is only possible within organized expeditions during warmer parts of the year.

Included in the West Transcaucasia Ecoregion (Abell et al., 2008: 409), biospeleological reasearch in Caucasus region began in 1929 in the south part, the Koutaia caves, and the first attempt to catalog the Caucasian cave fauna was made by Birstein (1950). After 1965, these studies gained a new impetus in the Western Caucasus, especially in the Alek massif near Sochi and in the Bzybski chain, the two contiguous massifs of Arabika (Gvozdetski et al., 1994). Several interesting cave-dwelling species have been recorded in this area, such as the leech Erpobdella absoloni ratchaensis Kob.; the slug Troglolestes sokolovi Ljovushkin & Matiokin, 1965; the harvestmen of the genus Nemaspela Silhavý, 1966; the endemic millipede genera Leucogeorgia Verhoeff, 1930 and the Archileuco georgia Lohmander, 1939; the monospecific amphipod genus Zenkevitchia Birstein, 1940; the shrimp Troglocaris schmidti fagei Birstein, 1939; and the endemic ground-beetle species of the genera Jeannelius Kurnakov, 1959, Meganophthalmus Kurnakov, 1959 and Duvalius Delarouzee, 1859, among others (Birstein, 1939; Ljovuschkin, 1972; Stoch, 1972; Golovatch, 1985; Belousov, 1991; Belousov et al., 1995; Kryzhanovskij et al., 1995; Chemeris, 2009).

Since the description of the cave salamander Proteus anguinus by Laurenti in 1752, thousands of cave-dwelling animals (troglo- and stygobionts) have been recorded all over the world, except in Antarctica (Culver et al., 2006; Gibert & Culver, 2009). Many speculations about biodiversity patterns and species distributions, and the relationship between cave length and species numbers have been made by scientists in the last years (Culver et al., 2006; Schneider & Culver, 2004; Zagmajster et al., 2008), but the vertical limit of its distribution in function of cave's great depths remain unknown.

Only a few invertebrates have been recorded at great depths, such as the scorpion Alacran tartarus Francke, 1982 and the nicoletiid zygentoman Anelpistina specusprofundis Espinasa & Voung, 2008 which have been collected at -750 and -920 meters in the Huautla Plateau (Oaxaca, Mexico) (Espinasa & Voung, 2008; Prendinia et al., 2010); the springtail Tritomurus veles Lukic, Houssin & Deharveng, 2010 in Croatia found at -430 m (Lukic et al., 2010); and the troglobiotic pseudoescorpion Neobisium (Blothrus) birsteini Lapschoff, 1940 collected in 2009 in the Krubera-Voronja cave (Sánchez-Dehesa & Zarazoga, 2010). But no arthropods had ever been recorded living at a depth of 2000 m below surface (Borgonie et al., 2011).

In the summer of 2010 an Ibero-Russian speleological expedition to Krubera-Voronja cave initiated a biospeleological study in the cave. The results are presented providing the first data of biocoenosis and vertical distribution of invertebrate fauna of the deepest cave on Earth.

MATERIAL AND METHODS

Region of study

Krubera-Voronja cave is located in the Ortobalagan valley, a glaciokarst landscape, within the Arabika Massif, one of the largest limestone massifs of the Western Caucasus in Abkhazia (Fig. 1, 2). This massif, strongly pronounced at elevations ranging between 1900 and 2500 metres, is composed of lower Cretaceous and upper Jurassic limestone (Klimchouk et al., 2009). This cave received its first name Krubera through a dedication to Alexander Kruber, a founder of karst science in Russia, and the latter Voronja (=Crow's cave) due to the presence of crow nests at the cave entrance.

Krubera-Voronja cave is developed in the thickly bedded and massive upper Jurassic limestone. Its entrance is located at 2240 meters above sea level, at 15 km from the Black Sea, through an open-air pit of 60 m deep in the slope of the valley. The cave has two main branches of strictly vertical pits separated by short meanders. At the depth of 1400 meters, in the main branch of the cave, several siphons require cave-diving techniques to reach the actual terminus of the cave, a last siphon at -2140 m that has been dived to a depth of 2191 m below the surface (García- Dils, 2004, 2006; Klimchouk et al., 2009).

The formation of the caves along the Ortobalagan valley was probably originated at 5.96 - 5.33 My in re- sponse to the Messinian salinity crisis, when the Black Sea was almost dry (Klimchouk et al., 2009). Evidence of this is the connection to submarine springs, proved by the use of dye tracing in Kujbyheskaja cave (Klim- chouk, 1990).

Sampling strategy

Field work was conducted in the Krubera-Voronja cave (Fig. 3) (UTM: 43° 24° 35 N, 40° 21° 44 E) until -2140 m deep by the Ibero-Russian CAVEX Team.

The cave was monitored from 27 July 2010 to 24 August 2010, from the base of the first shaft, in total darkness at -60 m, to the deepest part of the cave, the last siphon at -2140 meters.

Sets of pitfall traps (6 cm diameter and 7 cm deep, with a 1 cm diameter tube fixed inside at the centre) were used in the base of the first shafts and in each bivouac (-700 m, -1400 m and -1690 m). Traps were partially filled with 1.2-propanodiol, and Abkhazian cheese was used as bait. Monitoring of pitfalls was supplemented by one hour of active search during the visit to the cave. The stygofauna was sampled by direct collecting of the specimens from the final siphon.

Samples were sorted and specialists in each taxonomic group identified material.

RESULTS

Physical parameters

The temperature of the cave is very constant throughout the year and it was possible to record a vertical gradient in temperature, increasing with depth from 2 °C to 7.5 °C at the final siphon at -2140 meters (Fig. 3), during the sampling period.

The flow of water going down by gravity is constant along the cave, which allows movement of organic matter to the deepest parts of the cave in a short period of time. A small water flow (up to 1 l/s) appears in the cave at a depth of about -340 m, but it disappears in many sections, not varying significantly between the winter when all surface is covered by snow and the snow melting of spring and early summer. The rise in the level of the aquifer by autumn rains or during the spring may flood the cave to a depth of 1600 m, trapping stygofauna from the phreatic levels in the suspended siphons along the cave.

The invertebrate fauna and its vertical distribution

Sixteen species of invertebrates were found living inside Krubera-Voronja cave during the sampling period (Table 1, Fig. 4, 5, 6). Eight species exhibit clear troglomorphic characters such as eye redution or absence and depigmentation. Six of them were classified as troglobionts and two aquatic species as stygobionts (sensu Schiner, 1854 & Racovitza, 1907).

Invertebrate fauna was found from the base of the entrance pit at -60 m up to the last siphon at -2140 m. The deepest troglobiotic species, the recently described springtail Plutomurus ortobalaganensis (Fig. 5A), was found at -1980 m (Jordana et al. 2012), and the deepest stygobiotic species (Troglocaris sp. Fig. 6A and Zenkevitchia sp. Fig. 6B) was found at the depth of -2140 m, and nowhere else in the cave (Fig. 6). The flying dipteran Trichocera maculipennis was the only invertebrate recorded at all depth levels, from the surface down to the deepest unflooded part of the cave. The recently described leiodid beetle Catops cavicis (Fig. 4D) was found in abundance down to -1600 m, which is a remarkable depth for a non-adapted cave animal (Giachino, 2011).

DISCUSSION

Vertical distribution of the fauna

The highest biodiversity (12 species) was found at the bottom of the entrance pit of Krubera-Voronja at a depth of -70 m. Entrance pits can be considered as "ecological traps" due to the higher number of epigean species than of species with clear adaptations to subterranean life (Turquin & Bouvet, 1977). In the case of Krubera-Voronja the bottom of the first pit at -60 m acts like a big pitfall trap for epigean fauna, represented by surface species of Carabus groundbeetles, Gnaphosidae spiders and abundant mites. The "pitfall effect" also provides a microhabitat rich in organic matter, like vegetal detritus and fungi from the surface. This specific border habitat allows the survival of a community of detritivore troglophiles composed by several acari, the springtails Anurida stereoodorata (Fig. 5B), Deuteraphorura kruberaensis and Plutomurus ortobalaganensis, the leiodid beetle Catops cavicis, and the flying dipteran Trichocera maculipennis. This area provides an important food source for detritivorous troglobionts like the large Chordeumatida millipede (Fig. 4E). This also provides a hunting area for four troglobiont predators, the pseudoescorpion Neobisium birsteini (Fig. 4A), the harvestman Nemaspela sp. (Fig. 4B), the groundbeetle Duvalius sp., and also for the troglophilic spider Troglohyphantes sp. (Fig. 4C), the latter only recorded at this depth (Table 1). In the pools, larvae of the dipteran Trichocera maculipennis can be observed in abundance, attesting to the importance of the subterranean environment in the reproductive cycle of this species where available water in the epigean environment is very scarce, as is usual at high altitude on karst massifs.

Several meters after the entrance pit and going down into the cave, the vegetal detritus disappears and the fauna became scarce. Below -70 m the community appears to be supported by the dissolved organic matter (DOM) as occurs in other subterranean environments as well (Culver & Pipan, 2009), by some suspended particles of organic matter including micro-invertebrates and larvae that are carried by the percolating water and mainly by the constant water flow that appears here and there along the cave. Neither the presence of bacterial biofilms nor the concentration of dissolved organic carbon (DOC) was investigated in epikarst water, but it may also provide a source of organic matter for hypogean invertebrates in deep parts of the cave.

Reaching major depths, the most abundant detritivorous animals are Acari, the two troglobiont springtails Schaefferia profundissima and Plutomurus ortobalaganensis, and the troglobiont chordeumatid millipede. The presence of the leiodid Catops cavicis down to -1600 meters is surprisingly deep for a nontroglomorphic beetle, which leads us think that it may be in an early stage of recent colonization of the subterranean environment in this area. The last two species were also recorded during our expedition in contiguous caves around Krubera cave, like in Berschilskaja cave at depths of -3 and - 15 meters. The only predator recorded at great depths in Krubera- Voronja cave was the pseudescorpion Neobisium birsteini. The springtail Schaefferia profundissima was only recorded at -1600m, while other troglobiont species were at different depths (see Table 1; Fig. 7).

The deepest troglobiont found was the springtail Plutomurus ortobalaganensis, recorded at -1980 m, but the deepest terrestrial invertebrate found inside Krubera-Voronja were females of the dipteran Trichocera maculipennis reaching the depth of - 2140 m, unexpected for a flying epigean species. This species is well adapted to cold and its presence in the subterranean ecosystem at high altitudes is well documented in western European caves, and in surface habitats in northern Europe (Matile, 1994; Plachter, 1983). The ecological role of this dipteran is under appreciated in caves, and the presence of this species at -2000m in Krubera-Voronja has been observed in winter (García-Dils, pers. comm)., when the epigean conditions enable their survival in the surface for months. So, their larvae can be carried by hydrochoria through the entire cave, representing an important food source in such deep systems. Species of this family have been observed above -1000m in Berger cave in the Vercors massif, France (Reboleira, pers. obs)..

The troglobiotic fauna of Krubera-Voronja cave appears in areas of abundant air flow. The troglobiont millipede, that was also found in other caves around the Ortobalagan valley at small depths, was found in Krubera-Voronja at -1500m (García-Dils, pers. comm)., in a windy area under a water cascade, probably feeding on the bacterial biofilm of the walls.

The presence of macro-stygofauna is confined to the deepest siphons of the cave at -2140 m, represented by the giant gammarid amphipod Zenkevitchia sp. (~20 mm body size) and by the small shrimp Troglocaris sp. (~5 mm body size). The abundance of both stygobionts and the size of the amphipod suggests that the groundwater of Krubera- Voronja cave is rich in nutrients.

During the rainy seasons of spring and autumn, the cave floods up to -1600 meters depth (García-Dils, pers. comm).. This periodic flood that occurs several times along the year, can trap stygobiont fauna in the suspended pools and siphons (Hüppop, 2000). After succumbing with the decrease of the water level the corpses of this fauna can be a nutrient supply to troglobiont species at major depths in an upwelling effect from the rise of phreatic water (Fig. 3).

BIOGEOGRAPHY OF KRUBERA-VORONJA FAUNA

The community of Krubera-Voronja cave is composed of genera or species groups also known from other subterranean habitats in the Caucasus. Following the ridge of high troglobiont diversity of Europe through Asia, as suggested by Culver et al. (2006), the Caucasian area can be included in the potential subterranean hotspots of the karst regions around the world, argument that can explain the high biodiversity found in Krubera-Voronja cave.

Nemastela harvestmen include troglobiotic species inhabiting caves of Crimea and Caucasus (Chemeris, 2009). Ground-beetles of the genus Duvalius and the pseudescorpion Neobisium birsteini are also recorded from several caves on the Western Caucasus (Harvey, 2011; Kryzhanovskij et al., 1995). Studies on endogean and hypogean carabid beetles from the Caucasus region suggest the penetration of the hypothetical ancestor forms of the endogean beetles from the Boreal Egeida (Jeannel, 1930), while other groups came from the Hyrcanian Provinces and the Toros Mountains, a fauna derived from West Himalayan ancestors (Zamotajlov et al., 2010). The genus of the carabid beetle found on the cave has a wide distribution along the Mediterranean area expanding through Asia (Casale & Laneyrie, 1982).

It is well know the hydrological connection of Arabika massif groundwater with the Black sea (Klimchouk et al., 2009), but the stygobionts from Krubera-Voronja seem to have no relation with a thalassostygobiont ancestor. Recent molecular studies on sytgobiont species of the genus Troglocaris from West-Balkan lineages relate the split between the Caucasian and the Dinaric karst at 6 - 11 My, which allows the supposition of a common freshwater ancestor of cave shrimps during the Paratethys phase, in opposition to the marine relict hypothesis, preciously used to explain this biogeographical relation (Sket & Zaksek, 2009; Zaksek et al., 2010). The amphipod Zenkevitchia is a cave-dwelling endemic genus from the Caucasian caves (Holsinger, 1994).

FINAL REMARKS

The deepest troglobiont documented is the springtail Plutomurus ortobalaganensis, a small detritivorous invertebrate that inhabits Krubera- Voronja cave from -60 m to -1980 m. The amphipod Zenkevitchia sp. and the shrimp Troglocaris sp. are the first stygobiotic invertebrates ever recorded below -2000 meters.

The penetration of non-troglomorphic fauna until -2140 meters deep is remarkable, showing that there is not a direct relation between the degree of troglomorphism and the depth occupied in a cave, which leads new perspectives to the idea that only cave-dwelling fauna have their entire life cycle inside the subterranean environment. So, life in caves should not be seen only as an evolutionary dead end towards the troglomorphic syndrome, as it has been suggested before (Prendinia et al., 2010), but also as a shelter for epigean species populations, especially for long periods of time when surface conditions are severe for their survival, in case of extreme cold or heat.

With the evidence of how deep invertebrate life can be found inside Krubera-Voronja cave, registered until its major depth of 2140 m, several options may explain this fact: 1) food supply carried by water flow along the cave may support macro-invertebrate fauna in the deep parts of karst systems; 2) the presence of non-troglomorphic diptera may be a main support for such invertebrate biocoenosis; 3) some primary, chemolithotrophic production at microbiological level may be contributing to the survival of this biocoenosis in deep parts of subterranean environments. New biospeleological deep explorations will help us to understand the ecosystem of the deep subsurface biota.

ACKNOWLEDGEMENTS

We acknowledge generations of cavers that explored the Arabika massif and to all that contribute to the discovery and exploration of deep caves, which enabled us to undertake this research. We express our gratitude to the CAVEX Team, especially to Sergio García-Dils, Pilar Orche Amaré, Javier Le Pera and Francisco Martínez for their kind cooperation in the biological sampling and to Denis Provalov for providing photographs. We are indebted to the following specialists for the taxonomical identification of invertebrate fauna: Juan A. Zaragoza (Pseudoscorpiones); Carlos Prieto (Opiliones); Damià Jaume (Stygobiotic Crustacea); Rafael Jordana and Enrique Baquero (Collembola); Vicente M. Ortuño (Carabidae); Pier Giachino (Leiodidae); and Jaroslav Stary (Diptera). We are particularly indebted to Pedro Oromí and David C. Culver, for careful reading the manuscript and for kind helpful comments and suggestions. All specimens were collected under the permit of Abkhazia government, included in the CAVEX Team Expedition, from July to August of 2010.

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