Corresponding author: Elena S. Chertoprud (
Academic editor: O. Moldovan
The freshwater fauna of nine caves in central Abkhazia, western Caucasus, revealed 35 species of stygobionts, including 15 new species to be described elsewhere. The number of species per station increased from the depth towards the entrance in caves Golova Otapa and Abrskila, becoming the highest in the epigean part. In both caves, two abundance peaks of aquatic invertebrates were registered: one in the entrance area, associated with the development of amphibiotic insect larvae, the other in the depths due to the high numbers of stygobionts. In Cave New Athos, the highest species richness and abundance were observed in large lakes. In caves Golova Otapa and Abrskila, two faunistic complexes with complementary distributions were found, the first due to amphibiotic insects in the cave entrance area, the second one composed of stygobionts in the deep areas. The impact of anthropogenic factors on aquatic cave communities was also noted. The stygobiotic faunas of all caves studied were clearly divided into three groups, following the number of river valleys in which they were situated. The stygobiont faunas of the caves located within one river valley appeared to be 50% similar. In contrast, the fauna composition of the stygobionts from caves situated in different valleys shared not more than 12% species in common. Stygobiotic shrimps and gastropod mollusks show profound local endemism. Stygobiotic
Chertoprud ES, Palatov DM, Borisov RR, Marinskiy VV, Bizin MS, Dbar RS (2016) Distribution and a comparative analysis of the aquatic invertebrate fauna in caves of the western Caucasus. Subterranean Biology 18: 49–70. doi:
Cave biotopes are often inhabited by unique complexes of aquatic species. At least some of these species are completely absent in epigean ecosystems. Such a refugial character of stygobiotic communities is developed in consequence to the constant environmental parameters in subterranean waterbodies which remain stable not only for some years, but also on a geological time scale (
The study of the stygobiotic fauna in the western Caucasus started with the works of
In the recent years, inventorying and cataloguing the subterranean fauna of the western Caucasus, in particular stygobiotic invertebrates, have been carried out (
At the same time, a number of invertebrate groups inhabiting the caves of the western Caucasus remain almost untreated taxonomically. Descriptions of cavernicolous
Not surprisingly, both the ecology and community structure of stygobiotic fauna in the western Caucasus are far from well-known. Investigations which would comprise all taxa of aquatic invertebrates inhabiting individual cave systems are extremely rare. Usually such studies concern both stygo- and troglofaunas, only partially complete though (
Complex studies of cavernicolous species communities are of importance to biodiversity analyses and biogeographical reconstructions, as well as to the ecological monitoring of troglobitic ecosystems. There are some fundamental problems that remain unresolved: first of all, what is the real species richness of a karst massif? How far can different taxonomic groups of stygobionts disperse? Which changes or successions in aquatic communities can be observed with an increasing distance from the entrance? Which is the influence of anthropogenic impacts on those changes? The latter question is extremely topical, allowing for the use data on stygobiotic species as indicators of anthropogenic pressure in touristic caves (
In the current study, an analysis of the freshwater fauna in nine caves of central Abkhazia, western Caucasus is presented. There are three different aims in this study: (1) to provide an inventory of the species richness of freshwater invertebrates; (2) to elucidate the patterns of species distribution within a single cave considering the anthropogenic factor; and (3) to perform a comparative analysis of the stygobiotic faunas inhabiting the different regions of Abkhazia.
Our investigation focused on the Gumishinsko-Panavskiy speleoregion (
Map of the study regions of Abkhazia. Caves:
(1)
(2)
(3)
Tourists mostly visit the New Athos Cave (
In all of the karst caves, quantitative macrobenthos sampling was undertaken. In the long horizontal Abrskila and Golova Otapa caves, the sampling stations were set in transects along the river from the deepest halls to the entrance area. One station was situated above ground not far away from a cave entrance.The transect in Abrskila Cave comprised 11 stations, versus nine in Golova Otapa Cave (Figures
Map of Cave Abrskila. Sampling stations marked by red points (accordingly
Map of Cave Golova Otapa. Sampling stations marked by red points (accordingly
Map of Cave New Athos. Sampling stations marked by red points (accordingly Abhastur 2009).
In Nizhnyaya Shakuranskaya and Srednyaya Shakuranskaya caves, as well as in Tsebel’dinskaya Cave, macrobenthos samples were collected at five stations each. All stations were located along the first 200 meters of the main flooded gallery. In both wells examined and in Simona Kananita Cave, sampling was done in only one station. However, this latter station included all available aquatic habitats.
At all of the stations, the basic hydrological and physical parameters of waterbodies (width, depth, flow rate, type of sediments, silting, and water temperature) were measured. The general characteristics of the collected material are presented in Table
The main characteristics of material from the study caves of Abkhazia, western Caucasus.
Cave/Well | Number of stations | Number of samples (macrobenthos) | Number of taxa |
---|---|---|---|
New Athos | 12 | 36 | 11 |
Simona Kananita | 1 | 3 | 1 |
Nizhnyaya Shakuranskaya | 5 | 15 | 17 |
Srednyaya Shakuranskaya | 5 | 15 | 11 |
Tsebel’dinskaya | 5 | 15 | 14 |
Abrskila | 10 | 30 | 14 |
Golova Otapa | 9 | 27 | 10 |
Uapatyh | 1 | 3 | 5 |
85 m | 1 | 3 | 2 |
Quantitative samples of macrobenthos were taken with a hemispherical scraper with an area of 0.02 m2 and a mesh size of 1 mm. Each sample included organisms pooled from five scrapers collected at a distance of five meters from each other. The sample area was approximately 0.1 m2. Macrobenthos was collected from the samples and preserved in 90% ethanol.
For species identifications, reference material representing most of the invertebrate groups and kept in the Zoological Institute of the Russian Academy of Sciences (St. Petersburg) and the Zoological Museum of the Moscow State University was used. Identification keys are only known for the Caucasian members of the genus
Pairwise similarity of the species composition from different samples in one cave was evaluated using the Czekanowski index (D) for quantitative data (
where Xi, Yi are the proportion of individuals belonging to the each species of all individuals found in samples X and Y, respectively.
To compare the composition of troglobitic faunas, the taxonomic overlap (in %) was calculated between the species lists of different caves. The similarity in faunal composition between the caves was estimated using the Kulczynski index (
where
We applied the multi-dimensional scaling method in PRIMER (version 6) for a graphical presentation of species composition similarity between caves (
In the waterbodies of the study caves, 46 taxa of aquatic invertebrates were found to populate subterranean and epigean habitats. Among them, there are 35 stygobiotic species: four species of
The list of stygobiontic fauna from the examined caves of Abkhazia. (Caves: 1 — New Athos, 2 — Simona Kananita, 3 — Nizhnyaya Shakuranskaya, 4 — Srednyaya Shakuranskaya, 5 — Tsebel’dinskaya, 6 — Abrskila, 7 — Golova Otapa, 8 — Well Uapatyh, 9 — Well 85 m).
Species | Cave | ||||||||
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Gudautsky region | Gulrypshsky region | Ochamchirsky region | |||||||
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | |
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Number of species on the station | 1.6 | 1 | 3.2 | 2.9 | 3.2 | 2.7 | 3.4 | 3 | 3 |
Total number of species | 9 | 1 | 14 | 9 | 11 | 9 | 8 | 3 | 3 |
* — species are still to be described.
The taxonomic status of many stygobiotic groups from the western Caucasus is still questionable. This problem especially applies to
The situation concerning the Caucasian stygobiotic bivalve subgenus
The aquatic faunas of the small caves (Simona Kananita, Uapatyh and the 85 m wells) are poor, and represent taxonomically depauperated derivatives from the faunas of the neighboring larger caves. In this regard, an analysis of the community structure was performed based on he three largest caves, Abrskila, Golova Otapa, and New Athos, that have been studied in detail.
Spatial variations in abundance and species richness of the fauna along the gradient of subterranean environmental conditions. (X-axis: 0 — the cave entrance area, negative values — epigean zone, positive values — cave zone).
A different situation was observed in New Athos that had no natural horizontal gallery with an entrance to the surface. This cavity offered virtually no conditions for studying a gradient of environmental conditions, nor did it allow for an evaluation of the distance variations in species complexes to be made. The samples collected in New Athos were located near the touristic trails and in halls further away making possible the study of the human impact. The highest number of hydrobionts was found in Goluboe, Anatolija and Bezymjannoe lakes, which all lie away from the tourist trails (abundance 100–150 ind/m2; the average number of species per station, 5.5). On the contrary, in waterbodies located near touristic trails, stygobionts were almost absent. Only some of them occurred in the halls with limited access by tourists, where the number of organisms reached 30 ind./m2, the average number of species per station being 2.5.
A.
Individual specimens of stonefly larvae
B.
In Abrskila and Golova Otapa, the density of stygobiotic organisms gradually increased with distance from the entrance. However, the distribution of species was highly heterogeneous along the subterranean part: spots of high abundance are interspersed with areas with few specimens. Local aggregations of stygobionts seem to be in places where water seeps into the cave. The main dominant species is
In New Athos, the complex of stygobiotic fauna is only present in the large lakes, dominated by the shrimp
Successions in the species complexes in the streams of Abrskila and Golova Otapa are shown in Figure
Spatial variations in relative abundance of main invertebrates groups along the gradient of subterranean environmental conditions. (X-axis: 0 — the cave entrance area, negative values — epigean zone, positive values — cave zone).
A comparative analysis of the stygobiotic invertebrate fauna of nine caves from central Abkhazia was conducted. These caves are located in three river valleys. Caves of the Ochamchirsky region (Abrskila, Golova Otapa, Uapatyh and the 85 m wells) are located within the water catchment area of Mokvi River, caves of the Gulrypshsky region (Nizhnyaya Shakuranskaya, Srednyaya Shakuranskaya and Tsebel’dinskaya) in the valley of Kodori River, while caves of the Gudautsky region (New Athos and Simona Kananita) in the valley of Psyrtskha River. The distance between the most separated caves, those from the Gudautsky and Ochamchirsky regions, is approximately 60 km (Figure
Using the Kulczynski similarity index, the stygobiont lists of the investigated caves can be seen as being very different from one another (K = 0.12 ± 0.15). However, when we consider the species lists from caves located within the same river valley and lying not more than 2–3 km apart, their faunas are quite similar (K = 0.77 ± 0.08). This applies to Abrskila, Golova Otapa, and two adjacent wells located in the Mokvi River valley. Another group of similar cave faunas is in both Shakuranskaya and Tsebel’dinskaya. However, the subterranean faunas of neighboring river valleys lying at a distance of several dozen kilometers show no more than 12% of shared species from the total list, for example the species complexes of the Gulrypshsky and Ochamchirsky regions. A comparative analysis of the species lists based on the Kulczynski index demonstrates a clear separation of the faunas into three groups, each corresponding to its own river valley (Figure
Two-dimensional ordination with superimposed clusters of the stygobiotic faunas from different caves, based on Kulszinski similarity index. River valleys are shown by different colors. Caves:
Estimating the distribution of the main taxonomic stygobiont groups shows that species of cavernicolous shrimps, gastropods, turbellarians, and oligochaetes are highly local in range (Table
In our material, all main groups of the Caucasian stygobionts were found, except
At present, information on the taxonomic composition of the western Caucasian stygobiotic fauna is far from complete. New research in even readily accessible and regularly visited caves alone is deemed to inevitably increase the list of cavernicolous taxa. In the western Caucasus, biological studies have hitherto been carried out in at least 200 caves (
The stygobiotic fauna of the Abkhazian study caves showed very high abundance rates, as a rule. This is especially clearly visible in large flooded cave systems.. However, in many caves of the Balkan Peninsula (
Besides this, the community structure significantly depended of the hydrological type of water bodies and heterogeneity in aquatic habitats. Species richness is also higher in the caves with streams and rivers in comparison with those with stagnant ponds (
In the entrance areas of Abrskila and Golova Otapa caves, stygobionts were fully replaced by epigean species. In Cave Abrskila Cave, apparently due to artificial light, larvae of epigean
In New Athos Cave, the anthropogenic influence was remarkable near the walking trails, especially close to basins. Many of coins left behind by tourists could change the hydrochemical composition of water. On the other hand, cleaning up the speleothems from microalgae growing in the lighted places led to intrusions of cleansers into rimstone pools and puddles. This may be the reason of macrofauna was virtually absent from all basins near the touristic trails.
A number of methods for the assessment of anthropogenic pressure have been developed for marine or freshwater ecosystems, but these are not applicable to subterranean waters. The first criterion of a cave community disturbance is reduction of troglobiont abundance (
Amphipods are often considered to be wider distributed across the karst regions than other stygobiotic taxa (
Further biospeleological investigations are necessary to reveal more detailed patterns in the distribution and diversity of the stygobiotic fauna of the western Caucasus. More research will almost certainly extend the ranges of some species. On the other hand, molecular analysis may help in detecting additional taxa with restricted distributions. Estimating the real species richness and ecological preferences of stygobionts may lay the grounds for tracing consistent patterns of cave fauna formation in the region.
An analysis of the stygobiotic fauna from nine caves of central Abkhazia, western Caucasus, provides the following ecological observations:
(1) In the studied caves were found 35 species of stygobionts:
(2) In the subterranean rivers of Abrskila and Golova Otapa caves, the species richness and faunal diversity was revealed as increasing from the most remote stations inside the caves to the entrance areas, reaching the highest values in the epigean area. In both caves, two abundance peaks of aquatic invertebrates were registered: one in the entrance area, associated with the development of amphibiotic insect larvae, the other one in the depth of the caves due to the high numbers of stygobionts. In Cave New Athos, the highest species richness and fauna abundance were observed in large lakes.
(3) In caves Abrskila and Golova Otapa, two ecofaunistic complexes with complementary distributions were revealed. The first is a complex of amphibiotic insects in the cave entrance area, the second a complex of stygobionts in the remote parts of the caves. In Cave New Athos, which is devoid of a entrance area, only a stygobiotic faunistic complex was found.
(4) The most significant anthropogenic impact on stygobionts was observed in Cave New Athos, where almost all waterbodies located near the excursion trails were devoid of a macrofauna. Hydrobionts mostly inhabited large lakes which were distant from the touristic routes. Both artificial illumination and extraneous material brought inside from the surface are the anthropogenic impacts that help epigean amphibiotic insect larvae colonize the subterranean habitats.
(5) The stygobiotic faunas of the study karst caves are clearly divided into three groups, according to the number of river valleys in which they are located. The fauna compositions of the stygobionts from caves situated within one river valley are similar to no less than 50%. The compositions of the stygobionts from caves located in neighboring valleys (30 to 60 km apart) contain not more than 12% of shared species.
(6) In the stygobiotic shrimps and
The studies were supported by the program “Scientific bases for the creation of a national depository bank of living systems” of the Russian Science Foundation № 14-50-00029, and by the Russian Foundation for Basic Research [Project № 15-54-40011_Abh-a]. We are also obliged to Sergei Golovatch (Moscow) for editing the English of an advanced draft, and to the two anonymous reviewers for the suggestions that improved the manuscript scientific content.
Here, the term “troglobionts” means subterranean animals