Research Article |
Corresponding author: Elena S. Chertoprud ( horsax@yandex.ru ) Academic editor: Rodrigo Lopes Ferreira
© 2021 Rostislav R. Borisov, Elena S. Chertoprud, Dmitry M Palatov, Anna A. Novichkova.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Borisov RR, Chertoprud ES, Palatov DM, Novichkova AA (2021) Variability in macrozoobenthic assemblages along a gradient of environmental conditions in the stream water of karst caves (Lower Shakuranskaya Cave, western Caucasus). Subterranean Biology 39: 107-127. https://doi.org/10.3897/subtbiol.39.65733
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The fauna of the stream water in the Lower Shakuranskaya Cave in central Abkhazia, western Caucasus, was studied. This cave has a large inlet and an extended entrance ecotone area of approximately 60 m, which makes it a convenient area for studying macrozoobenthic assemblages across a gradient of environmental factors. The cave has 13 species of stygobionts, 10 species of stygophiles and 18 species of stygoxenes. The number of species and the abundance and biomass of stygobionts per station were the highest near the boundary of the photic zone, at a distance of 50–60 m from the entrance to the cave, and gradually decreased toward both the remote parts of the cavity and the cave exit. The most abundant stygobionts were gastropod mollusks of the Hydrobiidae family, and Xiphocaridinella shrimp comprised the main part of the biomass. It has been shown that the main environmental factors determining the distribution of macrozoobenthos are luminosity and distance from the entrance to a cave. According to the differences in their reactions to these environmental factors, several groups of species were identified. In addition, three main assemblages of macrozoobenthic species were described: (1) an assemblage of epigean species near the cave entrance area; (2) stygobionts in remote parts of the cave outside the photic zone; and (3) a mixed assemblage in the cave ecotone, where a faint light penetrates. The specific details related to the faunal structure in the ecotone of the cave are discussed, as well as active and passive methods by which stygoxenes invade underground cavities.
Abkhazia, distribution, ecological factors, species richness, stygobionts, stygophiles, stygoxenes
Natural communities are usually not discrete but gradually change each other under the influence of environmental factors (
Caves can serve as a model system for studying community variation along an environmental gradient at a local spatial scale. The entrances of caves are transition zones where epigeic and endogeic organisms can encounter each other. These ecotones are rich in food due to primary producers and accumulated debris from epigeic ecosystems, especially in comparison to the food in deeper parts of the same systems (
The aquatic invertebrate fauna of caves from the western Caucasus is rich (nearly 110 species) and highly taxonomically specific, with endemics accounting for more than 90% of the species (
The work in this study was devoted to analyzing the structure and spatial distribution of macrozoobenthos assemblages in the watercourse of the Lower Shakuranskaya Cave (Abkhazia, western Caucasus). Here, we tested the hypothesis that the macroinvertebrate assemblages in the cave ecotone may significantly differ from the assemblages in the remote parts of the cave, both in terms of species composition and structural dominance. We attempted to identify the main factors determining the penetration of epigeic species into the underground cavities.
The research was carried out in the Lower Shakuranskaya Cave, located in the Gulripshi district of Abkhazia, on the orographically right shore of the Jampal River, 1.5 km south of the village of Amtkel. The configuration of this cave allowed us to conduct research on a 650 m long transect, with a focus on the ecotone zone of the cave. The substrate of the Lower Shakuranskaya Cave consists of Late Cretaceous limestones and belongs to the speleological area of the southern slope (speleological province of the Greater Caucasus) of the Gumishkhinsko-Panavsky speleological district (
A Location of the Lower Shakuranskaya Cave on the map of Abkhazia B sampling stations location scheme in the Lower Shakuranskaya Cave in 2018–2019. In numbers – stations, sampled in February 2018, May and October, 2019; in letters – additional stations, sampled in October, 2019 (for each station indicated numbers of stygobionts, stygophiles and stygoxenes). Views on the cave stream C at station 2 (ecotone zone) D at station 4 E at station 5.
Sampling stations were set in a transect along the stream course in the main cave gallery. The transect had a length of approximately 650 m and included eight stations located from the deepest halls to the entrance area (Fig.
The high heterogeneity of the biotopes and low values of faunal abundance and species richness often make it difficult to carry out ecological studies in caves to a full extent. To compose a complete picture of the structure of species assemblages, quantitative complex samples of hydrobionts were obtained at each station (one complex sample per station). Each complex sample included organisms from three sites 3 m away from each other at a given station. At each station, the samples covered both the areas with the maximum depths and those at the water edge. The main substrate types at the studied stations were stones and clay sand as well as calcified rimstone walls. Collecting aquatic invertebrates was conducted with a hemispherical sampler (diameter 11 cm) with a mesh size of 0.5 mm. The total area of one complex sample at each station was 0.5 m2. All the collected organisms were fixed with 90% ethanol. The species composition, abundance and fresh biomass were determined. The biomass was measured with Acculab ALC-210d4 electronic scales (Germany) with an accuracy of 0.001 mg.
At each station, the main hydrological characteristics of the water inflow (width, depth, water discharge, and type of sediments) and illumination (at midday) were measured (Table
Measurements were obtained by the same person at all stations of a transect. The sampling protocol followed the classic scheme used to study freshwater invertebrates (for example,
The main characteristics of the studied stations in Lower Shakuranskaya Cave. (Temperature and hydrochemical characteristics of water are given for October 2019).
Characteristic | Stations | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
1 | 2 | a | b | c | 3 | 4 | 5 | 6 | 7 | 8 | |
Substrates* | 1 | 1 | 1 | 1 | 1 | 2 | 2 | 2 | 2 | 2 | 2 |
Distance from the cave entrance, m | 0 | 12 | 24 | 36 | 48 | 60 | 280 | 380 | 460 | 520 | 650 |
Illuminance, lx | 555 | 13.17 | 2.70 | 0.07 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Maximum stream depth, m | 0.25 | 0.20 | 0.20 | 0. 03 | 0.30 | 0.40 | 0.50 | 0.40 | 0.30 | 0.50 | 0.3 |
Maximum stream width, m | 1.0 | 1.0 | 1.0 | 1.0 | 2.5 | 3.0 | 3.0 | 3.0 | 3.0 | 5.0 | 4.0 |
Maximum flow rate, m/s | 0.47 | 0.35 | 0.30 | 0.20 | 0.20 | 0.30 | 0.30 | 0.30 | 0.30 | 0.20 | 0.20 |
Temperature, °C (October 2019) | 12.8 | 12.8 | 12.8 | 12.8 | 12.8 | 12.5 | 12.5 | 12.5 | 12.7 | 12.6 | 12.9 |
Mineralization, ppm (October 2019) | 176 | 178 | 175 | 170 | 170 | 188 | 211 | 226 | 250 | 250 | 250 |
pH (October 2019) | 7.7 | 7.8 | 7.8 | 7.8 | 7.8 | 7.9 | 7.9 | 7.8 | 7.85 | 7.9 | 7.7 |
In this research, the term “stygon” is used, which is suggested for aquatic underground communities, and the terms “stygobionts”, “stygophiles”, and “stygoxenes” are used for classifying such organisms (
To evaluate the effects of environmental factors on the community structure, we used distance-based linear modeling (DistLM) and redundancy analysis (RDA). The analysis was performed twice, for the whole massive of data and separately for the data of 2019 year. Our environmental data contained four variables for the whole dataset (year, season, distance, and luminosity), and six additional variables were included for the set of samples collected in 2019 (maximum depth of the stream, maximum width, flow rate, water temperature, total mineralization (total dissolved solids (TDS) and pH). All the available factors were included to each DistLM test. First, marginal tests were performed to determine the effect of each variable on the variation in species assemblage structure. Then, the best-fitting model was selected using the Akaike information criterion (AICc). This criterion is used to select significant factors in a model and take into account sample size by increasing the relative penalty for model complexity with small data sets. Sequential tests are provided for each variable that is added to the model.
A dbRDA (distance-based redundancy analysis) analysis was used to ordinate the fitted values from a given model. Additionally, the original data were analyzed using the MDS (nonmetric multidimensional scaling) factored with luminosity. The analysis was performed in Primer and Permanova+ PRIMER-E, Plymouth, UK (Clarke and Gorley 2001). The ordination of the samples was performed on the basis of the rank matrix of Bray-Curtis similarities.
Regression analysis was performed to indicate the variation in the number of species along the gradient effect of the environmental factors. We used linear regression analysis in Microsoft Excel (Microsoft, Redmond, WA, USA) for the dataset including number of species at each station and four explanatory factors – season, distance, luminosity and year. The Shannon diversity index was calculated for the samples using Excel too. We also applied the constrained ordination technique canonical correspondence analysis (CCA) to determine the impact of the environmental variables on the invertebrate community and show the variations in the species assemblages in accordance with the observed environmental factors in PAST (
In total, 42 species of aquatic invertebrates were found in the stream of the Lower Shakuranskaya Cave in 2018–2019: Turbellaria – 2; Oligochaeta – 4; Hirudinea – 1; Gastropoda – 6; Bivalvia – 1; Amphipoda – 5; Decapoda – 2; Ephemeroptera – 3; Plecoptera – 2; Coleoptera – 5; Trichoptera – 7; and Diptera – 4. Among them, 14 species were categorized as stygobionts, 10 as stygophiles, and 18 as stygoxenes based on the available literature data (Table
Distribution of aquatic invertebrates on the transect stations in the stream of the Lower Shakuranskaya Cave in 2018–2019.
Species | Stations | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
1 | 2 | a† | b† | c† | 3 | 4 | 5 | 6 | 7 | 8 | |
Turbellaria | |||||||||||
2 Dugesia taurocaucasica (Livanov, 1951) | *** | ** | *** | ** | * | * | |||||
3 Dendrocoelum sp. | * | ||||||||||
Oligochaeta | |||||||||||
2 Haplotaxis gordioides (Hartmann, 1821) | * | ||||||||||
2 Rhynchelmis sp. | * | ||||||||||
3 Stylodrilus sp. | *** | ** | *** | *** | ** | * | |||||
2 Eisenia sp. | * | ||||||||||
Hirudinea | |||||||||||
1 Haemopis sanguisuga (Linnaeus, 1758) | * | * | |||||||||
Gastropoda | |||||||||||
2 Tschernomorica caucasica (Starobogatov, 1962) | ** | *** | *** | *** | * | ||||||
3 Caucasogeyeria horatieformis (Starobogatov, 1962) | ** | ** | ** | ** | |||||||
3 Pontohoratia birsteini (Starobogatov, 1962) | *** | ** | *** | *** | *** | *** | *** | ** | * | * | |
3 Caucasopsis schakuranica (Starobogatov, 1962) | * | ** | * | ** | ** | * | |||||
3 Caucasopsis shadini (Starobogatov, 1962) | ** | ||||||||||
3 Caucasopsis sp. | * | * | * | ||||||||
Bivalvia | |||||||||||
3 Euglesa cf. ljovuschkini (Starobogatov, 1962) | ** | ** | ** | ** | |||||||
Amphipoda | |||||||||||
3 Niphargus magnus Birstein, 1940 | * | * | |||||||||
3 Niphargus inermis Birstein, 1940 | ** | * | ** | ** | ** | * | ** | * | ** | * | |
3 Niphargus cf. ablaskiri Birstein, 1940 | * | ||||||||||
3 Zenkevitchia yakovi Sidorov, 2015 | * | ** | ** | ** | ** | ** | ** | ||||
2 Gammarus cf. komareki (Schaferna, 1922) | **** | * | |||||||||
Decapoda | |||||||||||
3 Xiphocaridinella falcirostris Marin, 2020 | * | * | ** | *** | * | ** | |||||
3 Xiphocaridinella osterloffi (Juzbaš’jan, 1941) | * | *** | *** | *** | *** | **** | *** | ** | * | ** | * |
Insecta | |||||||||||
Ephemeroptera | |||||||||||
1 Electrogena zimmermanni (Sowa, 1984) | * | * | |||||||||
1 Baetis (Rhodobaetis) cf. gemellus Eaton, 1885 | **** | ** | * | ||||||||
Leptophlebiidae | |||||||||||
1 Paraleptophlebia werneri Ulmer, 1920 | * | * | |||||||||
Plecoptera | |||||||||||
1 Nemoura martynovia Claasen, 1936 | * | ||||||||||
2 Leuctra sp. | * | * | |||||||||
Coleoptera | |||||||||||
1 Agabus (Gaurodytes) guttatus (Paykull, 1798) | * | ||||||||||
2 Limnius colchicus Delève, 1963 | * | ||||||||||
1 Riolus somcheticus (Kolenati, 1846) | * | ||||||||||
1 Elmis sp. | * | ||||||||||
2 Odeles sp. | * | * | |||||||||
Trichoptera | |||||||||||
1 Tinodes valvatus Martynov, 1913 | * | ||||||||||
2 Plectrocnemia latissima Martynov, 1913 | * | * | |||||||||
1 Chaetopterygella abchazica Martynov, 1916 | * | * | * | ||||||||
1 Stenophylax clavatus (Martynov, 1916) | * | ||||||||||
1 Lithax incanus (Hagen, 1859) | ** | * | |||||||||
1 Ernodes palpatus (Martynov, 1909) | * | ||||||||||
1 Schizopelex cachetica Martynov, 1913 | * | * | ** | ||||||||
Diptera | |||||||||||
1 Macropelopia sp. | * | ||||||||||
1 Parametriocnemus sp. | * | * | |||||||||
1 Cnetha sp. | * | * | |||||||||
1 Dixa submaculata Edwards, 1920 | * | ||||||||||
Total number of species | 15 | 23 | 9 | 11 | 8 | 12 | 11 | 9 | 10 | 8 | 9 |
The highest abundance values (up to 250 ind/m2) were recorded at the stations in the ecotone zone (Fig.
Among the stygophiles, the most abundant were a flatworm (Dugesia taurocaucasica (Livanov, 1951)) (up to 54 ind/m2), snail (Tschernomorica caucasica (Starobogatov, 1962)) (up to 52 ind/m2) and amphipod (Gammarus cf. komareki (Schaferna, 1922)) (up to 52 ind/m2). These species were associated mainly with the slightly illuminated part of the ecotone zone.
Mayfly larvae Baetis cf. gemellus Eaton, 1885 (up to 142 ind/m2), and caddisfly larvae Lithax incanus (Hagen, 1859) (up to 20 ind./m2) were the most numerous among the stygoxenes. These species were recorded in the ecotone part, and their maximum abundance was observed at the most illuminated station 1.
The highest biomass values were recorded in the ecotone zone at stations 2 and 3 (Fig.
Of the four environmental variables we measured for the whole dataset (year, season, distance, and luminosity), the DistLM analysis identified luminosity and distance as explaining the highest amount (31.7% and 29%, respectively) of the variation in species assemblage structure (Table
A significant proportion of the species assemblage variations remains unexplained, which is due to the high heterogeneity of the other environmental conditions in the biotopes studied. By taking into account a greater variety of environmental factors, we attempted to conduct a separate, more detailed analysis for the third sampling event in autumn 2019. For this period of research, some additional data were available. The DistLM analysis showed that of all the factors (season, distance from the cave entrance, illumination, maximum depth of the stream, maximum width, flow rate, water temperature °C, total mineralization TDS ppm and pH), only two, the flow rate and pH, were nonsignificant and therefore eliminated (Fig.
The observed factors affected both the species composition and species richness of organisms in the samples. Using the regression analysis, only the factor of distance was selected as significant (P-value 0.00006). Altogether, 54.4% of the variation in the number of species can be explained by the model. The obtained regression equation predicts a decrease in the number of species by 0.009184 with a one-meter increase in distance; in other words, a 100-meter decrease in the distance from the cave entrance leads to a one-species drop in the number of species.
Variable | AICc | SS(trace) | Pseudo-F | P | Prop. | Cumul. | res.df |
---|---|---|---|---|---|---|---|
MARGINAL TESTS | |||||||
Distance | 16257 | 10.209 | 0.001 | 0.29 | |||
Luminosity | 17783 | 11.612 | 0.001 | 0.317 | |||
Year | 3256.3 | 1.5414 | 0.152 | 0.051 | |||
Season | 2506.7 | 1.17 | 0.301 | 0.045 | |||
SEQUENTIAL TESTS | |||||||
+ Season | 209.51 | 2506.7 | 1.17 | 0.298 | 0.045 | 0.045 | 25 |
+ Distance | 202.74 | 15615 | 9.875 | 0.001 | 0.278 | 0.323 | 24 |
+ Luminosity | 195.43 | 11833 | 10.42 | 0.001 | 0.211 | 0.534 | 23 |
+ Year | 197.19 | 1203.5 | 1.063 | 0.408 | 0.0215 | 0.556 | 22 |
To further illustrate the ordination of the investigated stations according to their species compositions, we used nonmetric MDS, which revealed three groups, i.e., three species assemblages, that were clustered together on the basis of preference for luminosity (Fig.
The CCA plot (Fig.
The two-dimensional nMDS ordination of the investigated cave sites, based on Bray–Curtis similarities (stress = 0.09) and factored with luminosity: 0 – 0 lx, 1 – 0.07–2.7 lx, 2 – 13.17 lx, 3 – 555 lx. Dots are labeled: first number – season/year of research: 1 – winter 2018, 2 – spring 2018, 3 – autumn 2019; second number – no of sampling station.
The CCA ordination of hydrobionts species from Nizhnyaya Shakuranskaya Cave. Black points – stygobionts, blue points – stygophiles, green points – stygoxenes. Abbreviations: A gut – A. guttatus, B gem – B. gemellus, C hor – C. horatieformis, C schak – C. schakuranica, C shad – C. shadini, C sp – Caucasopsis sp., Ch abch – C. abchazica, Cn sp – Cnetha sp., E sp – Elmis sp., D sub – D. submaculata, D tau – D. taurocaucasica, Dend sp – Dendrocoelum sp., E ljov – E. cf. ljovuschkini, Es sp – Eisenia sp., E palp – E. palpatus, E zimm – E. zimmermanni, G kom – G. cf. komareki, H gor – H. gordioides, H sang – H. sanguisuga, L col – L. colchicus, L inc – L. incanus, L sp – Leuctra sp., M sp – Macropelopia sp., N abl – N. cf. ablaskiri, N iner – N. inermis, N magn – N. magnus, N mart – N. martynovia, O sp – Odeles sp., P birst – P. birsteini, P lat – P. latissima, Par sp – Parametriocnemus sp., P wern – P. werneri, R som – R. somcheticus, Rh sp – Rhynchelmis sp., S cach – S. cachetica, S clav – S. clavatus, Sty sp – Stylodrilus sp., T cauc – T. caucasica, T valv – T. valvatus, X falc – X. falcirostris, X ost – X. osterloffi, Z yak – Z. yakovi.
The main characteristics of the three identified species assemblages of macrozoobenthic organisms are presented below:
A total of 14 stygobiont species were found in the Lower Shakuranskaya Cave in 2018–2019, and this number is comparable to the variety of stygophiles (10) and stygoxenes (18). Earlier (in 2012), 14 species of stygobionts were observed in this cave (
The two major groups in the stygobiont assemblage were gastropods belonging to Caucasopsis, Caucasogeyeria, and Pontohoratia (f. Hydrobiidae) and shrimp belonging to Xiphocaridinella (f. Atyidae) (Fig.
Significant changes in the dominance structure and qualitative and quantitative characteristics along the Lower Shakuranskaya Cave gallery occur. Thus, three types of macrozoobenthic assemblages, continually changing each other, were indicated. The ecotone consists of mixing assemblages in which stygoxenes, stygophiles and stygobionts are abundant simultaneously. The abundance and species richness of stygobionts increase from the onset of the ecotone zone, peak at 50–60 m from the cave entrance and decrease further into the cave (Table
The peak abundance in the ecotone may be related to bottom sedimentation and food availability. The bottom in the ecotone zone is covered with rocky soils with a large number of microcavities forming favorable habitats for organisms. In contrast, substrate in deeper parts comprises calcified hump dams and baths without suitable shelters. Some other researches demonstrated positive relationships between environmental heterogeneity and the diversity of aquatic organisms in cave and surface streams (
Apart from the beneficial aspects of the ecotone zone, stygobionts can passively drift out from the cave with water currents. Indeed, stygobionts are occasionally found outside the caves as a result of seasonal floods. For example, Xiphocaridinella shrimp (
It must be noted that the abundance and biomass of stygobionts in our study were not extremely low in the deeper and oligotrophic parts of the studied cave (more than 200 m), where species apparently feed on the microbial community containing heterotrophic and, to a lesser extent, chemoautotrophic bacteria (
Thus, this study confirms the hypothesis about the increase in species richness and abundance of aquatic organisms in the ecotone zone (
The entrance of the Lower Shakuranskaya Cave is large (approximately 70 m2). Adult amphibiotic insects were not found inside the cave, and their larvae usually do not occur further than 60 m deep. Only certain stygoxenes (Haemopis sanguisuga (Linnaeus, 1758), Ernodes palpatus (Martynov, 1909), Schizopelex cachetica Martynov, 1913 and Parametriocnemus sp.) can penetrate through the photic zone. The active penetration of stygophiles and stygoxenes further than the ecotone zone indicates their ability to actively migrate against the flow. Most likely, the intensity of these migrations is determined by the presence of an available food, as in the case of the leech H. sanguisuga (Linnaeus, 1758), which feeds on stygobiont oligochaetes.
The finding of stygoxenic and stygophilic insect larvae at a great distance from the cave entrance may be a consequence of drift (i.e., the movement of benthic organisms with the current). This phenomenon is widespread in watercourses and plays a significant role in the distribution of benthos in mountain regions (
In the context of global climate changes affecting organic matter flows in ecosystems, a significant transformation of cave ecosystems can be expected (
In the Lower Shakuranskaya Cave, 42 species of aquatic invertebrates occurred: 14 – stygobionts, 10 – stygophiles, and 18 – stygoxenes. The species richness and abundance of stygobionts were the greatest near the boundary of the photic zone and gradually decreased both further into the cave cavity and up to the exit from it. In the cave, the distributions of most stygoxenes and stygophilic species were limited to the illuminated ecotone zone. The main factors regulating the spatial distributions of macrozoobenthic organisms were the distance from the cave entrance and the light intensity (illuminance). The greatest species richness and abundance of fauna were noted at stations in the shaded ecotone, where stygobionts, stygophiles and stygoxenes co-occur. The most likely reasons for this scenario are the higher abundance of food resources for aquatic invertebrates, the removal of stygobionts by the water current, and the possibility of faunal epigean elements penetrating the ecotone zone.
The study is supported by the Russian Foundation for Basic Research (RFBR) (grant 20-04-00803_A). This research was performed according to the Development program of the Interdisciplinary Scientific and Educational School of M.V. Lomonosov Moscow State University "The future of the planet and global environmental change".