CC BY
20Трансформация экосистем Ecosystem Transformation www.ecosysttrans.com
Stygobiotic faunal elements in spring assemblages of West Transcaucasia
Dmitriy M. Palatov1' 2*, Agniya M. Sokolova2' 3
1 M.V. Lomonosov Moscow State University, Leninskie Gory 1/12, Moscow, 119234 Russia
2 A.N. Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences,
Leninsky prospect 33 Moscow, 117071 Russia
3 N.K. Koltsov Institute of Developmental Biology, Russian Academy of Sciences,
Ulitza Vavilova 26, Moscow, 119334 Russia
*triops@yandex.ru
Received: 28.01.2018 Accepted: 06.03.2018 Published online: 30.01.2019
DOI: 10.23859/estr-180128 УДК 574.587 (1-924.7)
URL: http://www.ecosysttrans.com/ publikatsii/detail_page.php?ID=95
ISSN 2619-094X Print ISSN 2619-0931 Online
Translated by D.D. Pavlov
Macroinvertebrates of stygobiotic origin contributing to benthic assemblages in springs of the two regions of West Transcaucasia were investigated. The regions concerned, basins of the Khosta-Kudeps-ta Rivers (Krasnodarskiy krai) and Myussera Upland (Abkhazia), are well-studied and drastically different in a number of features. Frequency of occurrence, abundance and the position of stygobiotic species in the structure of crenal assemblages are given. Stygobi-onts dominated in 50% of cases, more often in helocrenes with variable runoff than in rheocrenes stably connected with watercourses. Stygo- and crenobiotic primary aquatic invertebrates (crustaceans and mollusks) demonstrate pronounced local endemism at the species level. Under certain circumstances spring assemblages can be considered as island ones.
Keywords: zoobenthos, crenal zone, rheocrenes, helocrenes, local endemism, Belgrandiella, Niphargus.
Palatov, D.M., Sokolova, A.M., 2019. Stygobiotic faunal elements in spring assemblages of West Transcaucasia. Ecosystem Transformation 2 (1), 35-43.
Introduction
Assemblages of spring waterbodies are often built up by faunistic elements of different ecological origin. They can include oxyphilic and rheophilic groups characteristic for small rivers and brooks; ubiquitous species, characteristic for small waterbodies of any type; typical inhabitants of temporary pools; obligate crenobionts, etc. (Chertoprud, 2006). Species of stygobiotic origin carried into spring waterbodies from ground waters and possessing corresponding morphological features and adaptations (depigmentation, characteristic disproportionality of the body, etc.) are a particular group of crenal organisms. Mass introductions of stygobionts into spring assemblages usually occur in regions that have not been subject to surface glaciation in recent geological past (Chertoprud and Peskov, 2007).
West Transcaucasia is one of such areas and the discussed groups is represented by crustaceans: amphipods of Anopogammarus (Gammaridae) and Niphargus (Niphargidae) genera, single species of Synurella (Crangonictidae), isopods Proasellus as well as gastropods Belgrandiellinae (Hydrobiidae), some oligochaetes (Stylodrilus, Rhyacodrillinae) and turbellaria (Dendrocoelopsis) (Turbanov et al., 2016). Stygomorphic species become dominant over specialized complexes of crenobiont amphibiotic insects in a number of spring assemblages. In this case, it is proposed to call the resulting associations troglocrenal (Chertoprud, 2010, 2011). They are known from the studied territory but described only generally (Chertoprud, 2010).
Aim of the present work was to describe composition and occurrence of stygobiotic complex
of species in crenal assemblages from two large spring areas - the Khost and Kudepsta river basins (Krasnodar region, Russia) and the Myusser (Kavakluk) upland basins (Gudauta district, Abkhazia) in the Western Transcaucasia.
Material and methods
A total of 55 quantitative samples of macrobenthos collected in spring waterbodies on the territory of West Transcaucasia in 2008-2014 were studied: 27 samples taken in the Malaya and Bolshaya Khosta basins; 15 samples from Kudepsta basin; 13 samples from the territory of Myusser upland within the Pitsunda-Myusser reserve.
Samples were taken from all types of springs (rheocrenes, limnocrenes, helocrenes) from all available microbiotopes using a hydrobiological scraper (area 0.02 m2, 0.25-1 mm mesh size) or (when sampling from waterbodies with maximum depth of several millimeters) by total collection of organisms from the substrate (stones, wet rocks, leaf litter). Sampling area was 0.1 m2, usually. Animals were taken immediately from the scraper where bottom substrate was filtered and flushed. Samples were fixated immediately after collection with 70% ethanol.
Organisms were identified using literature containing first descriptions of species and identification keys for studied stygobiont groups (Birshtein, 1936, 1952; Martynov, 1932; Starobogatov, 1962). Mollusk preparations were done with acupuncture needles under dissecting microscope Carton TRIO 0750. Temporary glycerin preparations were used during analysis of diagnostically important structures of appendages (antennae, gnatopods, pereopods, pleopods, telson, uropods, etc.) of identified arthropods. Clarification of the integument was achieved by keeping studied objects in lactic acid solution. Preparations were studied using Olympus CX21 light microscope.
Metabolism value calculated according to the following formula (Kucheruk and Savilova, 1985): D=k-N°25-B075,
where D - metabolism value, ml 02/m2; N -abundance of organisms, ind./m2; B - their biomass, g; k - coefficient, specific for each group of invertebrates, was chosen as the main measure of taxon’s abundance when studying assemblage structure. We used values of k given in Alimov (1979). The intensity of metabolism is proportional to the rate of nutrition and respiration of the organism being a more adequate reflection of its role in the assemblage comparing with abundance and biomass. Since the metabolic rate of small animals is higher than that of large ones, metabolic rate increases more slowly than biomass with increasing body size.
Crenal assemblages were compared mainly using relative abundance - the share of each species in the total metabolism of the assemblage. Absolute values (total metabolism and community biomass) were also compared, but were of minor importance.
The structural hierarchy of communities was described on the basis of Ulfstrand classification (1968), developed for amphibiotic insects. The dominant species should be at least 25% of the total assemblage, subdominants - at least 10%. If the proportion of a particular taxon in the total metabolism of an assemblage was 75 percent or more, such a taxon was called superdominant.
Physical-geographic and geological features of studied areas
Choice of the study area was conditioned due to the following features. Despite their close geographical location, they differ significantly in a number of geological and hydrological characteristics (Fig. 1). The neighboring basins of the Khosta and Kudepsta rivers are located within a single biospeleological area (Birshtein and Levushkin, 1967), their valleys are washed in thick layers of limestone rocks rich in various karstic cavities, including large flooded caves. Large limestone massifs - Alec (headwaters of Malaya and Bolshaya Khosta), Vorontsovskiy (upper Kudepsta), Akhunsky (between the Khosta and Matsesta), and others (Dublyansky et al., 1985) are located here. In such conditions, spring water bodies are often directly connected with underground reservoirs, from where leaching of stigobionts occurs fairly regularly. A number of narrowly localized stygobiont endemics were described from both cave and spring reservoirs of the region (Birshtein, 1952, 1967; Martynov, 1932).
A completely different situation is observed within the Myusser Upland. In the geological sense, it is a peculiar island, separated from the southern slopes of the Bzyb and Gagra Ridges of the Greater Caucasus by a wide hollow - the Kaldkhvar corridor. The low-mountainous hilly-ridge relief with heights not exceeding 250-270 m, composed of conglomerate rocks (Bebiya et al., 1987), is characteristic. There are completely no karst relief forms (caves, craters, etc.), spring water bodies have no direct connection with groundwater. No stigobiont forms were previously known directly from the territory of the Myusser Upland.
Thus, a comparison of the crenobiont fauna (in this case, its stygobiont component) of these geologically different, but geographically close areas is of interest in the context of studying springs as island habitats, identifying potential abilities of crenal and stygobiont forms for settlement and local speciation.
Figure 1. Map of the studied area. Roman numerals denote surveyed regions: I - Khosta and Kudepsta basins; II - Myusser Upland basin.
Results
Stygobiont invertebrates in spring assemblages: species composition and occurrence
Eight species possessing stygomorphic features linked with groundwater one way or another were found in the springs of the surveyed territory. Six species were found in springs of Khosta and Kudepsta river basins, four - in springs of Myusser Upland. Quantitative parameters of their occurrence in crenal assemblages of studied regions are given in Table 1. Khosta and Kudepsta basins
Six species were found in this area: two species of gastropod mollusks Belgrandiellinae, three species of Niphargus amphipods and one species of Proasellus isopods.
• Belgrandiella caucasica Starobogatov, 1962 (Mollusca: Gastropoda: Hydrobiidae)
A species of small (shell height 1-1.5 mm) gastropods typical for spring and cave waterbodies of West Caucasus at least on the territory from Tuapse to Psou. Described from Krasnoaleksandrovskaya cave watercourse, we have also found it in Dolgaya cave and in a number of springs in the vicinity of Tuapse and Lazarevskoye (Palatov and Vinarski, 2015; Sokolova and Palatov, 2015). It is quite common (found in 52% of samples) in the spring waterbodies of the Khosta and Kudepsta basins. It is evenly spread throughout the study area - from low-
mountain springs in the suburbs of the city of Khosta to springs in the headwaters of the main rivers of the region at absolute altitudes of 800-900 m. The species is quite eurybiotic, inhabiting waterbodies of various types from rheocrenes and underflow streams of mountain rivers (for instance found in the hyporhea of Mal. Khosta River) to helocrenes and barely noticeable seepages on the slopes of the valleys. Forms mass aggregations (up to 90 ind. per sample) on leaf litter and woody substrates. Despite such a large abundance, the role of this species in the total metabolism of assemblages is small (due to extremely small individual biomass) and averages 3-4%, in some cases up to 9% of the indices of community’s total metabolism.
The species has significant conchological and anatomical variability. Previously considered populations were described as a separate species B. nemethi Schutt, 1993. However, we could not find stable differences when comparing topotypical materials of these two species (Fig. 2A, C, D), therefore B. nemethi is considered a junior synonym for B. caucasica in this work.
• “Paladilhiopsis” sp. (Mollusca: Gastropoda: Hydrobiidae)
Not being able to study the genital system of the male of this species (only females are present in the samples), we refrain from confidently determining its genus and species. Conchologically, it is close to Paladilhiopsis orientalis Starobogatov, 1962 (Fig. 2B)
Table 1. Data on the occurrence, density, and the average share according to metabolism for stygobiont species found in the composition of spring assemblages of studied regions.
Species Occurrence, % Average density, Occurrence, % ind. per sample Average share in assemblages according to metabolism, %
Khosta and Kudepsta basins
Belgrandiella caucasica 52 19.4 3.5
«Paladilhiopsis» sp. 21 6.3 0.7
Proasellus cf. infirmus 38 13.7 13.5
Niphargus abchasicus 48 20.7 45
Niphargus cf. pseudolatimanus 31 3.9 20.3
Niphargus cf. gurjanovae 1 6 13.4
Myusser Upland basin
Belgrandiella sp. 54 27.2 3
Proasellus cf. infirmus 31 1.5 2.8
Niphargus derzhavini 62 41.4 42.3
Niphargus cf. gurjanovae 15 5.5 2.4
described from Krasnoaleksandrovskaya cave. The species is relatively rare in spring waterbodies of the studied area, its occurrence is 21%. It also does not form dense aggregations, usually there are 3-4 individuals per sample, the maximum is 27 individuals in one sample (a spring in the valley of the Kudepsta river under Krasnaya Volya village). The share in the total metabolism of the assemblage, is usually below one percent, in the only case it reached 5%. The species is distributed sporadically, most often found in the springs of the middle course of the Khosta and Kudepsta rivers at an altitude of 150-200 m.
In the Transcaucasia, representatives of “Paladilhiopsis" genus are mainly found in cave habitats being rare in springs. Probably, all these findings are exclusively due to the occasional flushing of mollusks from the hyporheic streams. In the Khosta and Kudepsta basins “Paladilhiopsis" sp. was met mainly in powerful rheocrenes with a stable water discharge. Not found in helocrenes.
• Proasellus cf. infirmus (Birstein, 1936) (Crustacea: Isopoda: Asellidae)
Found individuals of Proasellus are morphologically close to Proasellus infirmus (Birstein, 1936) described from the springs of the Gumista valley (Central Abkhazia); we did not find any significant differences. However, for confident identification of the species, it is necessary to compare our specimens with type specimens of P. infirmus. As in the case with typical P infirmus, the found populations are difficult to attribute to real stygobionts - animals are pigmented (obviously weaker than epigean Asellus) and have partially reduced eyes. Most likely, they are obligate crenobionts, occasionally penetrating into groundwater.
Occurrence of Proasellus cf. infirmus in the springs of the Khosta and Kudepsta basins is 38%.
In about half of the cases, these crustaceans are among the dominating species complex within the assemblages, accounting for 15-25% of its total metabolism, but never becoming super dominants, that are able to suppress the accompanying amphipod species from Niphargus and Gammarus genera, completely. The highest density was recorded in the springs of the middle current of Malaya Khosta -up to 45 individuals per sample. Points of detection P. cf. infirmus in the study area are usually observed in the lower and middle currents of the main rivers, to the absolute altitude of 300 m. The species does not occur in the springs of the upper stream, in the springs on the ridges and the main large caves. It inhabits both in stable rheocrenes and helocrenal seeps.
• Niphargus abchasicus Martynov, 1932 (Crustacea: Amphipoda: Niphargidae)
The most widespread species of Niphargus in the study area, which was described from the local spring waterbodies and found here later (Levushkin, 1963). The occurrence is 48%, while in most cases the species dominates in the assemblages, accounting for 23-67% of the total abundance of metabolism. At the same time, N. abchasicus is unevenly distributed over the studied territory: mass finds are associated with the coastal low-mountain zone (including the city of Khosta). The occurrence decreases when moving northwards, to the headwaters of the rivers and the Alec ridge. The species almost never occurs in the spring sources of Bolshaya and Malaya Khosta and Kudepsta rivers, being replaced by N. cf. pseudolatimanus Birstein, 1952.
Observed populations correspond exactly to the diagnosis given by Martynov (1932), later updated by Derzhavin (1945) and Birshtein (1952) in terms of morphology. Nevertheless, some individuals
differ possessing a larger number (3-4) of thorns on dactyles of pereopods III - VII, which quite fits into the norms of individual variability.
• Niphargus cf. pseudolatimanus Birstein, 1952 (Crustacea: Amphipoda: Niphargidae)
The species (possibly a group of species) is morphologically close to N. latimanus Birstein, 1952 and N. pseudolatimanus Birstein, 1952 described from the upper Kudepsta caves. In general, combined morphological features of spring populations have an intermediate character between these two species, somewhat approaching N. pseudolatimanus. But here, too, the differences are manifested in a different form of the gnatopod, smaller number of segments in antenna II and in other, mostly quantitative, features. Morphologically close populations are widespread in the West Transcaucasia - from the Khosta and Kudepsta basins to the vicinity of Tuapse and Novorossiysk (Sokolova and Chambers, 2015).
In the springs of the Khosta and Kudepsta basins, the species is found in 31% of the springs on average, often together with N. abchasicus, yielding to it in numbers everywhere. We did not find it in the springs of the low-mountainous seaside coastal strip: the species is mostly found in the middle and upper courses of region’s main rivers (especially common in the springs of Vorontsovka village). There were springs in the upper Khosta and Kudepsta where it made up 100% of the population (up to 25 individuals per sample). In all other cases, the species was not prone to superdominance, never accounting for more than 20% of the total metabolism of the assemblage, and even less in the presence of N. abchasicus.
• Niphargus cf. gurjanovae Birstein, 1941 (Crustacea: Amphipoda: Niphargidae)
A species morphologically close to N. gurjanovae Birstein, 1941, known from the springs of Western Georgia. The latter is described only from females and not in great detail, which makes it difficult to identify individuals found reliably. We also had only females in the number of several specimens.
The species is rare in the surveyed area. Found only in four springs, three of which are located in close proximity to each other, in the upper reaches of Kudepsta river. Only in one case did the species demonstrate subdominance, accounting for 38% of the total abundance of the assemblage. In other cases, this index was at the level of 5-10%.
Thus, the springs of the Khosta and Kudepsta basins are inhabited by six species of invertebrates associated with groundwaters by their origin. Each of these species is found in all three main valleys of the region: the Kudepsta valley, Bolshaya and Malaya Khosta, but the frequency of occurrence of most species depends on the height above sea level and/or distance from the coast. In total, species of stygobiont origin dominate in the assemblages of 55% of springs. These are predominantly helocrenes
and rheocrenes, with an unstable connection to a larger watercourse (river or stream). Representatives of the fairly eurybiont genus Gammarus (Amphipoda) dominate in 21% of springs. Most often, these are springs having a permanent connection with a larger watercourse. Amphibiotic insects form dominant complexes in 24% of cases. Usually, in springs lacking amphipods and isopods for some reason. Myusser Upland basin
Four species have been found here: one species of gastropod mollusks of genus Belgrandiella, two species of Niphargus amphipods, one species of Proasellus isopod.
• Belgrandiella sp. (Gastropoda: Hydrobiidae)
This species is almost identical to B. caucasica
(Fig. 2F) in terms of conchological parameters yet stably differs from the latter by at least the structure of the male reproductive system. The penis is characterized by the reduction of the lateral process typical for genus Belgrandiella as a whole (Fig. 2E), as well as the wider main lobe (Fig. 2G). This observation is based on the dissections of ten males.
Belgrandiella sp. was found in 54% of the surveyed springs in the Myusser Upland territory. As in the case of B. caucasica, this species often reached high density (up to 93 individuals per sample), but did not play a significant role in the assemblages. On average, the share of the species in the total abundance of the assemblage in metabolism was 1-4%, and up to 15% in single springs.
Belgrandiella sp. occurs in springs all over Mysra and Riapshi rivers and in the valleys of the small coastal streams of the Myusser Upland. Not found in the adjacent areas of the Bzyp lowland. Perhaps an endemic of the Myusser Upland.
• Proasellus cf. infirmus (Birstein, 1936) (Crustacea: Isopoda: Asellidae)
Morphologically identical to the populations from the Khosta and Kudepsta basins. In the springs of the Myusser Upland is less common - found in 31% of waterbodies. At the same time, almost all findings were single, the maximum was two individuals per sample. Therefore, this species does not play a significant role in the spring assemblages of the region, reaching only a few percent of the total abundance based on metabolism.
• Niphargus derzhavini Birstein, 1952 (Crustacea: Amphipoda: Niphargidae)
The most common Niphargus species in the area. Described from springs near the Olginsky grotto, in the vicinity of Adzapsh village (Otradnoye) and the town of Gagra, “Transfer” of the typical habitat of this type into the vicinity Olginskoye village, Gulripsh district of Abkhazia (Sidorov, 2014) was clearly erroneous - there are no morphologically close forms in the specified area. On the contrary, completely identical animals live in the vicinity of Gagra.
Figure 2. Belgrandiellinae from the springs of West Transcaucasia: A - shells of Belgrandiella caucasica Starobogatov, 1962, springs near the Krasnoaleksandrovskaya cave, Lazarevsky district of the city district of Sochi, Krasnodar Region, N 44°0'36.03”, E 39°21'11.72”, collected on 01.05.2015; B - shells of “Paladilhiopsis” sp., a spring in the valley of Kudepsta river, near the village of Krasnaya Volya, Khostinsky district of the Sochi city district of the Krasnodar Region, N 43°33'44.99 ", E 39°55'58.69”, 23.02. 2009; C - shell of B. caucasica Starobogatov, 1962, spring in the valley of Malaya Khosta river, at the intersection with the road to Khleborob village, Khostinsky district of Sochi City District of the Krasnodar Region, N 43°34.871', E 39°52.428', 04.25.2015; D - shell of B. nemethi SchQtt, 1993, spring seepage on the right bank of Khosta river, near SNT "Rassvet”, Khleborob sett., Khostinsky district of Sochi City District of Krasnodar Region, N 43°33'0.62”, E 39°53'3.44”, 15.04.2008; E - penis of B. caucasica Starobogatov, 1962, a spring in the valley of Malaya Khosta river, at the intersection with the road to Khleborob village, Khostinsky district of the Sochi City district of the Krasnodar Region, N 43°34.871”, E 39°52.428', 04.25.2015, side and bottom view, arrow shows a characteristic lateral process; F - shell of Belgrandiella sp., a spring on the right bank of Myussera (Mysra) river, at the mouth of the first large tributary on the left, Gudauta District, Republic of Abkhazia, N 43°11'52.30”, E 40°27'0.03”, 02.19.2010; G - penises Belgrandiella sp., a spring on the right bank of the river Myussera (Mysra), at the mouth of the first large tributary on the left, Gudauta district, Republic of Abkhazia, N 43°11'52.30 ", E 40°27'0.03”, 02.19.2010, side and bottom views, arrow shows the absence of lateral process characteristic for B. caucasica. The scale segment corresponds to: A, C, D, F - 300 |jm; B - 500 |jm; E, G - 200 |jm.
The occurrence of N. derzhavini is 62% in the springs of the region. In most cases, the species dominates in the assemblages, averaging 40-45% of the total abundance of the assemblage’s metabolism. In several cases, this figure exceeded 80%. The species also forms fairly dense aggregations - from 40 to 80 individuals per sample. On the territory of the Myusser Upland, the species is widespread everywhere, in the helo- and rheocrenes, also penetrating into some springs of Lake Inkit floodplain and Bzyp plain.
• Niphargus cf. gurjanovae Birstein, 1941 (Crustacea: Amphipoda: Niphargidae)
The species is morphologically identical to the populations found in the spring reservoirs of the Khosta and Kudepsta basins. Its occurrence is relatively low in the basin of the Myusser Upland, constituting 15%. The density of populations is also small: 1-5, up to 10 individuals per sample. This species is not represented in the complex of dominants, reaching a maximum of 5% of the total metabolism of the assemblage.
Thus, the springs of the Myusser upland are inhabited by four species of invertebrates associated with groundwaters by their origin. Most of them are tied to large valleys of the upland: the valley of Mysra and Riapshi rivers, as well as the valleys of coastal streams. Only the most common stygobiont, N. derzhavini, is encountered in the adjacent territories of the Bzyp plain and the floodplain of Lake Inkit.
In total, species of stygobiont origin dominate in the assemblages of 52% of springs of the Myusser Upland. Genus Gammarus amphipods dominate in 39% of springs, complexes of crenobiont amphibiotic insects in 9% of springs.
It has long been noticed that all variants of spring assemblages can be divided into two groups: one dominated by complexes of crenal insects and the other dominated by non-insects, i.e. crustaceans and mollusks (Barqurn and Death, 2006; Gray, 2005). The group of assemblages dominated by crustaceans dominates in the springs of the Western Transcaucasia, 80% versus 20%. The dominance of crustaceans of stygobiont origin is observed in 55% of cases.
Some zoogeographic patterns
Ranges of crenobiont forms are almost always larger than the ranges of typical stygobionts living in underground cavities. Many species, for example, the Caucasian Niphargus or Troglocaris are known only from one particular cave or a complex of communicating caves (Birshtein and Levushkin, 1967). Obviously, the ranges of stygobionts, which spread to the springs, are somewhat wider, but they are still inferior to real epigean forms. Thus, the range of N. abchasicus, as far as we know at the moment, includes only the territory squeezed between the sections of the lower reaches of Sochi and Mzymta rivers. An obviously related
species, N. derzhavini inhabits the spring waters of the Gagra - Mysra section and, possibly, parts of the Gudauta plain. Further to the south-east, starting from Novyi Afon and at least to the Gumista river valley, spring water bodies are mostly inhabited by N. iniochus Birstein, 1941 (unpublished data), which was described from a creek of the cave entrance zone near the Andreyevka village (Akhalsheniya). The species of crenal gastropods and a number of other groups probably follow along the Black Sea coastline in a similar fashion. Separate endemic faunistic complexes of stygo- and crenobionts can be located on a very small area - 20-30 km2. In particular, a similar effect has been repeatedly described for stygobiont fauna of the Balkan Peninsula (Georgiev and Hubenov, 2013; Sket, 1999). Thus, the spring areas of West Transcaucasia do indeed exhibit a certain island effect, remaining largely isolated from each other in the faunistic sense, at least at the level of non-flight primary aquatic organisms.
Conclusions
1. Stygobiont elements West Transcaucasia spring assemblages’ fauna are mainly represented by crustaceans (Amphipoda and Isopoda) from Niphargus and Proasellus genera, as well as by specific gastropods of the Belgrandiellinae subfamily.
2. Stygobionts dominate in spring communities in about 50% of cases. Typically, the dominants are amphipods of genus Niphargus.
3. More often stygobionts dominate in helocrenes with a variable volume of flow, compared to rheocrenes, which are stably connected with watercourses. Epigean species of Gammarus are usually the dominant group in rheocrenes.
4. Stygo- and crenobiont primary aquatic invertebrates (crustaceans and mollusks) exhibit local species endemism. In general, spring communities can be considered as island communities under certain conditions.
Acknowledgments
The authors are grateful to R.A. Rakitov (PIN RAS) for the opportunity to work on a scanning electron microscope. Some of the photographs used in the work were taken by the authors on the equipment of the Collective Center of M.V. Lomonosov Moscow State University with financial support from the Ministry of Education and Science of the Russian Federation.
References
Alimov, A.F., 1979. Intensivnost’ obmena u vodnykh poikilotermnykh zhivotnykh [Metabolism intensity in aquatic poikilotherms]. Obshchie osnovy izucheniya vodnykh ekosistem [General Principles of the Study of Aquatic Ecosystems]. Nauka, Leningrad, USSR, 5-20. (In Russian).
Barqurn, J., Death, R.G., 2006. Spatial patterns of macroinvertebrate diversity in New Zealand springbrooks and rhithral streams. Journal of the North American Benthological Society 25, 768-786.
Bebia, S.M., Kolakovsky, A.A., Yabrova-
Kolkavskaya, V.S., Adzimba, Z.I., Shengelia, E.M., Dolukhanov, A.G., Urushadze, T.F., Rusanov, A.B., Shalabashvili, G.K., Kitsmareyshvili, L.S.,
Puchkina, E.E., Tarasov, A.I., Tugushi, K.N., Balabanov, I.P., Bondurovsky, G.M.,
Povolotskaya, V.S., Kvirkelia, B.D., Kakulia, G.A., Berdzenishvili, M.G., Tuniev, B.S., 1987. Pitsundo-Mussersky Zapovednik [Pitsundo-Mussersky Reserve]. Agropromizdat, Moscow, Russia, 190 p. (In Russian).
Birstein, J.A., 1936. O vodyanykh oslikakh Kavkaza [On the Water Lice of the Caucasus]. Sbornik Trudov Zoologicheskogo Muzeya MGU [Proceedings of the Zoological Museum of the Moscow State University] 3, 235-242. (In Russian).
Birstein, J.A., 1952. Podzemnye bokoplavy
rayona Khosta-Gudauta (Zapadnoe Zakavkaz’e) [Subterranean Amphipods of the Khosta-Gudauta Region (Western Transcaucasia)]. Byulleten Moskovskogo Obshchestva Ispytatelei Prirody. Otdel Biologicheskiy [Bulletin of the Moscow Society of Naturalists. Department of biology] 57 (1), 26-39. (In Russian).
Birstein, J.A., 1967. Podzemnye vodyanye osliki (Crustacea: Isopoda: Asellota) Zakavkaz’ya
[Subterranean Water Lice (Crustacea: Isopoda: Asellota) of Transcaucasia]. Zoologicheskii Zhurnal [Russian Journal of Zoology] 46 (6), 856-865. (In Russian).
Birstein, J.A., Ljovuschkin, S.I., 1967. Nekotorye itogi i zadachi izucheniya podzemnoy fauny SSSR [Some Results and Goals of Studies of the Subterranean Fauna of the USSR]. Zoologicheskii Zhurnal [Russian Journal of Zoology] 46 (10), 1509-1535. (In Russian).
Chertoprud, M.V., 2006. Rodnikovye soobshchestva makrobentosa Moskovskoy oblasti [Spring macrobenthos communities of the Moscow province]. Zhurnal Obshchei Biologii [Journal of General Biology] 67 (5), 376-384. (In Russian).
Chertoprud, M.V., 2010. Reofil’nye soobshchestva makrobentosa Severo-Zapadnogo Zakavkaz’ya [Rheophilic macrobenthic communities of the Northwest Transcaucasia]. Materialy IV Vserossiyskogo simpoziuma po amfibioticheskim i
vodnym nasekomym i X Trikhopterologicheskogo simpoziuma [Proceedings of the IV All-Russia Symposium on Amphibiotic and Aquatic Insects of Russia and X Trichopterological Symposium], North Ossetian State University, Vladikavkaz, Russia, 131-135. (In Russian).
Chertoprud, M.V., 2011. Diversity and classification of rheophilic macrozoobenthos in middle latitudes of European Russia. Biology Bulletin Reviews 1 (3), 165-184.
Chertoprud, M.V., Peskov, K.V., 2007. Biogeografiya reofil’nogo makrobentosa yugo-vostochnoy Evropy [The rithral macrobenthos community biogeography of southeastern Europe]. Zhurnal obshchei biologii [Journal of General Biology] 68 (1), 52-63. (In Russian).
Derzhavin, A.N., 1945. Podzemnye bokoplavy Zakavkaz’ya [Subterranean Amphipods of Transcaucasia]. Izvestiya Akademii Nauk Azerbaidzhanskoi SSR [Proceedings of the Academy of Sciences of the Azerbaijan SSR] 8, 27-43. (In Russian).
Dublyansky, V.N., Klimenko, V.I., Vakhrushev, B.A., Iliukhin, V.V., 1985. Karst i podzemnye vody gornykh massivov Zapadnogo Kavkaza [Karst and Groundwaters of Mountain Massifs of the Western Caucasus]. Nauka, Leningrad, USSR, 150 p. (In Russian).
Georgiev, D., Hubenov, Z., 2013. Freshwater snails (Mollusca: Gastropoda) of Bulgaria: an updated annotated checklist. Folia Malacologica 21 (4), 237-263.
Gray, D.P, 2005. Braided river springs: distribution, benthic ecology and role in the landscape. Thesis for Master’s Degree in Ecology. University of Canterbury, UK, 221 p.
Kucheruk, N.V., Savilova, E.A., 1985.
Kolichestvennaya i ekologicheskaya kharakteristika donnoy fauny shel’fa I verkhnego sklona rayona severoperuanskogo apvellinga [Quantitative and ecological characteristics of benthic fauna of the shelf and upper slope of the North-Peruvian Upwelling]. Byulleten Moskovskogo Obshchestva Ispytatelei Prirody. Otdel Biologicheskiy [Bulletin of the Moscow Society of Naturalists. Department of biology] 89 (4), 59-70. (In Russian).
Ljovuschkin, S.I., 1963. Biospeleologicheskie issle-dovania v Zapadnom Zakavkaz’e letom 1960 g. [Biospeleological Studies in Western Transcauca-
sia in the Summer of 1960]. Novosti Karstovedeni-ya i Speleologii [News of Karstology and Speleology] 3, 66-68. (In Russian).
Martynov, A.V., 1932. K poznaniyu presnovodnoy fauny chernomorskogo poberezhya Kavkaza. I. Amphipoda [On the Freshwater Fauna of the Black Sea Coast of the Caucasus. I. Amphipoda]. Trudy Zoologicheskogo Instituta Akademii Nauk SSSR [Proceedings of the Zoological Institute of the USSR Academy of Sciences] 1 (1), 73-98. (In Russian).
Palatov, D.M., Vinarsky, M.V., 2015. Ekologia i rasprostranenie gastropod podsemeystva Bel-grandiellinae (Mollusca: Gastropoda: Hydrobiidae sensu lato) na territorii Zapadnogo Zakavkazya [Ecology and Distribution of Snails of the Subfamily Belgrandiellinae (Mollusca: Gastropoda: Hydrobiidae sensu lato) in Western Transcaucasia]. In: Turbanov, I.S., Marin, I.N. and Gongalsky, K.B. (eds.), Materialy Vserossiyskoy molodezhnoy kon-ferencii “Biospeleologiya Kavkaza b drugikh rayon-ov Rossii” [Proceedings of the All-Russian Conference “Biospeleology of the Caucasus and Other Regions of Russia”]. Kostromskoi Pechatnyi Dom, Kostroma, Russia, 49-54. (In Russian).
Sidorov, D.A., 2014. Towards the systematics of the subterranean amphipod genus Niphargus (Crustacea: Amphipoda: Niphargidae) of Transcaucasia: new records of N. inermis and N. iniochus in Abkhazia. Arthropoda Selecta 23 (4), 363-377.
Sket, B., 1999. High biodiversity in hypogean waters and its endangerment - the situation in Slovenia,
the Dinaric karst, and Europe. Crustaceana 72 (8), 767-779.
Sokolova, A.M., Palatov, D.M., 2015. Stygobiont Fauna of the Black Sea Coast near Tuapse. In: Turbanov, I.S., Marin, I.N. and Gongalsky, K.B. (eds.), Materialy Vserossiyskoy molodezhnoy kon-ferencii “Biospeleologiya Kavkaza b drugikh rayon-ov Rossii” [Proceedings of the All-Russian Conference “Biospeleology of the Caucasus and Other Regions of Russia”]. Kostromskoi Pechatnyi Dom, Kostroma, Russia, 76-79. (In Russian).
Starobogatov, Ya.I., 1962. K poznaniyu molluskov podzemnykh vod Kavkaza [On the Knowledge of Mollusks from the Subterranean Waters of the Caucasus]. Byulleten Moskovskogo Obshchestva Ispytatelei Prirody Otdel Biologicheskiy [Bulletin of the Moscow Society of Naturalists. Department of biological] 67 (6), 42-54. (In Russian).
Turbanov, I.S., Palatov, D.M., Golovatch, S.I., 2016. The state of the art of biospeleology in Russia and other countries of the former Soviet Union: a review of the cave (endogean) invertebrate fauna. 1. Introduction - Crustacea. Entomological Review 96 (7), 926-963.
Ulfstrand, S., 1968. Benthic animal communities in Lapland streams. Oikos (Supplement) 10, 1-120.
Williams, D.D., Williams, N.E., 1998. Invertebrate communities from freshwater springs: what can they contribute to pure and applied ecology. In: Bo-tosaneanu, L. (ed.). Studies in crenobiology: The biology of springs and springbrooks. Backhuys Publishers, Leiden, The Netherlands, 251-261.
