Oribatid mites in a succession of permafrost soils in Central Yakutia

ABSTRACT

Thermokarst troughs formed on ice-rich ground in Central Yakutia harbor contrasting soils that have developed from lake silt through a marsh stage to meadow and steppe-like soils. Associated processes result in radical transformations of an important component of the decomposer community in the biological cycle—the oribatid mites community. During the transition of soil from a Histic Reductaquic Cryosol to a Gleyic Cryosol and, finally, to a Turbic Chernic Cryosol, the number of species increased from three to six to thirteen. Total abundance of oribatid mites increased from 1,600 m⁻² (±265) to 2,442 m⁻² (±328) to 8,640 (±588) m⁻². A characteristic feature of these permafrost soils was the considerable similarity of the populations in the Gleyic Cryosol and the Turbic Chernic Cryosol and their negligible overlap with the oribatids population of the Histic Reductaquic Cryosol. The peculiarity of the Histic Reductaquic Cryosol is manifested both in quantitative parameters of the communities and in their qualitative characteristics, such as the dominance structure and the sets of species with different ecological preferences.

KEYWORDS:

• Eastern Siberia
• Cryosol
• oribatid mites
• abundance
• species richness

Introduction

The basis of relief in the Central Yakutian landscape are large deposits of ice that have formed during the harsh and humid climate of the Pleistocene. Most of the ice has been preserved throughout the Holocene due to the extremely continental conditions in Central Yakutia with its very cold winters. However, intermittently warmer conditions degraded parts of the ice deposits and formed thermokarst depressions, most likely during the early Holocene 11,000 to 9,000 years before present (Katamura et al. 2006). Thermokarst formation seems to have been inhibited in later periods (Katamura et al. 2009). The thermokarst process begins with the formation of a shallow lake in a boreal forest ecosystem on permafrost soil. Through its storage of heat the lake increases the thaw depth of permafrost. While ice-rich layers melt, land subsides and a shallow thermokarst depression forms, locally known as “alas.” The lake forms the contour of the future alas trough. At the bottom of the lake sapropel is sedimented, carbonates build up in the form of abundant small shells, and the composition of the sediment becomes more dense. As the alas loses water to the atmosphere, belts of different ecosystems form around the remainder of the lake in a long-term secondary succession. First, marsh soils develop around the waterlogged shoreline where decomposition is limited. Hence, organic matter accumulates. With time and increasing distance from the receding shoreline, the active permafrost increasingly dries up and the former marsh turns into a meadow. This drying is accompanied by an upward transport of salts that collect near the surface. Meadow ecosystems in this permafrost region are characterized by high productivity but also by a fast turnover rate of organic matter (Desyatkin 2008). The final stage of development in the alas is an ecosystem with typical steppe characteristics in terms of both soils and vegetation. This ecosystem starts to form in the outermost and most elevated parts of the alas through further drying of the active layer (Savvinov, Mironova, and Bosikov 2005; Desyatkin 2008). Today, the central part of an alas in the Central Yakutian landscape is usually occupied by a lake or pond, surrounded with increasing distance from the waterside by marsh, meadow, and steppe vegetation on corresponding soils (Figure 1). Current vegetation types may have established in the late Holocene, perhaps one or two millennia before present (Katamura et al. 2006, 2009). The depth of alases varies from 2 to 30 m, depending on the thickness of the melted ice deposits. At present, alases occupy significant areas in Central Yakutia. In the Lena–Amga interfluves, for example, they occupy 20 to 30 percent of the territory (Ivanov, Mironova, and Savvinov 2004; Desyatkin 2008).

Figure 1. (left) Map of the Arctic. The North Pole is in the middle (small black cross); oceans are in blue and land is in white. The land mass on the right-hand side shows the northern part of the Eurasian continent. A red circle indicates the location of the study site in the middle basin of the Lena River (gray line passing through the red circle). (middle) photograph of Khotu Alas taken by the Ikonos satellite in July 2002. (right) Schematic soil map of approximately the same area as depicted in the photograph. A red line marks the border of Khotu Alas and the lake in its center is in blue. The pattern associated with the numbers indicates the soil types listed in Table 1: (1) Histic Reductaquic Cryosol, (2) Gleyic Cryosol, (3) Turbic Chernic Cryosol. Pattern 4 covers the area unaffected by thermokarst processes.

Table 1. Position, soil type, and vegetation parameters as found at the three investigated sites in August 2017.

		Soil type		Vegetation
Site	Geomorphological position	Russian soil classification	International classification(WRB 2014 2015)	Phytocenosis	Cover	Height
1	20 m from waterside and 200 m from fringe of alas	Permafrost alas peaty-gley	Histic Reductaquic Cryosol	Marshy sedge meadow (uncut)	100%	55 cm
2	90 m from waterside and 130 m from fringe of alas	Permafrost alas chernozem-meadow	Gleyic Cryosol	Grass meadow (cut for hay)	80%	40 cm
3	150 m from waterside and 70 m from fringe of alas	Permafrost alas meadow-chernozem	Turbic Chernic Cryosol	Steppe-like grass meadow (cut for hay)	80%	40 cm

Note. The Russian soil classification is according to Yelovskaya (1987) and translated literally. WRB = World reference base for soil resources.

Decomposition and mineralization of organic matter is an essential part of the biological cycle in all ecosystems. Most of it is carried out by soil microorganisms and about 15 percent of organic matter is decomposed by soil animals (Tate 1987). The biomass of soil animals is less than 1 percent of the mass of plant residues accruing for decomposition (Zvyagintsev, Babieva, and Zenova 2005), but without soil animals, decomposition is delayed two to five times (Striganiva 1980). A meta-analysis of fauna exclusion experiments concluded that the presence of soil animals enhances litter decomposition rates globally on average by 35 percent (Garcia-Palacios et al. 2013). About 25 percent of annual litterfall in boreal forests is consumed by litter-feeding fauna (Heděnec et al. 2022). One numerous and important group of soil-dwelling animals is microarthropods, which are a key link in the chain of soil organic matter decomposition (Seniczak 2011). Two taxonomic groups dominate this category of soil animals: Collembola and oribatid mites (oribatids). Oribatids are very sensitive to abiotic changes occurring during a succession (Salazar-Fillippo et al. 2023). However, oribatids in soils of natural ecosystems of Central Yakutia have received little attention so far. Available data are limited to the soils of pastures in this region (Krivolutskii 1978; Andreeva and Tatarinova 2018) and soil under birch and larch forest (Andrievskii, Yakutin, and Puchnin 2021). The aim of this study was to investigate the peculiarities of changes in the population of oribatid mites during the evolution of permafrost alas soils of Central Yakutia.

Materials and methods

This study was conducted in the Gorny District of the Republic of Sakha (Yakutia). The Gorny District occupies the southeastern part of the Lena–Vilyui watershed. Alas is a widespread form of relief in the area. Most alases in that area are flat with a small depth of depression and sides that are not steep. The bottom of the alases is flat and near the lakes often pockmarked. Many alases have an elongated valley-like shape. Sometimes a chain of troughs connects them, resembling a small grassy river. Salinization in meadow soils of alases in the Gorny District is poorly expressed (Egorov et al. 1970; Savvinov, Mironova, and Bosikov 2005). Three permafrost soils of Khotu Alas (62°28′ N, 126°02′ E) were selected as objects of study: a Histic Reductaquic Cryosol, a Gleyic Cryosol, and a Turbic Chernic Cryosol (Table 1).

All of the investigated soils are on a catena about 130 m long (Figure 1, Table 1). The height difference between Site 1 and Site 3 is about 3 m. Soil types were confirmed in an earlier study (Conen et al. 2011) by digging a pit (length 1.2 m, width 0.6 m, depth 1.0 m), and quadruplicate samples were collected from each soil type within a circle of 20 m to analyze organic carbon (C_org) and salinity. All four replicate samples were analyzed for C_org but bulked for salinity measurements.

The pH of aqueous soil extract was determined using a pH meter. Determination of sodium, potassium, calcium, and magnesium in the aqueous extract was carried out by flame photometric method. Chloride ions were determined by the Mohr method; that is, by titration with silver nitrate. Soil carbon content was determined by the wet oxidation method according to Tyurin (Arinushkina 1970; Shamrikova et al. 2022). Soil chemical properties were determined for the upper 10 cm, which we considered to be homogeneous in these soils. Vegetation was assessed in terms of cover and height. Ivanov, Mironova, and Savvinov (2004) studied the vegetation of alas meadows in the same region and found the following species to be dominant on Histic Reductaquic Cryosol: Carex juncella, Poa palustris, Calamagrostis langsdorffii; on Gleyic Cryosol: Ranunculus borealis, Poa pratensis, Thalictrum simplex, Hordeum brevisubulatum, Vicia cracca, Artemisia tanacetifolia, Artemisia gmelinii, Aster alpinus; and on Turbic Chernic Cryosol: Elytrigia repens, Agrostis trinii, Festuca rubra, Vicia cracca, Thalictrum simplex, Galium verum.

Soil samples for oribatids population analysis were taken in August 2017 from the upper 5 cm of soil at each site; that is, from within an area with homogenous soil properties and a homogenous vegetation cover extending over a few hundred square meters. Ten replicate samples of 25 cm² each were taken at each of the three sites. The distance between neighboring replicates was between 5 and 10 m. One of the replicates from Site 1 and one from Site 2 were lost in transit. Extraction of mites from soil was carried out with a Berlese-Tullgren funnel (Tullgren 1918), 10.5 cm in dimeter, heated by a light bulb from above and completely drying within two weeks. The extracted mites were collected in ethanol and placed in permanent preparations (Fora liquid) in which their species was determined under a microscope. Guides used for the identification of species included Gilyarov (1975a) and Bayartokh (2010). The distribution of oribatids was analyzed in terms of species richness and abundance (density), which reflect the ecological status of living organisms (Chenov 1991). Numbers of mites were calculated per 1 m² based on the horizontal cross-sectional area (25 cm²) of the soil core sampler (Gilyarov 1975b).

Results and discussion

The upper 10 cm of soil at all three sites was slightly alkaline or neutral, with pH values between 7.1 and 7.7 (Table 2). Dominant ions in all soils were HCO³⁻, Ca²⁺, and Mg²⁺. They constituted 80 to 90 percent of the total composition of water extract. Twenty meters from the waterline (Site 1) the upper 10 cm of the Histic Reductaquic Cryosol was only slightly saline. Ninety meters from the waterline (Site 2) the concentrations of HCO³⁻ and Ca²⁺ were increased five- and sevenfold, respectively. Also strongly enhanced were Na⁺ and SO₄²⁻, rendering the top 10 cm of soil at Site 2 sulfate-sodic and highly saline. At Site 3, about 130 m from the waterline and 70 m from the edge of the alas (Site 3) SO₄²⁻ and Na⁺ concentration had declined to values similar to what they were near the waterline (Site 1), whereas HCO³⁻ and Ca²⁺ concentrations were between those at Site 1 and Site 2. Overall, the outermost site (Site 3) was characterized by medium saline-sodic conditions in the upper 10 cm of soil.

Table 2. Properties of the top 10 cm of soil at the three investigated sites.

Site	рН	Сorg (%)	HCO3−	SO4^2−	Cl−	Ca^2+	Mg^2+	Na^+	К^+
1	7.2	16.14 (1.9)	0.314	0.033	0.083	0.201	0.151	0.043	0.013
2	7.7	5.96 (2.4)	1.606	0.442	0.048	1.491	0.073	0.206	0.031
3	7.1	2.52 (0.6)	0.773	0.045	0.051	0.625	0.11	0.051	0.105

Note. Ion concentrations are in mmol_c kg⁻¹. Means and standard deviations (in parenthesis) of C_org are shown in %. Salinity and pH were measured on the same but bulked samples. Therefore, only a single value is available.

The highest concentration of C_org was found in the upper horizon of the Histic Reductaquic Cryosol (Site 1; Table 2). At the stage of the Gleyic Cryosol (Site 2), waterlogging was absent near the surface, providing organic matter decomposers with more favorable conditions as reflected in reduced C_org, which might have been much higher during the preceding marsh phase when the lake had been larger and Site 2 was still closer to its waterline. Concentration of C_org in the upper 10 cm was 2.7 times smaller at Site 2 compared to Site 1. In the course of further desiccation and soil development, concentration of C_org had decreased again by a factor of 2 from Site 2 to Site 3.

A total of seventeen species of oribatid mites (oribatids) were found in the three studied alas soils (Table 3). The values of quantitative community indices (species richness and abundance) increased from near the waterline toward the edge of the alas. Species number increased with soil age from three (Site 1) to six (Site 2) to thirteen (Site 3), similar to a soil chronosequence in Norway, where species numbers were three, eight, and thirteen on land from where a glacier had retreated 32–48, 52–66, and 72–227 years earlier (Hagvar, Solhay, and Mong 2009). The number of species in the oldest soil of this series (10,000 years) was nineteen (Hagvar, Solhoy, and Mong 2009). Total abundance of oribatids in the alas soils increased by a factor of 1.5 from Site 1 to Site 2. An even larger increase, by a factor of 3.5, was observed from Site 2 to Site 3. This large difference likely results from the highly saline conditions at Site 2 limiting oribatid abundance (Yakutin, Andrievskii, and Anopchenko 2018) and the relaxation of this limitation at the less saline Site 3. Enhanced litter decomposition rates by the larger oribatid population at Site 3 might partly explain why C_org was only half as large at that site as compared with Site 2 (García-Palacios et al. 2013). The abundance of oribatids under the meadows at Sites 2 and 3 was on average the same as outside of alas troughs under birch and larch forest (Andrievskii, Yakutin, and Puchnin 2021) but at the lower limit of values in soils under meadow in the geographically contiguous Far East of the Russian Federation (Ryabinin 2009). The abundance of oribatids in the Histic Reductaquic Cryosol of Site 1 was an order of magnitude lower than what has been reported for a subarctic peat bog in northern Sweden (Makkula, Cornelissen, and Aerts 2019). The increase in oribatid abundance with increasing distance from the lake is opposite to what had earlier been found in the same alas for microbial biomass in surface soil. Microbial biomass concentration was highest close to the lake and declined steadily to about one-third toward the edge of the alas (Yakutin and Puchnin 2012).

Table 3. Taxa found at the three investigated sites in terms of average number of specimens (± uncertainty) and relative abundance (%).

Species	Number of specimens (m^−2) and relative abundance (%)
	Site 1	Site 2	Site 3
Tectocepheus velatus (Michael, 1880)	–	1,422 ± 251 (58.2)	3,400 ± 369 (39.3)
Protoribates capucinus (Berlese, 1908)	–	–	2,120 ± 291 (24.5)
Microppia minus (Paoli, 1908)	–	178 ± 89 (7.3)	840 ± 183 (9.7)
Tectoribates ornatus (Schuster, 1958)	–	533 ± 154 (21.8)	680 ± 165 (7.9)
Punctoribates minimus (Shaldybina, 1969)	–	–	400 ± 126 (4.6)
Achipteria coleoptrata (Linnaeus, 1758)	–	222 ± 99 (9.1)	320 ± 113 (3.7)
Ceratozetella sp.	–	–	240 ± 98 (2.8)
Oppiella nova (Oudemans, 1902)	–	–	200 ± 89 (2.3)
Peloptulus phaenotus (Koch, 1844)	–	–	200 ± 89 (2.3)
Acrotritia duplicata (Grandjean, 1953)	–	–	120 ± 69 (1.4)
Liochthonius lapponicus (Tragardh, 1910)	–	–	40 ± 40 (0.5)
Scheloribates latipes (Koch, 1844)	–	–	40 ± 40 (0.5)
Oppia sp.	–	–	40 ± 40 (0.5)
Scutovertex sp.	–	44 ± 44 (1.8)	–
Punctoribates hexagonus (Berlese, 1908)	1,378 ± 247 (86.1)	44 ± 44 (1.8)	–
Astegistes pilosus (Koch, 1841)	178 ± 89 (11.1)	–	–
Moritzoppia jamalica (Gordeeva y Grishina, 1991)	44 ± 44 (2.8)	–	–
Total abundance	1,600 ± 268	2,443 ± 331	8,640 ± 588
Number of species	3	6	13

Note. Uncertainty was estimated as the square root of the number of specimens found in the analyzed soil samples, scaled to 1 m².

Oribatid species were distributed unevenly over the biotopes of the permafrost alas soils. The oribatid communities of the three studied ecosystems differed appreciably in terms of species composition and in the relative abundance of species within these communities (Table 3). Dominance structure in the most mature soil (Turbic Chernic Cryosol, Site 3) was closest to that of other soil ecosystems in that the relative abundance of species followed a relatively smooth distribution. Ranked by the number of specimens, the distribution closely (r² = 0.94) followed an exponential function. The two most abundant species (Tectocepheus velatus and Protoribates capucinus) accounted for a total of 63.8 percent of the community, whereas the two dominant species in the permafrost chernozem–meadow at Site 2 (Tectocepheus velatus and Tectoribates ornatus) accounted for 80 percent of the community of that ecosystem. Characteristically, Tectocepheus velatus and Protoribates capucinus are widespread polyzonal and eurytopic species. In a total of 234 locations in the Far East of the Russian Federation, they have been documented for 167 and 42 locations, respectively (Ryabinin 2015). In Central Yakutia, Tectocepheus velatus was also identified as the most abundant species outside alas troughs (Andrievskii, Yakutin, and Puchnin 2021). The second most common species at Site 2, Tectoribates ornatus, is reported much more rarely from other places (Ryabinin 2015; GBIF 2023).

In the Histic Reductaquic Cryosol (Site 1) a single species (eudominant; Punctoribates hexagonus) constituted 86.1 percent of the community. Only two other species accounted for the rest (13.9 percent). Such a dominance structure, with a small number of species constituting the major part of the community, indicates either a disturbed biotope or unfavorable environmental conditions for the microarthropod species inhabiting it (Kuznetsova 2005). One factor for low numbers in soil near the waterline could be the high water table (Silvan, Laiho, and Vasander 2000; Laiho et al. 2001), which is a characteristic feature of the Histic Reductaquic Cryosol at Site 1.

The studied sequence of soils and ecosystems in the alas has formed naturally, initiated by thermokarst formation probably in the early Holocene (Katamura et al. 2006, 2009). The resulting alas evolved over a long time while the lake in the center of it gradually shrunk. Human influence is very low and limited to hay-making on the older soils at Sites 2 and 3. Therefore, we presume that natural environmental conditions prevailed during their development. These conditions became increasingly favorable for communities of oribatid mites when soil type changed from a Histic Reductaquic Cryosol (Site 1) to a Gleyic Cryosol (Site 2) and finally to a Turbic Chernic Cryosol (Site 3). This last stage of the succession supports thirteen of all seventeen species found in the alas. Nine species were recorded only in this soil. Four species found in the Turbic Chernic Cryosol (Site 3) were also found in the preceding soil type, the Gleyic Cryosol (Site 2). These were Tectocepheus velatus, Tectoribates ornatus, Achipteria coleoptrata, and Microppia minus. Together, they accounted for 89.1 percent of the community in the Gleyic Cryosol (Site 2), whereas in the older Turbic Chernic Cryosol (Site 3) they still contributed a substantial but smaller proportion (50.9 percent). The Bray-Curtis dissimilarity between Site 2 and Site 3 is 0.46. A decrease in the relative abundance of a dominant species with increasing soil maturity was also observed in the very long run in the time series in Norway mentioned before. There, the abundance of Tectocepheus velatus decreased from 57 percent in the age zone 32 to 48 years to 10 percent in the age zone 10,000 years (Hagvar, Solhoy, and Mong 2009). Of all seventeen oribatid species in the three studied ecosystems, only four species were not recorded at the most mature site (Turbic Chernic Cryosol, Site 3). One of them, Scutovertex sp. was exclusively found in the Gleyic Cryosol (Site 2), in the form of a single specimen.

Three other species were recorded almost exclusively in the youngest ecosystem (Histic Reductaquic Cryosol, Site 1), sharply distinguishing the oribatids community of this soil from that of the other soils. These three species are able to populate the waterlogged ecosystem, which is extremely unfavorable for the oribatid mites community as a whole (Silvan, Laiho, and Vasander 2000; Laiho et al. 2001). The clearly eudominant Punctoribates hexagonus (86.1 percent of the community) was recorded in the more favorable Gleyic Cryosol (Site 2) only as a single specimen, and the second most abundant species (subdominant), Astegistes pilosus (11.1 percent of the community), was found exclusively in the Histic Reductaquic Cryosol (Site 1), together with a single specimen of Moritzoppia jamalica. This demonstrates the unique ecological standing of Punctoribates hexagonus and Astegistes pilosus in the studied ecosystems. Although they are known as geographically widespread species, here they are obviously ecological hygrophiles. This ecological preference also seems to be inherent to both Punctoribates hexagonus and Astegistes pilosus in other natural zones. Both species are noted as moisture tolerant; for example, in the West Siberian forest–steppe, where they constitute a significant share of meadow–swamp solonchak communities (Grishina, Stebaeva, and Lapshina 1991). Further, Punctoribates hexagonus has been found in two wet meadows in northern Italy (Fischer and Schatz 2010) and both Punctoribates hexagonus and Astegistes pilosus were present in northern peat bogs (Mumladze, Murvanidze, and Behan-Pelletier 2013; Salisch et al. 2017). The combined evidence suggests their ecological specificity as hygrophilic species. The predominance of these two species in the ecosystem at Site 1 and their near absence in the two drier ecosystems (Sites 2 and 3), together with only a single specimen of one other species (Moritzoppia jamalica) found at Site 1, underlines that the Histic Reductaquic Cryosol in these very cold conditions is a habitat for a very specific oribatid mites population, consisting of species that may not be able to compete with other species at the drier sites.

Conclusion

The first stage of alas soil evolution characterized by low temperatures, wet conditions, and a weak salinity (Histic Reductaquic Cryosol) constitutes extreme conditions that manifest in a low abundance of oribatids represented by very few moisture-tolerant species. The transition from hydromorphic to automorphic soils considerably changes the habitat, making it drier and more saline. Concurrently, the population of oribatid mites restructures quantitatively and qualitatively. Overall abundance is increased severalfold at the stage of the zonal soil (Turbic Chernic Cryosol). Sets of species with different ecological preferences and dominance structure develop in which the very few species initially present are completely replaced by a more diverse community. Thus, the evolution of alas soils of Central Yakutia from lacustrine silt through the marsh stage to meadow and steppe-like soils is associated with a radical restructuring of an important component of the decomposing part of the biological cycle—the oribatid mites community.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was performed under the state assignment of the Institute of Soil Science and Agrochemistry, Siberian Branch of the Russian Academy of Sciences. Funding was obtained from the Ministry of Science and Higher Education of the Russian Federation.