Successions of Oribatid Mites (Acariformes: Oribatida) on Disturbed Areas N

ISSN 1062-3590, Biology Bulletin, 2009, Vol. 36, No. 5, pp. 510Ð515. © Pleiades Publishing, Inc., 2009. Original Russian Text © N.A. Ryabinin, A.N. Pan’kov, 2009, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2009, No. 5, pp. 604Ð609.

ECOLOGY

Successions of Oribatid Mites (Acariformes: Oribatida) on Disturbed Areas N. A. Ryabinina and A. N. Pan’kovb aInstitute of Water and Ecological Problems, Far East Division, Russian Academy of Sciences, Kim Yu Chen 65, Khabarovsk, 680000 Russia bSurgut State University, Energetikov 14, Surgut, 626400 Russia e-mail: [email protected] Received April 17, 2008

Abstract—During recovery succession, structural and functional changes in oribatid mite communities occur: the number of species increases, the structure becomes more complex, the proportion of surface-living and nonspecialized forms increases, and the role of parthenogenetic species decreases. The direction of succession is to form a community characteristic of the zonal type of vegetation. Four stages are selected. The colonizationÐ accumulation stage involves the initial accumulation of organic matter due to activity of microorganisms. Ori- batids are not numerous at this stage. The unstructured stage is characterized by unstable monodominant communities of parthenogenetic oribatids with short life cycles. The next stage is structuring, when the proportion of parthenogenetic forms decreases, and that of nonspecialized forms increases. Communities are monodominant. The ﬁnal stage is stabilization. The proportion of parthenogenetic species decreases noticeably. The generic and species composition of the communities stabilizes. The community achieves zonal features. DOI: 10.1134/S1062359009050136

Successions of oribatid mites on disturbed areas from three sides of a section of soil (down to 1 m) in three were studied on Kamchatka and the Kuril Islands on replications. The samples were taken from various layers soils exposed to ash fallout and at different stages of with care not to mix soil from the superposed layers. In soil formation. Other areas exposed to volcanic activity the stratiﬁed ash soils of Kamchatka, to study vertical were also studied. Moreover, the rock dumps of open distribution, the samples were taken according to the dis- pits of different ages in the surroundings of Khabarovsk position and thickness of layers of buried ash, slag, and were also surveyed. humus horizons.

MATERIALS AND METHODS RESULTS AND DISCUSSION Oribatid mites were collected according to the proto- col of complex survey of soils (Krivolutskii, 1975). Volcanogenic soils. Volcanoes a produce huge Modified Berlese-Tullgren funnels were used to extract amount of friable material (slag, ash, etc.) during eruptions. Thus, the Tyatya volcano on Kunashir Island in mites. The funnels were made of cardboard (a stationary 3 variant made of tin), and the metal net had a 3 × 3 mesh 1973 erupted over 200 mln. m of volcanic slag and ash, 2 (occasionally it was made of flimsy polygraphic gauze). which covered 20000 km and killed forests over an A 35°ë temperature on the sample surface was achieved area of 20 km2 (Markhinin, 1980). Slag and ash falling by applying 60-Wt bulbs (by regulating the lamp’s after eruptions are sterile (Ten, Kuzyakina, 1976). After hanger length). The extraction lasted for 4Ð6 days strong acids, alkali and other toxic compounds depending on the sample moisture. Oribatids were sorted adsorbed on the surface of ash particles are washed out out of the extract under a dissecting microscope. For spe- and the pyroclasts become a relatively suitable sub- cies identification, permanent slides were made with strate for various organisms to live on. Fora-Berlese solution as a fixing medium. The first settlers braving extreme conditions are In total, 30 biotopes on ash and slag fields of different chromogenic coryneformic and psychrophilic bacteria ages, under different vegetation, and on various recovery that are able to live in “starvation” conditions. There stages were studied. In each biotope, 15Ð20 samples of were only single bacterial cells in the ash materials col- 125Ð250 cm3 were collected, which is sufficient to esti- lected after the first rain since the Tyatya volcano mate the species composition and abundance of mites erupted. Two years later, the numbers of microorgan- (Krivolutskii, 1975; Chernov, 1975). In some biotopes, a isms in the ash material was tens of thousands of bacte- vertical distribution of oribatid mites along the soil pro- rial cells in 1 g of substrate. Three years later, it reached file was studied. For this aim, the samples were taken hundreds of thousands (Ten, Rogova, 1980). The repro-

510

SUCCESSIONS OF ORIBATID MITES (Acariformes: Oribatida) 511

Table 1. The abundance of microarthropods in ash and ash-layered soils, indiv. mÐ2 Trombidiids Ash field Oribatids Collembolans and Mesostigmatids Ash Since eruption 0 0 0 5 years (Tyatya volcano) Solitary Solitary less than 10000 20 years (Bezymyannyi volcano) 1200Ð2000 300Ð2400 Solitary 30 years (Klyuchevskaya Sopka volcano, 600Ð3600 200Ð1800 less than 200 Zavaritskii stream) over 50 years (Klyuchevskaya Sopka volca- 5000 3800 less than 1600 no, Kroshka crater) Ash-layered soils Ploughed field 1200 1000 500 Cereal-forb meadow 1200 Solitary less than 1100 Legume-forb meadow 7600 2800 less than 650 Alpine meadow 5700 46200 less then 7200 Green-moss spruce forest 34600 15800 less than 9500 duction rate of microorganisms is negligible due to low caused by intrapopulation processes of regulation pro- nutrient supply. The majority of microflora consists of viding the dynamic balance between the reproduction oligotrophic and oligonitrophilous chromogenic micro- and mortality of microbial populations (Kondrat’eva, organisms, which are able to grow on nitrogen-depleted 1996). and nitrogen-free substrates. In young sediments, chro- Microarthropods from the adjacent areas not mogenic forms constitute from 46 to 98% (Ten, Kuzy- affected by ash fallout colonize ash sediments. Inverte- akina, 1976; Pimenov, 1983). Species with short life brates spread by means of wind, birds, and water from cycles able to form resting spores prevail among those. rains and melted snow. The first colonists, minute trom- The continuous flow of microorganisms and organic bidiid mites, are connected with the upper 5Ð10 cm compounds from precipitation and marine splashes is a horizon. Their abundance reaches up to 10000 individ- nutrition source for colonizing bacteria. In addition, uals mÐ2 (Table 1). rainwater contains algae, protists, the pollen of conifers, liverworts, the spores of micromycetes, and Oribatid mites are solitary at the first stages of suc- mosses and lichens (Gregori, 1964). The majority of cession. Among them, the pioneer species are represen- introduced organisms die, and the soils receive fertili- tatives of the genus Suctobelbella and species with a zation equivalent to 5 kg of nitrogen per 1 ha a year. short life cycle and parthenogenetic reproduction, Lio- This amount of nitrogen facilitates colonization by veg- chthonius sellnicki and Oppiella nova (Ryabinin, etation (Gregori, 1964). Suitable conditions for the Pan’kon, 1987). development of more specialized microbial colonists The ash stratum is colonized by parthenogenetic are created by the gradual weathering of pyroclastic species that have advantages over amphimictic ones. materials and accumulation of introduced organic com- The prevalence of apomictic species during the coloni- pounds combined with the products of the vital activity zation of new environments at the early succession of microorganisms. stages has already been noted (Maynard, 1981). In par- Micobacteria, flavobacteria, and coryneformic ticular, this was observed during oribatid succession in organisms are replaced by actinomycetes, fungi, and peatbog extraction sites, where the parthenogenetic spore-forming bacteria (Pimenov, 1983). As shown by species L. sellnicki and O. nova were among the pio- Kuzyakina (1985), who studied microorganismal suc- neers and dominants (Chistyakov, 1971, 1974; cessions in ashes and slags of the Tyatya, Alaid, and Artem’eva, 1987, 1989). During ecogenesis on Surtsey Tolbachik volcanoes, the development of coenosis fol- Island (Iceland), a large number of parthenogenetic lowed the soil type. In the participation of all groups of species was noted among pioneer species. microorganisms and their vital activity products, volca- According to our own data, the vegetation-free sol- noclasts were partially transformed into collyrite, a fatara fields across all soil types (acid, hyeracid, and component of primary primitive soils. Schwabe (1970), ultrabasic) of the Golovnin volcano (Kunashir Island, who studied the egogenesis of the volcanic island Surt- Kuril Islands) are inhabited by widely distributed orib- sey close to the island, noted that primary coenoses atid forms (Table 2). O. nova dominates (over 50%) transform fast, often disappear, and lead to the forma- everywhere. The abundance of mites is low; the assem- tion of new ones that are more complex and complete. blages are unstable and often changeable. Tectocepheus Abundant fluctuations are typical for the pedogenic velatus, feeding on algae (Chistyakov, 1971), inhabited rocks at the primary stages of weathering. They are lichen films on the solfatara fields. Moreover, O. nova,

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Table 2. Abundance of mites in various substrates, indiv. mÐ2 Substrate Species hyperacid ultrabasic acid Oppiella nova 400 300 800 Quadroppia quadricarinata 0 100 0 Suctobelbella acutidens 100 100 200 S. falcata 100 0 0 S. opistodentata 0 0 200 S. subcornigera 0 200 0 Total 600 700 1200

Oripoda pinicola, and Carabodes peniculatus were bamboo, the conditions suitable for invertebrates to found as well. Under the moss cover, the abundance of inhabit were created. The amount of humified organic oribatids reached up to 300000 indiv. mÐ2. There were remains in ashes increased. When vegetation appeared, 14 species, with Trimalaconothrus glaber dominating the diversity of microflora and microfauna increased. (99%). This species possesses pseudoviviparity, which Twenty years after the Bezymyannyi volcano (Kam- can be considered as an adaptation to life in extreme chatka Peninsula) erupted, rather complex communi- environments. A gradual complication of oribatid ties were formed on the area covered by the fallen-out coenoses occurred under crowberries and mountain rocks. Sedges, woodreed mosses, and willow curtains pine: the number of species increased (42 instead of grew on the slag. Large soil invertebrates (enchytraeids, 18), the index of species saturation and the number of wireworms, millipedes, etc.) were noted here, as well as dominating species grew (Fig. 1). The community of rich microarthropod fauna including several collembo- oribatid mites became more stable, as judged by the lan species. The core of the oribatid fauna was repre- increased occurrence of species across the samples. In sented by eurybiontic species inhabiting tiny soil pores, the soil under mountain pine, the community composi- Epidamaeus sp., and Latovertex borealis. L. sellnicki tion approached the zonal type. However, dominant and O. nova dominated here. were parthenogenetic species and O. nova (72 and A similar picture was noted at the lava field of the 68%, respectively). Zavaritskii volcano (Kamchatka Peninsula) 30 years As a result of weathering and activity of microor- after the eruption (Fig. 2). In contrast to the previous ganisms, ash and solfatara fields are gradually trans- relatively flat biotope, large lumps of basalt and slag formed into a substrate suitable for vegetation to grow. heaped up chaotically. Interstitions between the heaps In contrast with massive-crystalline rocks, the coloni- filled up with ash and the products of destruction, as zation of friable sediments occurs simultaneously by well as with wind deposits. The vegetation cover was both high and lower plants, and not gradually. The same scarce. Microarthropods were distributed heteroge- was observed on Sursey Island. After ashes were cov- nously over the area. The highest abundance was found ered by legumes, sedges, and sometimes, mosses or in moss sods, with a monodominant complex formed

45 42 40 35 30 29 I 25 II 20 18

Quantity 15 14 14 10 10 6 5 3 4 4 0 12345

Fig. 1. The number of species (I) and genera (II) of oribatid mites on solfatara ﬁelds. Sampling areas: 1—no vegetation, 2—lichen, 3—moss, 4—crowberry, 5—mountain pine.

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16 I 14 12 II 10 8

Quantity 6 4 2 0 1234

Fig. 2. The number of species (I) and genera (II) of oribatid mites on slag dumps of different ages. Sampling areas: 1—Tyatya volcano, 2—Bezymyannyi volcano, Klyuchevskaya Sopka volcano: 3—Zavaritskii stream, 4—Kroshka crater. 100 90 I 90 80 II 70 63 60 50 50 40 38 38 30

Quantity 30 19 19 23 20 13 13 15 10 0 1 year 3 years 5 years 23 years 32 years Control

Fig. 3. The number of species (I) and genera (II) of oribatid mites on the rock dumps of different ages. by L. borealis. Motley grass patches hosted numerous and birch and aspen do so in dry areas; the proportion epigeic forms too. The abundance of mites reached up of pioneer species drastically decreases. Under the can- to 3000Ð4000 indiv. mÐ2, and that of collembolans opy of deciduous trees, conifers (mainly fir) appear. reached 2000 indiv. mÐ2. Fifteen to twenty years later, the differentiation of the Fifty years after the eruption (Kroshka crater, Kly- thin poorly stratified soil profile begins because of the uchevskaya Sopka volcano), the abundance and species accumulation and decomposition of litter and roots. and genera diversity of microarthropods increased After 30 to 35 years, the biocenosis acquires a zonal shape. almost two times: oribatid mites at 5000 indiv. mÐ2 and collembolans at 3800 indiv. mÐ2. The proportion of the The formation of plant communities and the direc- parthenogenetic species decreased from 75% (Tyatya tion of soil-forming process largely depend on the volcano) down to 25%. Large epigeic oribatid species activity of microorganisms and soil invertebrates. As in became abundant. the slag deposits of Kamchatka, the microbial commu- Rock Dumps of an Open Pit. Similar regularities can nities of the dumps after one year consist of be seen in colonization of the dumps of open pits. The saprophytes, oligonitrophiles, actinomycetes, and some studies were carried out in the surroundings of Kha- others. It has been documented (Krupskaya, 1992) that barovsk in the Korfovskii open pit at rock dumps 1, 3, dumps of 10 to 12 years in age with similar conditions 5, 23, and 32 years after the dump creation. The control of microbial communities are close to the natural soil plot was surveyed in the nearby Bol’shekhekhtsirskii varieties. Dumps that are 25 years old correspond to the Nature Reserve. zonal type. The Korfovskii open pit quarries crushed stone, and The one-year-old rock dumps were surveyed for overburden rock is deposited in the surroundings of the ground, leaf litter, and roots. Microarthropods were pit. Sometimes, the surface of the rock dump is leveled aggregated around the roots, and the community compo- by a bulldozer. A year after the dump formation, the sition was unstable. The inhabitants of tiny soil pores vegetation is sparse: Artemisia sp. and Atriplex sp. pre- dominated. Regrowth of grasses and trees and litter layer vail in dry places, and mosses, mainly Polytrichum sp., thickening led to the enrichment of the oribatid fauna and does in moist areas. Two to three years later, legumes population (Figs. 3, 4). The oribatid community slightly and cereals appear. Then alders emerge in moist places, stabilized, achieving a “forest” shape. At the first stages,

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% pores and parthenogenetic species decreases, while 100 epigeic and nonspecialized species appear. The third stage is structuring. An increase of abundance, species and genera diversity, and monodomi- 80 5 nance are the features of this stage. The proportion of 4 inhabitants of tiny soil pores with short life cycles and 60 3 parthenogenetic reproduction decreases, and that of nonspecialized increases. Communities are monodom- 40 2 inant. The soil proﬁle begins to differentiate. 1 The fourth stage is stabilization. The generic and 20 species composition of the communities stabilizes. The role of inhabitants of tiny soil pores and parthenogenetic species decreases. The community is poly/mon- 0 odominant; the cenotic role of epigeic forms increases. The community achieves zonal features.

1 year Hence, during recovery succession, structural and 3 years 5 years Control 23 years 32 years functional changes of oribatid communities towards increasing species diversity occur, namely, complicat- ing the structure, increasing the proportion of epigeic Fig. 4. The ratio of life forms of oribatid mites at various stages of succession. 1—epigeic forms, 2—the inhabitants and nonspecialized forms, and decreasing the cenotic of tiny soil pores, 3—the inhabitants of deep soil layers, role of parthenogenetic species. The general trend of 4—litter dwellers, 5—nonspecialized. succession is to form a community characteristic for the zonal type of vegetation. The features and the pace of each stage depend on the substrate characteristics, cli- oribatids from the families Brachychthoniidae, Oppi- matic features of the area, the duration of life cycles, idae, and Suctobelbidae prevailed, many of them having and the features of adjacent undisturbed habitats. parthenogenetic reproduction. O. nova, T. velatus, and Quadroppia quadricarinata were almost always among the dominant species. With vegetation regrowth, the REFERENCES abundance of oribatids increased from 19 to 50 species Artem’eva, T.I., Kompleksy pochvennykh zhivotnykh i (the control had 90 species), species saturation of genera voprosy rekul’tivatsii tekhnogennykh territorii (Complexes increased, and the distribution became more even. The of Soil Animals and Problems of Recultivation of Techno- proportion of inhabitants of tiny soil pores decreased, genically Modified Areas), Moscow: Nauka, 1989. while that of litter and surface inhabitants increased. The Artem’eva, T.I., Soil Animals as Indicators of Biological community achieved a more stable and balanced shape. Recultivation of Technogenically Modified Areas, in Tr. 9-go The colonization of rock dumps was supplied from the mezhdunar. kollokviuma po pochvennoi zoologii “Pochven- nearby undisturbed areas and aspired to the species com- naya fauna i pochvennoe plodorodie” (Proc. 9th Int. Colloq. plex typical for the soils of the cedar pineÐbroadleaf for- Soil Zoology “Soil Fauna and Soil Fertility), Moscow: est zone. Nauka, 1987, pp. 229Ð233. Chernov, Yu.I., The Main Synecological Characteristics of During recovery successions on disturbed areas in Soil Invertebrates and Methods of Their Analysis, in Metody the Russian Far East, there are several stages dependant pochvenno-zoologicheskikh issledovanii (Methods of SoilÐ on the initial substrates and climatic features. Each Zoological Studies), Moscow: Nauka, 1975, pp. 160Ð216. stage is characterized by the level of development and Chistyakov, M.P., Horizontal Distribution of Oribatei on organization of the biocenosis being formed. Depleted Peat Soils of Balakhninskaya Depression, The first stage is a colonization–accumulation one. Ekologiya, 1974, no. 3, pp. 53Ð58. It involves colonization of the substrate by pioneer Chistyakov, M.P., Seasonal Dynamics of Abundance of Ori- microorganisms with short life cycles that are able to batid Mites on Depleted Peat Soils of Gorky Oblast, live on nitrogen-free media and form resting forms. The Ekologiya, 1971, no. 6, pp. 78Ð83. communities are not structured and are species-poor Gregori, F., Mikroflora vozdukha (Air Microflora), Moscow: and rapidly changing. The initial accumulation of Mir, 1964. organic matter occurs in the substrate. Oribatids are sol- Kondrat’eva, L.M., Morskie bakterii i pervichnoe pochvoo- itary at this stage. brazovanie na vulkanoklastakh. Vladivostok; (Marine Bacte- ria and Primary Soil Formation on Volcanoclastic Sedi- The second stage is unstructured. Vegetation and ments), Vladivostok: Dal’nauka, 1996. microarthropods appear. The oribatid communities are Krivolutskii, D.A., Method of Complex Examination of Soils rapidly changing, unstable, monodominant, with low for Population with Microarthropods, in Metody pochvenno- abundance and species diversity, and with a mosaic dis- zoologicheskikh issledovanii (Methods of SoilÐZoological tribution. The proportion of inhabitants of tiny soil Studies), Moscow: Nauka, 1975, pp. 44Ð48.

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