Use of ciliate communities for monitoring ecological restoration of grain for the green in north-western China

Highlights

• To summarize the utilities of the ecological features based on community structure of the soil ciliates for assessing the ecological restoration quality in grain for green.

• Revealing the difference in the ciliate community patterns along with the ecological restoration quality of GFG;

• The soil physical-chemical variables and above-ground plants were the main factors affecting the soil ciliate community composition.

Abstract

A 1-year baseline survey was conducted in north-western China to evaluate the ecological restoration quality of grain for green (GFG) using soil ciliate communities. The aims of this study were focused on analyzing the changes of soil ciliate communities in four plots (A, GFG for 15 years; B, GFG for 13 years; C, layland; D, cultivated land) for GFG environmental assessment. Simultaneously we studied the effects of vegetation communities and physical-chemical variables with GFG changes on soil ciliates. A total of 114 species of ciliates were identified among the four sample sites, representing nine classes, 14 orders, 22 families and 37 genera. The community patterns of the soil ciliates were significantly correlated with the individual abundance of aboveground plants, soil water content, and soil porosity. The contents of total nitrogen were the main factor affecting the soil ciliate community composition. The species number, individual abundance, and diversity index of the ciliates was each in the order A>B>C>D; that is, the community composition of ciliates was complicated with the implementation of the GFG. It was shown that succession of ciliate community shift toward promoting the complexity with the progress of GFG. These findings demonstrate that soil ciliate communities may be used as a useful indicator to evaluate the effects of the ecological restoration quality of GFG.

Graphical abstract

Keywords

Soil ciliates / Grain for green / Soil physical-chemical factors / Vegetation community characteristics

References

[1] Abraham, J.S., Sripoorna, S., Dagar, J., Jangra, S., Kumar, A., Yadav, K., Singh, S., Goyal, A., Maurya, S., Gambhir, G., Toteja, R., Gupta, R., Singh, D.K., El-Serehy, H.A., Al-Misned, F.A., Al-Farraj, S.A., Al-Rasheid, K.A., Maodaa, S.A., Makhija, S., 2019. Soil ciliates of the Indian Delhi Region: Their community characteristics with emphasis on their ecological implications as sensitive bio-indicators for soil quality. Saudi Journal of Biological Sciences 26, 1305–1313

[2] Adl, S.M., Bass, D., Lane, C.E., Lukes, J., Schoch, C.L., Smirnov, A., Agatha, S., Berney, C., Brown, M.W., Burki, F., Cárdenas, P., Čepička, I., Chistyakova, L., Campo, J., Dunthorn, M., Edvardsen, B., Eglit, Y., Guillou, L., Hampl, V., Heiss, A.A., Hoppenrath, M., James, T.Y., Karnkowska, A., Karpov, S., Kim, E., Kolisko, M., Kudryavtsev, A., Lahr, D.J.G., Lara, E., Le Gall, L., Lynn, D.H., Mann, D.G., Massana, R., Mitchell, E.A.D., Morrow, C., Park, J.S., Pawlowski, J.W., Powell, M.J., Richter, D.J., Rueckert, S., Shadwick, L., Shimano, S., Spiegel, F.W., Torruella, G., Youssef, N., Zlatogursky, V., Zhang, Q., 2019. Revisions to the classification, nomenclature, and diversity of eukaryotes. Journal of Eukaryotic Microbiology 66, 4–119

[3] Berger, H., 1999. Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Springer Netherlands.

[4] Berger, H., 2011. Monograph of the Gonostomatidae and Kahliellidae (Ciliophora, Hypotricha). Springer Netherlands.

[5] Bremner, J., 1960. Determination of nitrogen in soil by the Kjeldahl method. Journal of Agricultural Science 55, 11–33

[6] Buonanno, F., Ortenzi, C., 2010. The protozoan toxin climacostol and its derivatives: Cytotoxicity studies on 10 species of free-living ciliates. Biologia 65, 675–680

[7] Burton, K.L., Mark, D.E., 2001. Species diversity of bats (Mammalia: Chiroptera) in Iwokrama forest, Guyana, and the Guianan subregion: implications for conservation. Biodiversity and Conservation 10, 613–657

[8] Chang, R.Y., Fu, B.J., Liu, G.H., Wang, S., Yao, X.L., 2012. The effects of afforestation on soil organic and inorganic carbon: A case study of the Loess Plateau of China. Catena 95, 145–152

[9] Chauvat, M., Titsch, D., Zaytsev, A.S., Wolters, V., 2011. Changes in soil faunal assemblages during conversion from pure to mixed forest stands. Forest Ecology and Management 262, 317–324

[10] Chen, X.Y., Xue, W.F., Xue, J.G., Griffiths, B.S., Liu, M.Q., 2020. Contribution of bacterivorous nematodes to soil resistance and resilience under copper or heat stress. Soil Ecology Letters 2, 220–229

[11] Cui, B.S., Zhao, H., Li, X., Zhang, K.J., Ren, H.L., Bai, J.H., 2010. Temporal and spatial distributions of soil nutrients in Hani terraced paddy fields, southwestern China. Procedia Environmental Sciences 2, 1032–1042

[12] Davidson, E.A., Belk, E.L., Boone, R.D., 1998. Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biology 4, 217–227

[13] Domonell, A., Brabender, M., Nitschea, F., Bonkowski, M., Arndt, H., 2013. Community structure of cultivable protists in different grassland and forest soils of Thuringia. Pedobiologia 56, 1–7

[14] Editorial Committee of Chinese Flora of Chinese Academy of Sciences, 1993. Flora Reipublicae Popularis Sinicae. Beijing: Science Press.

[15] Feng, D.R., Wang, J.M., Fu, M.C., Liu, G.C., Zhang, M., Tang, R.B., 2019. Spatiotemporal variation and influencing factors of vegetation cover in the ecologically fragile areas of China from 2000 to 2015: a case study in Shaanxi Province. Environmental Science and Pollution Research International 26, 28977–28992

[16] Fiore-Donno, A.M., Richter-Heitmann, T., Degrune, F., Dumack, K., Regan, K.M., Marhan, S., Boeddinghaus, R.S., Rillig, M.C., Friedrich, M.W., Kandeler, E., Bonkowski, M., 2019. Functional traits and spatio-temporal structure of a major group of soil protists (Rhizaria: Cercozoa) in a temperate grassland. Frontiers in Microbiology 10, 1332–1346

[17] Foissner, W., 1992. Estimating the species richness of soil protozoa using the “non-flooded Petri dish method”. Netherlands Springer.

[18] Foissner, W., 1993. Colpodea (Ciliophora). New York Dieter M.

[19] Foissner, W., 1998. An updated compilation of world soil ciliates (Protozoa, Ciliophora), with ecological notes, new records, and descriptions of new species. European Journal of Protistology 34, 195–235

[20] Foissner, W., 1999. Soil protozoa as bioindicators: pros and cons, methods, diversity, representative examples. Agriculture, Ecosystems & Environment 74, 95–112

[21] Gabilondo, R., Blanco, S., Fernández-Montiel, I., García, D.A., Bécares, E., 2018. Ciliates as bioindicators of CO₂ in soil. Ecological Indicators 85, 1192–1203

[22] Geisen, S., Koller, R., Hünninghaus, M., Dumack, K., Urich, T., Bonkowski, M., 2016. The soil food web revisited: Diverse and widespread mycophagous soil protists. Soil Biology & Biochemistry 94, 10–18

[23] Hao, B.B., Cao, S.P., Li, Y., Liu, J., Qiang, D.H., Liu, C.H., 2020. Temporal and spatial changes of soil animals in returning farmland to forestland in different years in Wuqi County. Journal of Arid Land Resources and Environment 34, 130–136.

[24] Heger, T.J., Straub, F., Mitchell, E.A.D., 2012. Impact of farming practices on soil diatoms and testate amoebae: A pilot study in the DOK-trial at Therwil, Switzerland. European Journal of Soil Biology 49, 31–36

[25] Jackson, M.L., 1973. Soil Chemical Analysis. Prentice Hall of India Pvt. Ltd.

[26] Kai, V., Jaanus, P., 1999. Diversity of bryophyte vegetation in some forest types in Estonia: a comparison of old un-managed and managed forests. Biodiversity and Conservation 8, 1595–1620

[27] Kosiba, J., Wilk-Woz’niak, E., Krztoń, W., 2019. The effect of potentially toxic cyanobacteria on ciliates (Ciliophora). Hydrobiologia 827, 325–335

[28] Li, W.Q., Chen, J.H., Zhang, Z.M., 2020. Forest quality-based assessment of the returning farmland to forest program at the community level in SW China. Forest Ecology and Management 461, 1–12

[29] Lin, B., Zhao, X.R., Zheng, Y., Qi, S., Liu, X.Z., 2017. Effect of grazing intensity on protozoan community, microbial biomass, and enzyme activity in an alpine meadow on the Tibetan Plateau. Journal of Soils and Sediments 17, 2752–2762

[30] Lin, D.S., Greenwood, P.F., George, S., Somerfield, P.J., Tibbett, M., 2011. The development of soil organic matter in restored biodiverse Jarrah forests of South-Western Australia as determined by ASE and GCMS. Environmental Science and Pollution Research International 18, 1070–1078

[31] Liu, J., Yang, Q., Siemann, E., Huang, W., Ding, J.Q., 2019. Latitudinal and altitudinal patterns of soil nematode communities under tallow tree (Triadica sebifera) in China. Plant Ecology 220, 965–976

[32] Liu, M.Y., Liu, M.M., Li, P., Yang, J.H., Wang, J., Chang, Q.R., 2020. Variations in soil organic carbon decompositions of different land use patterns on the tableland of Loess Plateau. Environmental Science and Pollution Research International 27, 4337–4352

[33] Liu, N., Ning, Y.Z., Ma, Z.X., He, J.J., 2008. Ecological effects of soil pollution by fluoride on soil protozoa. Journal of Northwest Normal University 44, 83–86.

[34] Liu, T., Yang, L.H., Hu, Z.K., Xue, J.R., Lu, Y.Y., Chen, X.Y., Griffiths, B.S., Whalen, J.K., Liu, M.Q., 2020. Biochar exerts negative effects on soil fauna across multiple trophic levels in a cultivated acidic soil. Biology and Fertility of Soils 56, 597–606

[35] Lüftenegger, G., Foissner, W., Adam, H., 1985. R- and K-selection in soil ciliates: a field and experimental approach. Oecologia 66, 574–579

[36] Luo, X.T., Li, L.F., Wang, C.D., Bourland, W., Lin, X.F., Hu, X.Z., 2017. Morphologic and phylogenetic studies of two hypotrichous ciliates, with notes on morphogenesis in Gastrostyla steinii Engelmann, 1862 (Ciliophora, Hypotrichia). European Journal of Protistology 60, 119–133

[37] Mayzlish, E., Steiberger, Y., 2004. Effects of chemical inhibitors on soil protozoan dynamics in a desert ecosystem. Biology and Fertility of Soils 39, 415–421

[38] Mieczan, T., Adamczuk, M., Pogorzelec, M., 2017. Ciliates as restoration indicators in peatbogs — 10 years of study. European Journal of Protistology 62, 11–23

[39] Mo, L.C., Liu, J.K., Chen, J.C., Xie, Y., 2020. Quantifying ecosystem services of dominate forests in the Beijing mountain area. Environmental Science and Pollution Research International 27, 27773–27785

[40] Ning, Y.Z., Du, H.F., Zou, T., Wang, H.J., 2011a. Toxic effects of ent-kaurane diterpenoids on soil ciliate communities. Acta Ecologica Sinica 31, 183–194.

[41] Ning, Y.Z., Shen, Y.F., 1998a. Soil Protozoa in typical zones of China: I Faunal characteristics and distribution of species. Acta Ecologica Sinica 44, 5–9.

[42] Ning, Y.Z., Shen, Y.F., 1998b. Soil Protozoa in typical zones of China: II Ecological study. Acta Ecologica Sinica 44, 271–276.

[43] Ning, Y.Z., Wan, G.H., Yang, Y.G., Wu, W.N., Zhou, X.Y., Wang, Y.F., Liu, N., Cheng, X., Chen, L.Y., 2019. Community characteristics of soil ciliates in different modes of returning cropland to forest in Hui County, Gansu. Chinese Journal of Ecology 38, 1697–1706.

[44] Ning, Y.Z., Wang, H.J., Yu, J.H., Du, H.F., 2011b. Response of the soil ciliate community to ecological restoration in Huajialing, Dingxi, Gansu. Zoological Research 32, 223–231.

[45] Ning, Y.Z., Wang, T.T., Dong, W.H., Yang, Y.G., Yan, Z.J., 2017a. Community characteristics of spring soil ciliates in forestlands converted from cultivated lands in Qingcheng county of Gansu Province. Journal of Northwest Normal University 53, 88–93.

[46] Ning, Y.Z., Wu, W.N., Du, H.F., Wang, H.J., 2016. Response of soil ciliate communities to ecological restoration after the implementation of the conversion of cropland to forest and grassland program: a case study of Platycladus orientalis forest. Acta Ecologica Sinica 36, 288–297.

[47] Ning, Y.Z., Xu, F.R., Wang, T.T., 2020. Community characteristics of soil ciliates in forestlands converted from cultivated lands in Qingcheng County, Qingyang City. Ecology and Environmental Sciences 29, 506–515.

[48] Ning, Y.Z., Yang, Y.G., Su, C., Chen, L.Y., Du, G.Z., 2017b. Effects of grazing on soil ciliate community in swamp meadow. Chinese Journal of Ecology 36, 1614–1621.

[49] Ning, Y.Z., Yang, Y.Q., Dong, W.H., Zhang, H.R., Ma, J.Y., 2018. Response of soil ciliate community to ecological restoration of different return patterns. Acta Ecologica Sinica 38, 3628–3638.

[50] Northwest Institute of Botany, Chinese Academy of Sciences, 1976. Flora Tsinlingensis. Beijing: Science Press.

[51] Ouyang, Z.W., 2010. Study on Ecological Effects of Different Models of Converting Cropland to Forest and Grass in Karst Peak-cluster-depression Region. Dissertation, Hunan Agricultural University.

[52] Pang, X.Y., Bao, W.K., 2011. Effect of substituting plantation species for native shrubs on the water-holding characteristics of the forest floor on the eastern Tibetan Plateau. Journal of Resources and Ecology 2, 217–224.

[53] Piché, N., Kelting, D.L., 2015. Recovery of soil productivity with forest succession on abandoned agricultural land. Restoration Ecology 23, 645–654

[54] Sabais, A.C.W., Scheu, S., Eisenhauer, N., 2011. Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecologica 37, 195–202

[55] Schulz-Bohm, K., Geisen, S., Wubs, E.R.J., Song, C., Boer, W.D., Garbeva, P., 2016. The prey’s scent–Volatile organic compound mediated interactions between soil bacteria and their protist predators. International Society for Microbial Ecology 16, 1751–7362.

[56] Shang, W., Zhao, L., Wu, X.D., Li, Y.Q., Yue, G.Y., Zhao, Y.H., Qiao, Y.P., 2015. Soil organic matter fractions under different vegetation types in permafrost regions along the Qinghai-Tibet Highway, north of Kunlun Mountains, China. Journal of Mountain Science 12, 1010–1024

[57] Shao, C., Li, L.Q., Zhang, Q.Q., Song, W.B., Bergere, H., 2014a. Molecular phylogeny and ontogeny of a new ciliate genus, Paracladotricha salina n. g. n. sp. (Ciliophora, Hypotrichia). Journal of Eukaryotic Microbiology 64, 901–902

[58] Shao, C., Lu, X.T., Ma, H.G., 2014b. A general overview of the typical 18 frontal-ventral transverse cirri oxytrichidae s. l. genera (Ciliophora, Hypotrichia). Journal of Ocean University of China 14, 522–532

[59] Shen, Y.F., 1999. Protozoology. Science Press, Beijing.

[60] Shen, Y.F., Zhang, Z.H., Gong, X.G., Gu, M.R., Shi, Z.X., Wei, Y.X., 1990. Modern biomonitoring techniques using freshwater microbiota. China Architecture & Building Press, Beijing.

[61] Song, W.B., Xu, K.D., Hu, X.Z., Lei, Y.L., Wei, J., Chen, Z.G., Shi, X.B., Wang, M., 1999. Progress in Protozoology. Qindao Ocean University Press, Qindao.

[62] Vogel, H.J., Roth, K., 2001. Quantitative morphology and network representation of soil pore structure. Advances in Water Resources 24, 233–242

[63] Wan, N.F., Gu, X.J., Ji, X.Y., Jiang, J.X., Wu, J.H., Li, B., 2014. Ecological engineering of ground cover vegetation enhances the diversity and stability of peach orchard canopy arthropod communities. Ecological Engineering 70, 175–182

[64] Wanner, M., Birkhofer, K., Fischer, T., Shimizu, M., Shimano, S., Puppe, D., 2020. Soil testate amoebae and diatoms as bioindicators of an old heavy metal contaminated floodplain in Japan. Microbial Ecology 79, 123–133

[65] Xiong, W., Jousset, A., Guo, S., Karlsson, I., Zhao, Q.Y., Wu, H.S., Kowalchuk, G.A., Shen, Q.R., Li, R., Geisen, S., 2018. Soil protist communities form a dynamic hub in the soil microbiome. International Society for Microbial Ecology 18, 1751–7362

[66] Xue, G.Q., Liu, Q., Ren, X.F., Han, Y.Q., 2004. Determination of fifteen metal elements in Cynomorium songaricum by flame atomic absorption spectrophotometry (FAAS). Spectroscopy and Spectral Analysis 24, 1461–1463.

[67] Yang, Z.B., Jin, H.X., Wang, G., 2010. An assessment of restoration success to forests planted for ecosystem restoration in loess plateau, Northwestern China. Environmental Science and Pollution Research International 164, 357–368.

[68] Yeates, G.W., Bamforth, S.S., Ross, D.J., Tate, K.R., Sparling, G.P., 1991. Recolonization of methyl bromide sterilized soils under four different field conditions. Biology and Fertility of Soils 11, 181–189

[69] Zhang, C., Xue, S., Liu, G.B., Song, Z.L., 2011. A comparison of soil qualities of different revegetation types in the Loess Plateau, China. Plant and Soil 347, 163–178

[70] Zhang, L., Zhao, W., Zhang, R., Cao, H., Tan, W.F., 2018. Profile distribution of soil organic and inorganic carbon following revegetation on the Loess Plateau, China. Environmental Science and Pollution Research International 25, 30301–30314

[71] Zhang, M., Liang, W.J., Zhang, X.K., 2012. Soil nematode abundance and diversity in different forest types at Changbai mountain, China. Zoological Studies (Taipei) 51, 619–626.

[72] Zhang, Z.L., Li, N., Xiao, J., Zhao, C.Z., Zou, T.T., Li, D.D., Liu, Q., Yin, H.J., 2018. Changes in plant nitrogen acquisition strategies during the restoration of spruce plantations on the eastern Tibetan Plateau, China. Soil Biology & Biochemistry 119, 50–58

[73] Zhou, J.H., Hu, F., Jiao, J.G., Liu, M.Q., Li, H.X., 2012. Effects of bacterial-feeding nematodes and prometryne-degrading bacteria on the dissipation of prometryne in contaminated soil. Journal of Soils and Sediments 12, 576–585

[74] Zou, T., Shen, H.X., Ning, Y.Z., Ma, Z.X., 2009. Community characteristics of soil ciliates in the Mayan Forest Region of Xiaolong Mountains, Gansu. Chinese Journal of Zoology 44, 64–73.

Conflicts of interest

Authors declare that they have no competing interests.

Acknowledgments

Thanks to professor Henglong Xu from Ocean University of China for revising the abstract of this article. Thanks to Alan Warren, a protozoology expert and senior researcher at the Natural History Museum, London, UK, for providing guidance on the full text. This work was supported by the National Natural Science Foundation of China (Project number: 41761056, 41361055, 42067012).

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