Biocrusts impact soil properties and ecological stoichiometry characteristics in frozen ground regions on the Qinghai-Tibet Plateau

Highlights

● Biocrusts are one of the most important components of the land cover in frozen ground regions on the Qinghai–Tibet Plateau, which increased the silt particle content, enhanced field moisture capacity, and reduced soil bulk density.

● Biocrusts significantly increased levels of SOC (22.6−30.8 g kg⁻¹) and TN (2.1−2.8 g kg⁻¹) within the 0–40 cm soil layer, while they had no significant influence on the TP contents.

● Biocrusts also had influence on the stoichiometry characteristics, and the C/N, C/P and N/P ratios of the biocrusts were all higher than that of the bare land, which revealed that biocrusts enhanced the contents of SOC and TN in presuccessional period of biocrusts and reduced the availability of P in their postsuccessional period.

Abstract

Biocrusts (BSCs) are widely distributed in frozen ground regions on the Qinghai-Tibet Plateau, and they are considered an important component of cold ecosystems. However, the specific impacts of BSCs on frozen soil remains relatively unclear. The aim of our study was to clarify the influence of BSCs (light BSCs and dark BSCs in two different succession stages) on the physical properties and ecological stoichiometry characteristics of frozen soil. Our results showed that BSCs increased the silt particle content in 20–40 cm soil layer, leading to a decrease in soil bulk density. And the field water capacity increased about 10%–40% compared to bare land. Additionally, BSCs significantly increased the contents of soil organic carbon (SOC, 22.6–30.8 g kg⁻¹) and total nitrogen (TN, 2.1–2.8 g kg⁻¹) in the upper 40 cm soil layer, both of them were approximately 1.3–2.0 and 1.3–4.0 times higher than those observed in bare land. However, BSCs did not have significant influence on soil total phosphorus (TP). BSCs had a significant impact on the stoichiometric ratios within 40 cm. The C/N ratios of the two types of BSCs ranged from 8.8 to 13.5, the C/P ratios ranged from 6.6 to 13.8, and the N/P ratios ranged from 0.6 to 1.2, which were all higher than those of the bare land. There were no significant differences among the C/N, C/P, and N/P ratios between two types of BSCs. However, the increment of C/P and N/P ratios of dark BSCs were significantly higher than those of light BSCs within 0–30 cm, which indicated that a reduction in the availability of phosphorus during the later stages of BSCs succession. These findings provided a theoretical basis for further research on the ecological functions of BSCs in frozen ground regions.

Graphical abstract

Keywords

biocrusts / frozen soil / soil properties / stoichiometry characteristics / Qinghai-Tibet Plateau

References

[1] Aranibar, J.N., Anderson, I.C., Ringrose, S., Macko, S.A., 2003. Importance of nitrogen fixation in soil crusts of southern African arid ecosystems: acetylene reduction and stable isotope studies. Journal of Arid Environments54, 345–358.

[2] Bai, J.B., Xu, X.L., Song, M.H., He, Y.T., Jiang, J., Shi, P.L., 2011. Effect of temperature and added nitrogen on carbon mineralization in alpine soil on the Tibetan Plateau. Ecology and Environmental Sciences20, 855–859.

[3] Baumann, K., Jung, P., Samolov, E., Lehnert, L.W., Büdel, B., Karsten, U., Bendix, J., Achilles, S., Schermer, M., Matus, F., Oses, R., Osses, P., Morshedizad, M., Oehlschläger, C., Hu, Y.F., Klysubun, W., Leinweber, P., 2018. Biological soil crusts along a climatic gradient in Chile: Richness and imprints of phototrophic microorganisms in phosphorus biogeochemical cycling. Soil Biology and Biochemistry127, 286–300.

[4] Belnap, J., Lange, O.L., 2001. Biological Soil Crusts: Structure, Function, and Management. Springer-Verlage, Berlin, p. 503

[5] Belnap, J., 2003. Comparative Structure of Physical and Biological Soil Crusts. In: Belnap, J., Lange, O.L., eds. Biological Soil Crusts: Structure, Function, and Management, Springer-Verlage, Berlin, pp. 177–191.

[6] Belnap, J., 2011. Biological Phosphorus Cycling in Dryland Regions. In: Bünemann, E., Oberson, A., Frossard, E., eds. Phosphorus in Action. Soil Biology, vol 26. Springer, Berlin, Heidelberg

[7] Belnap, J., Büdel, B., 2016. Biological Soil Crusts as an Organizing Principle in Drylands. In: Weber, B., Büdel, B., Belnap, J., eds. Biological Soil Crusts: An Organizing Principle in Drylands. Springer, Cham, Switzerland (outside the USA), pp. 3–13

[8] Beymer, R.J., Klopateak, J.M., 1991. Potential contribution of carbon by microphytic crusts in pinyon-juniper woodlands. Arid Soil Research and Rehabilitation5, 187–198.

[9] Bowker, M.A., Eldridge, D.J., Val, J., Soliveres, S., 2013. Hydrology in a patterned landscape is co-engineered by soil-disturbing animals and biological crusts. Soil Biology and Biochemistry61, 14–22.

[10] Breen, K., Lévesque, E., 2008. The influence of biological soil crusts on soil characteristics along a high arctic glacier foreland, Nunavut, Canada. Arctic, Antarctic, and Alpine Research40, 287–297.

[11] Büdel, B., Dulić, T., Darienko, T., Friedl, T., 2016. Cyanobacteria and Algae of Biological Soil Crusts. In: Weber, B., Büdel, B., Belnap, J. (eds.), Biological Soil Crusts: An Organizing Principle in Drylands. Springer, Cham, Switzerland (outside the USA). pp. 55–80

[12] Chamizo, S., Cantón, Y., Rodríguez–Caballero, E., Domingo, F., Escudero, A., 2012a. Runoff at contrasting scales in a semiarid ecosystem: a complex balance between biological soil crust features and rainfall characteristics. Journal of Hydrology (Amsterdam) 452–453, 130–138

[13] Chamizo, S., Cantón, Y., Miralles, I., Domingo, F., 2012b. Biological soil crust development affect physicochemical characteristics of soil surface in semiarid ecosystems. Soil Biology and Biochemistry49, 96–105.

[14] Chapuis-Lardy, L., Le Bayon, R.C., Brossard, M., López-Hernández, D., Blanchart, E., 2011. Role of soil macrofauna in phosphorus cycling. In: Bünemann, E., Oberson, A., Frossard, E., eds. Phosphorus in Action. Soil Biology, vol 26. Springer, Berlin, Heidelberg.

[15] Cui, X.Q., 2018. Effects of enhanced precipitation, temperature and nitrogen addition on nitrogen fate and plant stoichiometry in temperate desert ecosystem in Xinjiang. Beijing, China Agricultural University

[16] DeLuca, T.H., Zackrisson, O., Gentili, F., Sellstedt, A., Nilsson, M.C., 2007. Ecosystem control son nitrogen fixation in boreal feather moss communities. Oecologia152, 121–130.

[17] Drahorad, S., Felix–Henningsen, P., Eckhardt, K.U., Leinweber, P., 2013. Spatial carbon and nitrogen distribution and organic matter characteristics of biological soil crusts in the Negev desert (Israel) along a rainfall gradient. Journal of Arid Environments94, 18–26.

[18] Fang, S.B., Feng, L., Liu, H.J., Zhang, X.S., Liu, J.D., 2008. Responses of biological soil crusts (BSC) from arid-semiarid habitats and polar region to global climate change. Acta Ecologica Sinica28, 3312–3321.

[19] Feng, W., 2014. Photosythetic carbon fixation of biological soil crusts in MU US desert and their impact on soil carbon emission. Beijing: Beijing Forestry University

[20] Gao, L.Q., 2012. The Effect and it’s Mechanism of Biological Soil Crusts on Soil Erodibility. Yangling, Research Center of Soil and Water Conservation and Ecological Environment Chinese Academy of Science and Ministry of Water Resources

[21] Gao, L.Q., Zhao, Y.G., Qin, N.Q., Zhang, G.X., Yang, K., 2012. Impact of biological soil crust on soil physical properties in the Hilly Loess Plateau Region, China. Journal of Natural Resources27, 1316–1324.

[22] Gao, L.Q., Zhao, Y.G., Xu, M.X., Sun, H., Yang, Q.Y., 2017. The effects of biological soil crust succession on soil ecological stoichiometry characteristics. Acta Ecologica Sinica38, 678–688.

[23] Gómez, D.A., Aranibar, J.N., Tabeni, S., Villagra, P.E., Garibotti, I.A., Atencio, A., 2012. Biological soil crust recovery after long-term grazing exclusion in the Monte Desert (Argentina). Changes in coverage, spatial distribution, and soil nitrogen. Acta Oecologica38, 33–40.

[24] Gong, X.Q., Wu, G.J., Zhang, C.L., Zhang, X.L., Xu, T.L., 2012. Dust change over the Tibetan Plateau in recent years using ice core records and satellite remote sensing data. Journal of Glaciology and Cryopedology34, 257–266.

[25] Guo, J.P., Liu, H., An, L.C., Wang, P.X., Gao, M., 2016. Study on variation of snow cover and its orographic impact over Qinghai-Xizang Plateau during 2001–2012. Plateau Meteorology35, 24–33.

[26] Guo, Y.R., Zhao, H.L., Zuo, X.A., Drake, S., Zhao, X.Y., 2008. Biological soil crust development and its topsoil properties in the process of dune stabilization, Inner Mongolia, China. Environmental Geology54, 653–662.

[27] Housman, D.C., Powers, H.H., Collins, A.D., Belnap, J., 2006. Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert. Journal of Arid Environments66, 620–634.

[28] Jiang, Z.Y., Li, X.Y., Wei, J.Q., Chen, H.Y., Li, Z.C., Liu, L., Hu, X., 2018. Contrasting surface soil hydrology regulated by biological and physical soil crusts for patchy grass in the high–altitude alpine steppe ecosystem. Geoderma326, 201–209.

[29] Jin, H.J., Wang, S.L., Lv, L.Z., He, R.X., Chang, X.L., Luo, D.L., 2010. Features and degradation of frozen ground in the sources area of the Yellow River, China. Journal of Glaciology and Cryopedology32, 10–17.

[30] Jones, D., Wilson, M.J., 1985. Chemical activity of lichens on mineral surfaces. A review. International Biodeterioration21, 99–104.

[31] Kakeh, J., Gorji, M., Sohrabi, M., Tavili, A., Pourbabaee, A.A., 2018. Effect of biological soil crusts on some physicochemical characteristics of rangeland soils of Alagol, Turken Sahra, NE Iran. Soil and Tillage Research181, 152–159.

[32] Lange, O.L., 1980. Moisture content and CO₂ exchange of lichens. Oecologia45, 82–87.

[33] Li, Y.K., Ouyang, J.Z., Lin, L., Zhang, F.W., Du, Y.G., Gao, G.M., Han, F., 2015. Evolution characteristics of biological soil crusts (BSCs) during alpine meadow degradation. Acta Ecologica Sinica34, 2238–2244.

[34] Lin, Y.Q., Qu, J.J., 1993. Crust development and changes of micro- environment on sand surface. Chinese Journal of Applied Ecology4, 393–398.

[35] Liu, Y.M., Li, X.R., Xing, Z.S., Zhao, X., Pan, Y.X., 2013. Responses of soil microbial biomass and community composition to biological soil crusts in the revegetated areas of the Tengger Desert. Applied Soil Ecology65, 52–59.

[36] Luo, D.L., Jin, H.J., Jin, X.Y., He, R.X., Li, X.Y., Muskett, R.R., Marchenko, S., Romanovsky, V.E., 2018. Elevation-dependent thermal regime and dynamics of frozen ground in the Bayan Har Mountains, northeastern Qinghai–Tibet Plateau, southwest China. Permafrost and Periglacial Processes29, 257–270.

[37] Luo, D.L., Jin, H.J., Lv, L.Z., Wu, Q.B., 2014. Spatial and temporal characteristics of freezing-thawing process of permafrost and seasonal permafrost in the source area of the Yellow River. Chinese Science Bulletin59, 3034–3045.

[38] Luo, Y.Y., Zhang, Y., Zhang, J.H., Ka, Z.J., Shang, L.Y., Wang, S.Y., 2012. Soil stoichiometry characteristics of alpine meadow at its different degradation stages. Chinese Journal of Ecology31, 254–260.

[39] Ming, J., 2013. Potential Nitrogenase activity of biological soil crusts from different erosion regions on the Loess Plateau, China. Yangling, Research Center of Soil and Water Conservation and Ecological Environment Chinese Academy of Science and Ministry of Water Resources

[40] Ming, J., Kong, L.Y., Zhao, Y.G., Du, Y.X., 2020. Effects of biological soil crusts on soil water-heat process of shallow soil layer in the frozen ground region on Qinghai-Tibet Plateau. Acta Ecologica Sinica40, 6385–6395.

[41] Ming, J., Sheng, Y., Jin, H.J., Zhang, Z., Du, Y.X., 2021. The impact of the biological soil crusts on the frozen soil properties of in the frozen ground region. Journal of Glaciology and Cryopedology43, 601–609.

[42] Ming, J., Zhao, Y.G., Wu, Q.B., He, H.L., Gao, L.Q., 2022. Soil temperature dynamics and freezing processes for biocrustal soils in frozen soil regions on the Qinghai-Tibet Plateau. Geoderma409, 115655.

[43] Miralles, I., Domingo, F., García-Campos, E., Trasar-Cepeda, C., Carmen Leirós, M., Gil-Sotres, F., 2012. Biological and microbial activity in biological soil crusts from the Tabernas desert, a sub-arid zone in SE Spain. Soil Biology and Biochemistry,55, 113–121.

[44] Ochoa-Hueso, R., Maestre, F.T., de los Ríos, A., Valea, S., Theobald, M.R., Vivanco, M.G., Manrique, E., Bowker, M.A., 2013. Nitrogen deposition alters nitrogen cycling and reduces soil carbon content in low-productivity semiarid Mediterranean ecosystems. Environmental Pollution179, 185–193.

[45] Qiu, D.X., Bowker, M.A., Xiao, B., Zhao, Y.G., Zhou, X.B., Li, X.R., 2023. Mapping biocrust distribution in China’s drylands under changing climate. Science of the Total Environment905, 167211.

[46] Quiquanpoix, H., Mousain, D., 2005. Enzymatic Hydrolysis of Organic Phosphorus. In: Frossard, E., Baldwin, D., Turner, B.L., eds. Organic Phosphorus in the Environment. CABI Publishing, Wallingford. pp. 89–112

[47] Rodríguez-Caballero, E., Cantón, Y., Chamizo, S., Afana, A., Solé-Benet, A., 2012. Effects of biological soil crusts on surface roughness and implications for runoff and erosion. Geomorphology 145–146, 81–89

[48] Serpe, M.D., Roberts, E., Eldridge, D.J., Rosentreter, R., 2013. Bromus tectorum litter alters photosynthetic characteristics of biological soil crusts from a semiarid shrubland. Soil Biology and Biochemistry60, 220–230.

[49] Souza-Egipsy, V., Wierzchos, J., Sancho, C., Belmonte, Á., Ascaso, C., 2010. Role of biological soil crust cover in bioweathering and protection of sandstones in a semi-arid landscape (Torrollones de Gabarda, Huesca, Spain). Earth Surface Processes and Landforms29, 1651–1661.

[50] Stark, L.R., Brinda, J.C., McLetchie, D.N., 2011. Effects of increased summer precipitation and N deposition on Mojave Desert populations of the biological crust moss Syntrichia caninervis. Journal of Arid Environments75, 457–463.

[51] Sterner, R.W., Elser, J.J., 2002. Ecological stoichiometry: The Biology of Elements from Molecules to the Biosphere. Quarterly Review of Biology, Princeton: Princeton University Press Princeton

[52] Su, Y.G., Zhao, X., Li, A.X., 2011. Nitrogen fixation in biological soil crusts from the Tengger Desert, northern China. European Journal of Soil Biology47, 182–187.

[53] Su, Y.G., Wu, L., Zhang, Y.M., 2012. Characteristics of carbon flux in two biologically crusted soils in the Gurbantunggut Desert, Northwestern China. Catena96, 41–48.

[54] Thompson, T.L., Zaady, E., Huancheng, P., Wilson, T.B., Martens, D.A., 2006. Soil C and N pools in patchy shrublands of the Negev and Chihuahuan Deserts. Soil Biology and Biochemistry38, 1943–1955.

[55] Türk, R., Gärtner, G., 2001. Biological Soil Crusts of the Subalpine, Alpine, and Nival Areas in the Alps. In: Belnap, J., Lange, O.L., eds. Biological Soil Crusts: Structure, Function, and Management, pp. 67–73

[56] Wang, A.G., 2013. Effect of Biological soil crust on soil CO₂ flux in different erosion region on the Loess Plateau. Yangling, Northwest Agricultural and Forest University

[57] Wang, G.X., Li, Y.S., Wu, Q.B., Wang, Y.B., 2006. Impacts of permafrost changes on alpine ecosystem in Qinghai–Tibet Plateau. Science in China. Series D, Earth Sciences49, 1156–1169.

[58] Wang, J.L., Zhong, Z.M., Wang, Z.H., Yu, C.Q., Shen, Z.X., Zhang, X.Z., Hu, X.X., Da-Ci, Z.G., 2014. Soil C/P distribution characteristics of alpine steppe ecosystems in the Qinghai-Tibetan Plateau. Acta Prataculturae Sinica23, 9–19.

[59] Wang, S.Q., Yu, G.R., 2008. Ecological stoichiometry characteristics of ecosystem carbon, nitrogen and phosphorus elements. Acta Ecologica Sinica28, 3937–3947.

[60] Wang, Y.S., Cheng, C.C., Xie, Y., Liu, B.Y., Yin, S.Q., Liu, Y.N., Hao, Y.F., 2017. Increasing trends in rainfall-runoff erosivity in the Source Region of the Three Rivers, 1961–2012. Science of the Total Environment592, 639–648.

[61] Weber, B., Belnap, J., Büdel, B., Antoninka, A.J., Barger, N.N., Chaudhary, V.B., Darrouzet-Nardi, A., Eldridge, D.J., Faist, A.M., Ferrenberg, S., Havrilla, C.A., Huber-Sannwald, E., Malam Issa, O., Maestre, F.T., Reed, S.C., Rodriguez-Caballeroet, E., Tucker, C., Young, K.E., Zhang, Y.M., Zhou, X.B., Bowker, M.A., 2022. What is a biocrust? A refined, contemporary definition for a broadening research community. Biological Reviews of the Cambridge Philosophical Society97, 1768–1785.

[62] Wu, Q.B., Shi, B., 2002. Discussion on the environmental protection of frozen soil during the Qinghai-Tibet railway construction. Hydrogeology and Engineering Geology45, 14–17.

[63] Xiao, B., Wang, H.F., Fan, J., Fischer, T., Veste, M., 2013. Biological soil crusts decrease soil temperature in summer and increase soil temperature in winter in semiarid environment. Ecological Engineering58, 52–56.

[64] Xiao, B., Zhao, Y.G., Shao, M.A., 2007a. Effects of biological soil crust on saturated hydraulic conductivity in water-wind erosion crisscross region, North of Shaanxi Province, China. Transactions of the Chinese Society of Agricultural Engineering23, 35–40.

[65] Xiao, B., Zhao, Y.G., Shao, M.A., 2007b. Effects of biological soil crust on soil physicochemical properties in water-wind erosion crisscross region, northern Shaanxi Province, China. Acta Ecologica Sinica27, 4662–4670.

[66] Xue, X., Guo, J., Zhang, F., Zong, L., Han, B.S., Huang, C.H., 2007. Development and cause of aeolian desertification in alpine region—In case of Maduo County in Yellow River source area. Journal of Desert Research27, 725–732.

[67] Yang, C.D., Long, R.J., Chen, X.R., Xu, C.L., Wang, J.M., 2008. Characteristics of carbon, nitrogen and phosphorus density in top soil under different alpine grasslands on the Eastern Qilian Mountains. Chinese Journal of Grassland30, 1–5.

[68] Yang, M.X., Yao, T.D., Nozomu, H., Fujii, H., 2006. Daily freezing-thawing cycle of surface soil in Qinghai-Tibet Plateau. Chinese Science Bulletin51, 1974–1976.

[69] Yang, L.N., Zhao, Y.G., Ming, J., Wang, A.G., 2013. Cyanobacteria diversity in biological soil crusts from different erosion regions on the Loess Plateau: a preliminary result. Acta Ecologica Sinica33, 4416–4424.

[70] Zhang, G.X., 2012. Mechanism of the effect of biological soil crust on the availability of phosphorous in the Hilly Loess Plateau Region, China. Yangling: Northwest A &F University

[71] Zhang, T., Armstrong, R.L., Smith, J., 2003. Investigation of the near-surface soil freeze–thaw cycle in the contiguous United States: algorithm development and validation. Journal of Geophysical Research Atomspheres 108, GCP 21-1–21-14.

[72] Zhang, Z., Ma, W., Feng, W.J., Xiao, D.H., Hou, X., 2016. Reconstruction of soil particle composition during freeze-thaw cycling: A review. Pedosphere26, 167–179.

[73] Zhang, Z., Ma, W., Qi, J.L., 2013. Structure evolution and mechanism of engineering properties change of soils under effect of freeze-thaw cycle. Journal of Jilin University (Earth Science Edition)46, 1904–1914.

[74] Zhao, H.L., Guo, Y.R., Zhou, R.L., Drake, S., 2010. Biological soil crust and surface soil properties in different vegetation types of Horqin Sand Land, China. Catena82, 70–76.

[75] Zhao, Y.G., Qin, N.Q., Weber, B., Xu, M.X., 2014. Response of biological soil crusts to raindrop erosivity and underlying influences in the Hilly Loess Plateau region, China. Biodiversity and Conservation23, 1669–1686.

[76] Zhong, L., Ma, Y., Salama, M.S., Su, B., 2010. Assessment of vegetation dynamics and their response to variations in precipitation and temperature in the Tibetan Plateau. Climatic Change103, 519–535.

[77] Zhou, X., Zhang, Y., Downing, A., 2012. Non-linear response of microbial activity across a gradient of nitrogen addition to a soil from the Gurbantunggut Desert, northwestern China. Soil Biology and Biochemistry47, 67–77.

[78] Zhu, G.L., 2017. Alpine grassland in Tibetan soil organic matter decomposition along an altitudinal transect under simulation of temperature changes. Linzhi, Tibet: Institute of Tibet Plateau Ecology

[79] Zou, D.F., Zhao, L., Sheng, Y., Chen, J., Hu, G.J., Wu, T.H., Wu, J.C., Xie, C.W., Wu, X.D., Pang, Q.Q., Wang, W., Du, E.J., Liu, W., Liu, G., Li, J., Qin, Y., Qiao, Y., Wang, Z., Shi, J., Cheng, G., 2016. A new map of permafrost distribution on the Tibetan Plateau. The Cryosphere11, 2527–2542.

Conflict of interest

No conflict of interest exits in the submission of this manuscript.

Acknowledgments

This work was jointly supported by the National Natural Science Foundation of China (Grant No. 41601072) and the Key Project of National Natural Science Foundation of China (Grant No. 41830758). We express our gratitude to the Prof. Yu Sheng, Dr. Dongliang Luo, Yuzhong Yang and Yongyong Zhang for the helpful comments on this manuscript. We are grateful to thank Dr. Murphy Stephen of the Yale University for his helpful guidance in language and grammatical editing of this manuscript.

RIGHTS & PERMISSIONS

2023 Higher Education Press