Effects of snow absence on available N pools and enzyme activities within soil aggregates in a spruce forest on the eastern Tibetan Plateau

Highlights

• Snow absence increased soil N availabilities within soil aggregates.

• Snow absence did not change net N mineralization rate within soil aggregates.

• Soil enzyme activities affected by snow were different within soil aggregates.

Abstract

Winter climate change has great potential to affect the functioning of terrestrial ecosystems. In particular, increased soil frost associated with reduced insulating snow cover may impact the soil nitrogen (N) dynamics in cold ecosystems, but little is known about the variability of these effects among the soil aggregates. A snow manipulation experiment was conducted to investigate the effects of snow absence on N cycling within soil aggregates in a spruce forest on the eastern Tibetan Plateau of China. The extractable soil available N (ammonium and nitrate), net N mineralization rate, and N cycling-related enzyme activities (urease, nitrate reductase, and nitrite reductase) were measured in large macroaggregate (>2 mm), small macroaggregate (0.25–2 mm), and microaggregate (<0.25 mm) during the early thawing period in the years of 2016 and 2017. Snow absence increased soil N availabilities and nitrite reductase activity in microaggregate, but did not affect net N mineralization rate, urease or nitrate reductase activities in any of the aggregate fractions. Regardless of snow manipulations, both soil inorganic N and nitrate reductase were higher in small macroaggregate than in the other two fractions. The effect of aggregate size and sampling year was significant on soil mineral N, net N mineralization rate, and nitrite reductase activity. Our results indicated that snow cover change exerts the largest impact on soil N cycling within microaggregate, and its effect is dependent on winter conditions (e.g., snow cover and temperature). Such findings have important implications for soil N cycling in snow-covered subalpine forests experiencing pronounced winter climate change.

Graphical abstract

Keywords

Ammonium / Climate change / Forest / N mineralization / Nitrate / Snow absence

References

[1] Allison, S.D., Jastrow, J.D., 2006. Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biology & Biochemistry 38, 3245–3256

[2] An, S., Mentler, A., Mayer, H., Blum, W.E., 2010. Soil aggregation, aggregate stability, organic carbon and nitrogen in different soil aggregate fractions under forest and shrub vegetation on the Loess Plateau, China. Catena 81, 226–233

[3] Aon, M., Colaneri, A., 2001. II. Temporal and spatial evolution of enzymatic activities and physico-chemical properties in an agricultural soil. Applied Soil Ecology 18, 255–270

[4] Bach, E.M., Hofmockel, K.S., 2014. Soil aggregate isolation method affects measures of intra-aggregate extracellular enzyme activity. Soil Biology & Biochemistry 69, 54–62

[5] Ballesteros-Cánovas, J.A., Trappmann, D., Madrigal-González, J., Eckert, N., Stoffel, M., 2018. Climate warming enhances snow avalanche risk in the Western Himalayas. Proceedings of the National Academy of Sciences of the United States of America 115, 3410–3415

[6] Barnett, T.P., Adam, J.C., Lettenmaier, D.P., 2005. Potential impacts of a warming climate on water availability in snow-dominated regions. Nature 438, 303–309

[7] Dorodnikov, M., Blagodatskaya, E., Blagodatsky, S., Marhan, S., Fangmeier, A., Kuzyakov, Y., 2009. Stimulation of microbial extracellular enzyme activities by elevated CO₂ depends on soil aggregate size. Global Change Biology 15, 1603–1614

[8] Durán, J., Rodríguez, A., Morse, J.L., Groffman, P.M., 2013. climate change effects on soil C and N cycles in urban grasslands. Global Change Biology 19, 2826–2837

[9] Edwards, L.M., 1991. The effect of alternate freezing and thawing on aggregate stability and aggregate size distribution of some Prince Edward Island soils. Journal of Soil Science 42, 193–204

[10] Edwards, L.M., 2013. The effects of soil freeze–thaw on soil aggregate breakdown and concomitant sediment flow in Prince Edward Island: A review. Canadian Journal of Forest Research 93, 459–472.

[11] Fang, X., Zhou, G., Li, Y., Liu, S., Chu, G., Xu, Z., Liu, J., 2016. Warming effects on biomass and composition of microbial communities and enzyme activities within soil aggregate in subtropical forest. Soil & Tillage Research 52, 353–365.

[12] Fansler, S.J., Smith, J.L., Bolton, H. Jr, Bailey, V.L., 2005. Distribution of two C cycle enzymes in soil aggregate of a prairie chronosequence. Biology and Fertility of Soils 42, 17–23

[13] Freppaz, M., Celi, L., Marchelli, M., Zanini, E., 2008. Snow removal and its influence on temperature and N dynamics in alpine soils (Vallee d’Aoste, northwest Italy). Journal of Plant Nutrition and Soil Science 171, 672–680

[14] Guggenberger, G., Elliott, E.T., Frey, S.D., Six, J., Paustian, K., 1999. Microbial contributions to the aggregation of a cultivated grassland soil amended with starch. Soil Biology & Biochemistry 131, 407–419

[15] Gupta, V., Germida, J., 1988. Distribution of microbial biomass and its activity in different soil aggregate size classes as affected by cultivation. Soil Biology & Biochemistry 20, 777–786

[16] IUSS Working Group, 2007. World Reference Base for Soil Resources 2006. First Update 2007. World Soil Resources Reports No. 103. FAO, IT EU, Rome.

[17] Jiao, S., Li, J., Li, Y., Xu, Z., Kong, B., Li, Y., Shen, Y., 2020. Variation of soil organic carbon and physical properties in relation to land uses in the Yellow River Delta, China. Scientific Reports 10, 1–12

[18] Kandeler, E., Gerber, H., 1988. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils 6, 68–72

[19] Kristiansen, S.M., Schjønning, P., Thomsen, I.K., Olesen, J.E., Kristensen, K., Christensen, B.T., 2006. Similarity of differently sized macro-aggregates in arable soils of different texture. Geoderma 137, 147–154

[20] Lavoie, M., Mack, M.C., Schuur, E.A.G., 2011. Effects of elevated nitrogen and temperature on carbon and nitrogen dynamics in Alaskan arctic and boreal soils. Journal of Geophysical Research. Biogeosciences 116.

[21] Li, Z., Tian, D., Wang, B., Wang, J., Wang, S., Chen, H.Y., Xu, X., Wang, C., He, N., Niu, S., 2019. Microbes drive global soil nitrogen mineralization and availability. Global Change Biology 25, 1078–1088

[22] Li, Z., Yang, W., Yue, K., Justine, M.F., He, R., Yang, K., Zhuang, L., Wu, F., Tan, B., Zhang, L., Xu, Z., 2017. Effects of snow absence on winter soil nitrogen dynamics in a subalpine spruce forest of southwestern China. Geoderma 307, 107–113

[23] Mendes, I.C., Bandick, A.K., Dick, R.P., Bottomley, P.J., 1999. Microbial biomass and activities in soil aggregates affected by winter cover crops. Soil Science Society of America Journal 63, 873–881

[24] Nie, M., Pendall, E., Bell, C., Wallenstein, M.D., 2014. Soil aggregate size distribution mediates microbial climate change feedbacks. Soil Biology & Biochemistry 68, 357–365

[25] Reichel, R., Wei, J., Islam, M.S., Schmid, C., Wissel, H., Schröder, P., Schloter, M., Brüggemann, N., 2018. Potential of wheat straw, spruce sawdust, and lignin as high organic carbon soil amendments to improve agricultural nitrogen retention capacity: an incubation study. Frontiers in Plant Science 9, 900

[26] Repo, T., Sirkiä, S., Heinonen, J., Lavigné, A., Roitto, M., Koljonen, E., Sutinen, S., Finér, L., 2014. Effects of frozen soil on growth and longevity of fine roots of Norway spruce. Forest Ecology and Management 313, 112–122

[27] Shibata, H., Hasegawa, Y., Watanabe, T., Fukuzawa, K., 2013. Impact of snowpack decrease on net nitrogen mineralization and nitrification in forest soil of northern Japan. Biogeochemistry 116, 69–82

[28] Six, J., Bossuyt, H., Degryze, S., Denef, K., 2004. A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil & Tillage Research 79, 7–31

[29] Steinweg, J.M., Fisk, M.C., McAlexander, B., Groffman, P.M., Hardy, J.P., 2008. Experimental snowpack reduction alters organic matter and net N mineralization potential of soil macroaggregate in a northern hardwood forest. Biology and Fertility of Soils 45, 1–10

[30] Stieglitz, M., Déry, S.J., Romanovsky, V.E., Osterkamp, T.E., 2003. The role of snow cover in the warming of arctic permafrost. Geophysical Research Letters 30, 51.4–54.4

[31] Tan, B., Wu, F., Yang, W., He, X., 2014. Snow removal alters soil microbial biomass and enzyme activity in a Tibetan alpine forest. Applied Soil Ecology 76, 34–41

[32] Wilpiszeski, R.L., Aufrecht, J.A., Retterer, S.T., Sullivan, M.B., Graham, D.E., Pierce, E.M., Zablocki, O.D., Palumbo, A.V., Elias, D.A., 2019. Soil aggregate microbial communities: towards understanding microbiome interactions at biologically relevant scales. Applied and Environmental Microbiology 85, e00324–e19

[33] Xiong, L., Xu, Z., Wu, F., Yang, W., Yin, R., Li, Z., Gou, X., Tang, S., 2014. Effects of snow pack on soil nitrogen transformation enzyme activities in a subalpine Abies faxioniana forest of western Sichuan, China. Chinese Journal of Applied Ecology 25, 1293–1299 (in Chinese).

[34] Xu, Z., Hu, R., Xiong, P., Wan, C., Cao, G., Liu, Q., 2010. Initial soil responses to experimental warming in two contrasting forest ecosystems, Eastern Tibetan Plateau, China: nutrient availabilities, microbial properties and enzyme activities. Applied Soil Ecology 46, 291–299

[35] Xu, Z., Liu, Q., Yin, H., 2014. Effects of temperature on soil net nitrogen mineralisation in two contrasting forests on the eastern Tibetan Plateau, China. Soil Research (Collingwood, Vic.) 52, 562–567

[36] Yang, K., Peng, C., Peñuelas, J., Kardol, P., Li, Z., Zhang, L., Ni, X., Yue, K., Tan, B., Yin, R., Xu, Z., 2019. Immediate and carry-over effects of increased soil frost on soil respiration and microbial activity in a spruce forest. Soil Biology & Biochemistry 135, 51–59

[37] Yi, X., Yuan, J., Zhu, Y., Yi, X., Zhao, Q., Fang, K., Cao, L., 2018. Comparison of the abundance and community structure of N-Cycling bacteria in paddy rhizosphere soil under different rice cultivation patterns. International Journal of Molecular Sciences 19, 3772

[38] Zaman, M., Chang, S., 2004. Substrate type, temperature, and moisture content affect gross and net N mineralization and nitrification rates in agroforestry systems. Biology and Fertility of Soils 39, 269–279

Acknowledgments

This work was supported by the National Natural Science Foundation of China (32071745, 31700542 and 31870602), the Program of Sichuan Excellent Youth Sci-Tech Foundation (2020JDJQ0052) and the National Key Research and Development Program of China (2016YFC0502505 and 2017YFC0505003)

RIGHTS & PERMISSIONS

2021 Higher Education Press