Abstract
Estimates of enzymatic activity are used as indices for soil quality, microbial nutrient demand, microbial growth, and activity. Mosses trap soil moisture, influence soil temperature, and create a microenvironment promoting an overall higher level of microbial activity, thus making the decomposition of organic matter more favorable. This study determines the role of mosses in influencing soil biochemical properties in three temperate forest types of the Garhwal Himalayas, Uttarakhand, viz., moist temperate deciduous forest, Ban oak forest, and moist deodar forest. Activities of major soil enzymes (dehydrogenase, β-glucosidase, acid phosphatase, aryl sulfatase, phenol oxidase, and urease) and soil microbial biomass carbon (SMBC) were determined under two different substrates, i.e., with and without moss cover in two different seasons, viz., monsoon and winter. The Pearson correlation of enzymes with specific soil nutrients they act upon has also been shown. The SMBC and on average activities of all the enzymes were predominantly higher in soil with moss cover during monsoon season and without moss cover in the winter season. SMBC in the three study sites ranged from 280.55 to 1707.64 µg C/g. Statistically significant differences (p < 0.01) were observed for all the properties within the substrates among all the three sites and across the two seasons. Our results suggest that mosses play a significant role in positively influencing soil biochemical properties in both seasons by creating a microscale mosaic that offers a high degree of heterogeneity in soil function. Our study emphasizes that mosses strongly affect soil enzyme activities and microbial biomass, thus improving soil health.
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References
Agrawala, N. K. (1973). Working plan for the Kedarnath Forest Division 1972–73 to 1981–82. Working plan circle, Nainital, Uttar Pradesh.
Allen, S. E., Grimshaw, H. M., Parkinson, J. A., & Quarmby, C. (1974). Chemical analysis of ecological materials. Blackwell Scientific Publications, Oxford, England.
Allison, S. D., & Vitousek, P. M. (2005). Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology and Biochemistry, 37(5), 937–944. https://doi.org/10.1016/j.soilbio.2004.09.014
Bahuguna, Y. M., Gairola, S., Semwal, D. P., Uniyal, P. L., & Bhatt, A. B. (2012). Soil physico-chemical characteristics of bryophytic vegetation residing Kedarnath Wildlife Sanctuary (KWLS), Garhwal Himalaya, Uttarakhand, India. Indian Journal of Science and Technology, 5(4), 2547–2553.
Bahuguna, Y. M., Gairola, S., Uniyal, P. L., & Bhatt, A. B. (2016). Moss flora of Kedarnath Wildlife Sanctuary (KWLS), Garhwal Himalaya, India. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 86(4), 931–943. https://doi.org/10.1007/s40011-015-0531-z
Bahuguna, Y. M., Sumeet, G., Semwal, D. P., & Uniyal, P. L. (2014). Species diversity and composition of bryophytic vegetation in Garhwal Himalaya with special reference to Kedarnath Wildlife Sanctuary (KWLS), Uttarakhand, India. International Journal of Ecology and Environmental Sciences, 40(2/3), 75–85.
Banerjee, S. P., & Badola, K. C. (1980). Nature and properties of some deodar (Cedrus deodara) forest soils of Chakrata forest division. Up. Indian Forester, 106(8), 558–560.
Bonan, G. B., & Shugart, H. H. (1989). Environmental factors and ecological processes in boreal forests. Annual Review of Ecology and Systematics, 20(1), 1–28. https://doi.org/10.1146/annurev.es.20.110189.000245
Bragazza, L., Robroek, B. J., Jassey, V. E., Arif, M. S., Marchesini, R., Guglielmin, M., & Cannone, N. (2019). Soil microbial community structure and enzymatic activity along a plant cover gradient in Victoria Land (continental Antarctica). Geoderma, 353, 144–151. https://doi.org/10.1016/j.geoderma.2019.06.033
Burns, R. G. (1982). Enzyme activity in soil: Location and a possible role in microbial ecology. Soil Biology and Biochemistry, 14(5), 423–427. https://doi.org/10.1016/0038-0717(82)90099-2
Burns, R. G. (1986). Interaction of enzymes with soil mineral and organic colloids. Interactions of Soil Minerals with Natural Organics and Microbes, 17, 429–451. https://doi.org/10.2136/sssaspecpub17.c11
Burns, R. G., & Dick, R. P. (Eds.). (2002). Enzymes in the environment: Activity, ecology, and applications. CRC Press, New York. https://doi.org/10.1201/9780203904039
Burns, R. G., DeForest, J. L., Marxsen, J., Sinsabaugh, R. L., Stromberger, M. E., Wallenstein, M. D., & Zoppini, A. (2013). Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biology and Biochemistry, 58, 216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Caldwell, B. A. (2006). Effects of invasive scotch broom on soil properties in a Pacific coastal prairie soil. Applied Soil Ecology, 32(1), 149–152. https://doi.org/10.1016/j.apsoil.2004.11.008
Casida, L. E. (1977). Microbial metabolic activity in soil as measured by dehydrogenase determinations. Applied and Environmental Microbiology, 34(6), 630–636. https://doi.org/10.1128/aem.34.6.630-636.1977
Champion, H. G., & Seth, S. K. (1968). A revised survey of the forest types of India. Manager of publications, Government of India, New Delhi.
Dar, J. A., & Somaiah, S. (2015). Altitudinal variation of soil organic carbon stocks in temperate forests of Kashmir Himalayas. India. Environmental Monitoring and Assessment, 187(2), 1–15. https://doi.org/10.1007/s10661-014-4204-9
Dick, R. P. (1994). Soil enzyme activities as indicators of soil quality. Defining Soil Quality for a Sustainable Environment, 35, 107–124. https://doi.org/10.2136/sssaspecpub35.c7
Eivazi, F., & Tabatabai, M. A. (1988). Glucosidases and galactosidases in soils. Soil Biology and Biochemistry, 20(5), 601–606. https://doi.org/10.1016/0038-0717(88)90141-1
Floch, C., Alarcon-Gutiérrez, E., & Criquet, S. (2007). ABTS assay of phenol oxidase activity in soil. Journal of Microbiological Methods, 71(3), 319–324. https://doi.org/10.1016/j.mimet.2007.09.020
Frankenberger, W. T., Jr., & Dick, W. A. (1983). Relationships between enzyme activities and microbial growth and activity indices in soil. Soil Science Society of America Journal, 47(5), 945–951. https://doi.org/10.2136/sssaj1983.03615995004700050021x
Ghiloufi, W., Seo, J., Kim, J., Chaieb, M., & Kang, H. (2019). Effects of biological soil crusts on enzyme activities and microbial community in soils of an arid ecosystem. Microbial Ecology, 77(1), 201–216. https://doi.org/10.1007/s00248-018-1219-8
Gholamhosseinian, A., Sepehr, A., Lajayer, B. A., Delangiz, N., & Astatkie, T. (2021). Biological soil crusts to keep soil alive, rehabilitate degraded soil, and develop soil habitats. In A. Vaishnav & D.K. Chaudhary (Eds.), Microbial polymers (pp. 289–309). Springer, Singapore. https://doi.org/10.1007/978-981-16-0045-6_13
Grandy, A. S., Sinsabaugh, R. L., Neff, J. C., Stursova, M., & Zak, D. R. (2008). Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry, 91(1), 37–49. https://doi.org/10.1007/s10533-008-9257-9
Hu, R., Wang, X. P., Zhang, Y. F., Shi, W., Jin, Y. X., & Chen, N. (2016). Insight into the influence of sand-stabilizing shrubs on soil enzyme activity in a temperate desert. CATENA, 137, 526–535. https://doi.org/10.1016/j.catena.2015.10.022
Kang, H., Kang, S., & Lee, D. (2009). Variations of soil enzyme activities in a temperate forest soil. Ecological Research, 24(5), 1137–1143. https://doi.org/10.1007/s11284-009-0594-5
Karaca, A., Cetin, S. C., Turgay, O. C., & Kizilkaya, R. (2010). Soil enzymes as indication of soil quality. In G. Shukla & A. Verma (Eds.), Soil enzymology (pp. 119–148). Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14225-3_7
Kaushal, S., Siwach, A., Baishya., R. (2021). Diversity, regeneration, and anthropogenic disturbance in major Indian Central Himalayan forest types: Implications for conservation. Biodiversity and Conservation, 30, 2451-2480. https://doi.org/10.1007/s10531-021-02203-w
Köhler, L., Tobón, C., Frumau, K. A., & Bruijnzeel, L. S. (2007). Biomass and water storage dynamics of epiphytes in old-growth and secondary montane cloud forest stands in Costa Rica. Plant Ecology, 193(2), 171–184. https://doi.org/10.1007/s11258-006-9256-7
Koranda, M., & Michelsen, A. (2021). Mosses reduce soil nitrogen availability in a subarctic birch forest via effects on soil thermal regime and sequestration of deposited nitrogen. Journal of Ecology, 109(3), 1424–1438. https://doi.org/10.1111/1365-2745.13567
Kunito, T., Saeki, K., Goto, S., Hayashi, H., Oyaizu, H., & Matsumoto, S. (2001). Copper and zinc fractions affecting microorganisms in long-term sludge-amended soils. Bioresource Technology, 79(2), 135–146. https://doi.org/10.1016/s0960-8524(01)00047-5
Liu, Y., Yang, H., Li, X., & Xing, Z. (2014). Effects of biological soil crusts on soil enzyme activities in revegetated areas of the Tengger Desert, China. Applied Soil Ecology, 80, 6–14. https://doi.org/10.1016/j.apsoil.2014.03.015
Ljungdahl, L. G. & Eriksson, K. E. (1985). Ecology of microbial cellulose degradation. In K.C. Marshall (Ed.), Advances in Microbial Ecology (8th ed., pp. 237–299). Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-9412-3_6
Nannipieri, P., Grego, S., & Ceccanti, B. (1990). Ecological significance of the biological activity in soil. In J.M. Bollag & G. Stotzky (Eds.), Soil biochemistry (6th ed., pp. 293-355). Markel Dekker, New York.
Nannipieri, P., Ceccanti, B., Cervelli, S., & Sequi, P. (1978). Stability and kinetic properties of humus-urease complexes. Soil Biology and Biochemistry, 10(2), 143–147. https://doi.org/10.1016/0038-0717(78)90085-8
Negi, H. R., & Gadgil, M. (1997). Species diversity and community ecology of mosses: A case study from Garhwal Himalaya. International Journal of Ecology & Environmental Sciences, 23, 445–462.
Raina, A. K., Pharasi, S. C., & Prasad, K. G. (1994). Clay mineralogical composition in soils under different forest vegetation of Garhwal Himalayas. Journal of the Indian Society of Soil Science, 42(1), 120–122.
Ross, D. J., Speir, T. W., Kettles, H. A., & Mackay, A. D. (1995). Soil microbial biomass, C and N mineralization and enzyme activities in a hill pasture: Influence of season and slow-release P and S fertilizer. Soil Biology and Biochemistry, 27(11), 1431–1443. https://doi.org/10.1016/0038-0717(95)00069-Q
Saha, S., Prakash, V., Kundu, S., Kumar, N., & Mina, B. L. (2008). Soil enzymatic activity as affected by long term application of farm yard manure and mineral fertilizer under a rainfed soybean–wheat system in NW Himalaya. European Journal of Soil Biology, 44(3), 309–315. https://doi.org/10.1016/j.ejsobi.2008.02.004
Sahu, V., & Asthana, A. K. (2014). Two mosses new to west Himalayan Bryoflora. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 84(3), 805–810. https://doi.org/10.1007/s40011-013-0290-7
Sedia, E. G., & Ehrenfeld, J. G. (2006). Differential effects of lichens and mosses on soil enzyme activity and litter decomposition. Biology and Fertility of Soils, 43(2), 177–189. https://doi.org/10.1007/s00374-006-0077-6
Shao, X., Yang, W., & Wu, M. (2015). Seasonal dynamics of soil labile organic carbon and enzyme activities in relation to vegetation types in Hangzhou Bay tidal flat wetland. PLoS One, 10(11), e0142677. https://doi.org/10.1371/journal.pone.0142677
Singh, J., Upreti, D. K., & Dubey, A. K. (2016). Effect of elevation gradient on the distribution of lichens and mosses of central Himalayan region, Uttarakhand, India. G-Journal of Environmental Science and Technology, 3(5), 44–47.
Sinsabaugh, R. L. (2010). Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology and Biochemistry, 42(3), 391–404. https://doi.org/10.1016/j.soilbio.2009.10.014
Sinsabaugh, R. L., Antibus, R. K., & Linkins, A. E. (1991). An enzymic approach to the analysis of microbial activity during plant litter decomposition. Agriculture, Ecosystems & Environment, 34(1–4), 43–54. https://doi.org/10.1016/0167-8809(91)90092-c
Sinsabaugh, R. L., Lauber, C. L., Weintraub, M. N., Ahmed, B., Allison, S. D., Crenshaw, C., & Zeglin, L. H. (2008). Stoichiometry of soil enzyme activity at global scale. Ecology Letters, 11(11), 1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Sinsabaugh, R. S. (1994). Enzymic analysis of microbial pattern and process. Biology and Fertility of Soils, 17(1), 69–74. https://doi.org/10.1007/BF00418675
Tabatabai, M. A., & Bremner, J. M. (1969). Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry, 1(4), 301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Tabatabai, M. A., & Bremner, J. M. (1970). Arylsulfatase activity of soils. Soil Science Society of America Journal, 34(2), 225–229. https://doi.org/10.2136/sssaj1970.03615995003400020016x
Tabatabai, M. A., & Bremner, J. M. (1972). Assay of urease activity in soils. Soil Biology and Biochemistry, 4(4), 479–487. https://doi.org/10.1016/0038-0717(72)90064-8
Tomar, U., & Baishya, R. (2020). Seasonality and moisture regime control soil respiration, enzyme activities, and soil microbial biomass carbon in a semi-arid forest of Delhi. India. Ecological Processes, 9(1), 1–13. https://doi.org/10.1186/s13717-020-00252-7
Vance, E. D., Brookes, P. C., & Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry, 19(6), 703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Wall, A., & Heiskanen, J. (2003). Water-retention characteristics and related physical properties of soil on afforested agricultural land in Finland. Forest Ecology and Management, 186(1–3), 21–32. https://doi.org/10.1016/S0378-1127(03)00239-1
Wilson, J. A., & Coxson, D. S. (1999). Carbon flux in a subalpine spruce-fir forest: Pulse release from Hylocomium splendens feather-moss mats. Canadian Journal of Botany, 77(4), 564–569. https://doi.org/10.1139/b99-002
Wu, J. J. R. G., Joergensen, R. G., Pommerening, B., Chaussod, R., & Brookes, P. C. (1990). Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biology & Biochemistry, 22(8), 1167–1169. https://doi.org/10.1016/0038-0717(90)90046-3
Yang, H., Liu, C., Liu, Y., & Xing, Z. (2018a). Impact of human trampling on biological soil crusts determined by soil microbial biomass, enzyme activities and nematode communities in a desert ecosystem. European Journal of Soil Biology, 87, 61–71. https://doi.org/10.1016/j.ejsobi.2018.05.005
Yang, M., Yang, D., & Yu, X. (2018b). Soil microbial communities and enzyme activities in sea-buckthorn (Hippophae rhamnoides) plantation at different ages. PLoS One, 13(1), e0190959. https://doi.org/10.1371/journal.pone.0190959
Acknowledgements
The authors sincerely thank PCCF and CWLW, Uttarakhand, and the divisional forest officers of the Chakrata Forest Division and Kedarnath Wildlife Sanctuary for granting the necessary permission to conduct this research. We acknowledge the support of Prof. P.L. Uniyal, Department of Botany, University of Delhi, for helping us with the identification of moss species, and Ms. Sharanjeet Kaur, project fellow, Department of Botany, University of Delhi, for making maps for the study sites. The authors also acknowledge the editor and the two anonymous reviewers for the constructive comments and encouragement, which helped improve the manuscript substantially.
Funding
The study was funded by Science and Engineering Research Board (SERB), Government of India, via Research Project (Project No. EEQ /2016/000164). Siddhartha Kaushal and Anshu Siwach thank the University Grants Commission (UGC), New Delhi, for providing a CSIR-UGC JRF fellowship. We also thank the Institution of Eminence (IoE), University of Delhi, for providing additional support through the Faculty Research Programme (FRP) grant (2020–21).
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Siwach, A., Kaushal, S. & Baishya, R. Terricolous mosses impact soil microbial biomass carbon and enzymatic activity under temperate forest types of the Garhwal Himalayas. Environ Monit Assess 193, 516 (2021). https://doi.org/10.1007/s10661-021-09295-5
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DOI: https://doi.org/10.1007/s10661-021-09295-5