Investigating drivers of active nitrification in organic horizons of tropical forest soils

Highlights

● Some O horizons showed higher nitrification rate than mineral horizons.

● Both total N and pH were positively correlated with nitrification rate in O horizon.

● Nutrient richness in litters supported active nitrification in O horizon.

● Nitrification rate in O horizon increased along with a pH threshold of 5.5–6.0.

Abstract

High nitrate leaching has been observed from the O horizons of some tropical forests; however, the drivers of high nitrate production (active nitrification) in these O horizons have not yet been identified. This study investigated the drivers of active nitrification in the O horizon of tropical forest soils by focusing on two of the most widely recognized controlling factors of nitrification, total N, and pH. We collected mineral and O horizons from eight tropical forests in Cameroon, Indonesia, and Malaysia and measured gross nitrification rates. Some O horizons showed significantly higher gross nitrification rates than mineral horizons, indicating that these O horizons have a high potential for nitrification. Gross nitrification rates in the O horizons were positively correlated with both total N and pH, and the chemical properties (e.g., total content of N, P, and base cations) were intercorrelated. These correlations suggested that the underlying driver of nitrification in the O horizon was nutrient richness in the litter. Results also indicated a threshold of gross nitrification rates around pH values of 5.5–6.0. We elucidate that active nitrification and subsequent high nitrate leaching from the O horizon could be driven by nutrient-rich litter, possibly derived from soil fertility and tree species.

Graphical abstract

Keywords

nitrogen dynamics / gross nitrification rate / organic horizon / forest floor / acidic soil / leguminous trees

References

[1] Bai, E., Houlton, B.Z., Wang, Y.P., 2012. Isotopic identification of nitrogen hotspots across natural terrestrial ecosystems. Biogeosciences9, 3287–3304.

[2] Booth, M.S., Stark, J.M., Rastetter, E., 2005. Controls on nitrogen cycling in terrestrial ecosystems: A synthetic analysis of literature data. Ecological Monographs75, 139–157.

[3] Breuer, L., Kiese, R., Butterbach-Bahl, K., 2002. Temperature and moisture effects on nitrification rates in tropical rain-forest soils. Soil Science Society of America Journal66, 834–844.

[4] Brooks, P.D., Stark, J.M., McInteer, B.B., Preston, T., 1989. Diffusion method to prepare soil extracts for automated nitrogen-15 analysis. Soil Science Society of America Journal53, 1707–1711.

[5] Brookshire, E.N.J., Gerber, S., Greene, W., Jones, R.T., Thomas, S.A., 2017. Global bounds on nitrogen gas emissions from humid tropical forests. Geophysical Research Letters44, 2502–2510.

[6] Brookshire, E.N.J., Gerber, S., Menge, D.N.L., Hedin, L.O., 2012. Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecology Letters15, 9–16.

[7] Carlyle, J.C., Lowther, D.J.R., Smethurst, P.J., Nambiar, E.K.S., 1990. Influence of chemical properties on nitrogen mineralization and nitrification in podzolized sands. Implications for forest management. Soil Research (Collingwood, Vic.)28, 981–1000.

[8] Corlett, R.T., Primack, R.B., 2011. Plants: Building Blocks of the Rain Forest. In: Corlett, R.T., Primack, R.B., eds. Tropical Rain Forests: An Ecological and Biogeographical Comparison. 2nd edition. Oxford: Blackwell Science Ltd., 32–75

[9] Corre, M.D., Veldkamp, E., Arnold, J., Joseph Wright, S., 2010. Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama. Ecology91, 1715–1729.

[10] Crews, T.E., 1999. The presence of nitrogen fixing legumes in terrestrial communities: Evolutionary vs ecological considerations. Biogeochemistry46, 233–246.

[11] De Boer, W., Kowalchuk, G.A., 2001. Nitrification in acid soils: Micro-organisms and mechanisms. Soil Biology & Biochemistry33, 853–866.

[12] Diabate, M., Munive, A., De Faria, S.M., Ba, A., Dreyfus, B., Galiana, A., 2005. Occurrence of nodulation in unexplored leguminous trees native to the West African tropical rainforest and inoculation response of native species useful in reforestation. New Phytologist166, 231–239.

[13] Elrys, A.S., Ali, A., Zhang, H., Cheng, Y., Zhang, J., Cai, Z.C., Müller, C., Chang, S.X., 2021b. Patterns and drivers of global gross nitrogen mineralization in soils. Global Change Biology27, 5950–5962.

[14] Elrys, A.S., Wang, J., Metwally, M.A.S., Cheng, Y., Zhang, J.B., Cai, Z.C., Chang, S.X., Müller, C., 2021a. Global gross nitrification rates are dominantly driven by soil carbon-to-nitrogen stoichiometry and total nitrogen. Global Change Biology27, 6512–6524.

[15] Epihov, D.Z., Batterman, S.A., Hedin, L.O., Leake, J.R., Smith, L.M., Beerling, D.J., 2017. N₂-fixing tropical legume evolution: A contributor to enhanced weathering through the Cenozoic? Proceedings. Biological Sciences284, 20170370.

[16] Foster, J.W., 2004. Escherichia coli acid resistance: Tales of an amateur acidophile. Nature Reviews. Microbiology2, 898–907.

[17] Fujii, K., Hartono, A., Funakawa, S., Uemura, M., Sukartiningsih, Kosaki, T., 2011. Acidification of tropical forest soils derived from serpentine and sedimentary rocks in east Kalimantan, Indonesia. Geoderma160, 311–323.

[18] Fyllas, N.M., Patino, S., Baker, T.R., Bielefeld Nardoto, G., Martinelli, L.A., Quesada, C.A., Paiva, R., Schwarz, M., Horna, V., Mercado, L.M., Santos, A., Arroyo, L., Jiměnez, E.M., Luizao, F.J., Neill, D.A., Silva, N., Prieto, A., Rudas, A., Silviera, M., Vieira, G., Lopez-Gonzalez, G., Malhi, Y., Phillips, O.L., Lloyd, J., 2009. Basin-wide variations in foliar properties of Amazonian forest: Phylogeny, soils and climate. Biogeosciences6, 2677–2708.

[19] Hart, S.C., Stark, J.M., Davidson, E.A., Firestone, M.K., 1994. Nitrogen Mineralization, Immobilization, and Nitrification. In: Weaver, R., Angle, S., Bottomley, P., eds. Method of Soil Analysis. Part 2. Microbiological and Biochemical Properties. Madison: SSSA Book Series, 985–1018

[20] Hedin, L.O., Brookshire, E.N.J., Menge, D.N.L., Barron, A.R., 2009. The nitrogen paradox in tropical forest ecosystems. Annual Review of Ecology, Evolution, and Systematics40, 613–635.

[21] Houlton, B.Z., Wang, Y.P., Vitousek, P.M., Field, C.B., 2008. A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature454, 327–330.

[22] Isobe, K., Suwa, Y., Ikutani, J., Kuroiwa, M., Makita, T., Takebayashi, Y., Yoh, M., Otsuka, S., Senoo, K., Ohmori, M., Koba, K., 2011. Analytical techniques for quantifying ¹⁵N/¹⁴N of nitrate, nitrite, total dissolved nitrogen and ammonium in environmental samples using a gas chromatograph equipped with a quadrupole mass spectrometer. Microbes and Environments26, 46–53.

[23] Jenny, H., 1950. Causes of the high nitrogen and organic matter content of certain tropical forest soils. Soil Science69, 63–69.

[24] Jones, A., Breuning-Madsen, H., Brossard, M., Dampha, A., Deckers, J., Dewitte, O., Gallali, T., Hallett, S., Jones, R., Kilasara, M., Le Roux, P., Micheli, E., Montanarella, L., Spaargaren, O., Thiombiano, L., Van Ranst, E., Yemefack, M., Zougmoré, R., 2013. Soil Atlas of Africa. Luxembourg: European Commission

[25] Kemmitt, S.J., Wright, D., Goulding, K.W.T., Jones, D.L., 2006. pH regulation of carbon and nitrogen dynamics in two agricultural soils. Soil Biology & Biochemistry38, 898–911.

[26] Kirkham, D., Bartholomew, W.V., 1954. Equations for following nutrient transformations in soil, utilizing tracer data. Soil Science Society of America Journal18, 33–34.

[27] Koba, K., Inagaki, K., Sasaki, Y., Takebayashi, Y., Yoh, M., 2010. Nitrogen isotopic analysis of dissolved inorganic and organic nitrogen in soil extracts. In: Ohkouchi, N., Tayasu, I., Koba, K., eds. Earth, Life and Isotopes. Kyoto: Kyoto University Press, pp. 17–36.

[28] Kyveryga, P.M., Blackmer, A.M., Ellsworth, J.W., Isla, R., 2004. Soil pH effects on nitrification of fall-applied anhydrous ammonia. Soil Science Society of America Journal68, 545–551.

[29] Lewis, W.M. Jr, Melack, J.M., McDowell, W.H., McClain, M., Richey, J.E., 1999. Nitrogen yields from undisturbed watersheds in the Americas. Biogeochemistry46, 149–162.

[30] Livingston, G.P., Vitousek, P.M., Matson, P.A. 1988. Nitrous oxide flux and nitrogen transformations across a landscape gradient in Amazonia. Journal of Geophysical Research93, 1593–1599.

[31] Li, Y., Chapman, S.J., Nicol, G.W., Yao, H., 2018. Nitrification and nitrifiers in acidic soils. Soil Biology & Biochemistry116, 290–301.

[32] Li, Z., Zeng, Z., Tian, D., Wang, J., Fu, Z., Zhang, F., Zhang, R., Chen, W., Luo, Y., Niu, S., 2020. Global patterns and controlling factors of soil nitrification rate. Global Change Biology26, 4147–4157.

[33] Markewitz, D., Davidson, E., Moutinho, P., Nepstad, D., 2004. Nutrient loss and redistribution after forest clearing on a highly weathered soil in Amazonia. Ecological Applications14, S177–S199.

[34] Marschner, B., Noble, A.D., 2000. Chemical and biological processes leading to the neutralisation of acidity in soil incubated with litter materials. Soil Biology & Biochemistry32, 805–813.

[35] Norton, J.M., Stark, J.M., 2011. Regulation and measurement of nitrification in terrestrial systems. Methods in Enzymology486, 343–368.

[36] Okuda, T., Manokaran, N., Matsumoto, Y., Niiyama, K., Thomas, S.C., Ashton, P.S., 2003. Ecology of a Lowland Rain Forest in Southeast Asia. Tokyo: Springer

[37] Pajares, S., Bohannan, B.J.M., 2016. Ecology of nitrogen fixing, nitrifying, and denitrifying microorganisms in tropical forest soils. Frontiers in Microbiology7, 1045.

[38] Qualls, R.G., Haines, B.L., Swank, W.T., 1991. Fluxes of dissolved organic nutrients and humic substances in a deciduous forest. Ecology72, 254–266.

[39] Schmidt, B.H.M., Wang, C.P., Chang, S.C., Matzner, E., 2010. High precipitation causes large fluxes of dissolved organic carbon and nitrogen in a subtropical montane Chamaecyparis forest in Taiwan. Biogeochemistry101, 243–256.

[40] Schwendenmann, L., Veldkamp, E., 2005. The role of dissolved organic carbon, dissolved organic nitrogen, and dissolved inorganic nitrogen in a tropical wet forest ecosystem. Ecosystems (New York, N.Y.)8, 339–351.

[41] Shibata, H., Satoh, F., Tanaka, Y., Sakuma, T. 1995. The role of organic horizons and canopy to modify the chemistry of acidic deposition in some forest ecosystems. Water, Air, & Soil Pollution85, 1119–1124.

[42] Shibata, M., Sugihara, S., Mvondo-Ze, A.D., Araki, S., Funakawa, S., 2017. Nitrogen flux patterns through Oxisols and Ultisols in tropical forests of Cameroon, Central Africa. Soil Science and Plant Nutrition63, 306–317.

[43] Soil Survey Staff, 2014. Keys to soil taxonomy. 12th ed. Washington, D.C.: USDA-NRCS

[44] Stark, J.M., Hart, S.C., 1996. Diffusion technique for preparing salt solutions, Kjeldahl digests, and persulfate digests for nitrogen-15 analysis. Soil Science Society of America Journal60, 1846–1855.

[45] Ste-Marie, C., Paré, D., 1999. Soil, pH and N availability effects on net nitrification in the forest floors of a range of boreal forest stands. Soil Biology & Biochemistry31, 1579–1589.

[46] Vitousek, P.M., 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology65, 285–298.

[47] Vitousek, P.M., Matson, P.A., 1988. Nitrogen transformations in a range of tropical forest soils. Soil Biology & Biochemistry20, 361–367.

[48] Vitousek, P.M., Sanford, R.L.Jr. 1986. Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics17, 137–167.

[49] Wilcke, W., Yasin, S., Abramowski, U., Valarezo, C., Zech, W., 2002. Nutrient storage and turnover in organic layers under tropical montane rain forest in Ecuador. European Journal of Soil Science53, 15–27.

[50] Zhao, W., Zhang, J.B., Müller, C., Cai, Z.C., 2018. Effects of pH and mineralisation on nitrification in a subtropical acid forest soil. Soil Research (Collingwood, Vic.)56, 275–283.

Acknowledgments

We thank Dr. Shigeru Araki, Dr. Tetsuhiro Watanabe, Dr. Kazumichi Fujii, and Dr. Kaori Ando for their support in soil sampling, Prof. Keisuke Koba and Dr. Jinsen Zheng for their support with the denitrifier method, and all members of Prof. Funakawa laboratory at Kyoto University. This study was supported by Center for Ecological Research, Kyoto University, a Joint Usage/Research Center, and financially supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (Grant numbers 24228007, 17H06171, and 19J14572). The authors have no relevant financial or non-financial interests to disclose.

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