Abstract
Because potassium (K) is a rock-derived essential element that can be depleted in highly-weathered tropical soils, K availability may limit some portion of soil microbial activity in tropical forest ecosystems. In this paper we tested if K limits microbial activity in the condition of sufficient labile C supply. An incubation experiment was performed using surface soil samples (0–10 cm depth) obtained from four permanent ecological research plots in a natural sub-tropical forest in southern China. Soil samples were taken in September 2016. Heterotrophic soil respiration rates and microbial biomass were measured after the addition of glucose (both D and L) with and without K (potassium chloride). We did not observe any effects of K addition on soil microbial respiration, suggesting that K does not limit the microbial activity in the condition of sufficient labile C supply. The lack of microbial response to added K can be attributed to the high mobility of K in forest ecosystems, which may have provided sufficient K to microbes in our soil samples (already provided at the beginning of the incubation). However, at the present stage, we cannot conclude that K is not a limiting factor of soil microbial activity in other tropical forest ecosystems because of the heterogeneity of tropical forest ecosystems and few observations. The hypothesis needs to be tested in larger numbers of tropical forests.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
For understanding ecosystem dynamics, it is essential to determine nutrients that limit biological processes, including soil microbial activity. Traditionally, in tropical forest ecosystems, soil microbial activity has been considered to be limited by P availability. This idea is based on several experimental results that P addition stimulated soil microbial respiration (Cleveland et al. 2002; Ilstedt and Singh 2005; Mori et al. 2010) and increased microbial biomass (Liu et al. 2012; Turner and Wright 2014). The low P availability in tropical soils due to deep weathering, chemical binds with aluminum (Al) and iron (Fe), and physico-chemical adsorption to Al and Fe (hydr) oxides (Cross and Schlesinger 1995) can explain the P shortage for microbial activities in tropical soils (but see a review by Mori et al. 2018).
However, soil microbial activity in tropical forest soils may be limited not only by P but also by other nutrients. Recently, the traditional view of single-nutrient limitation is under re-consideration (Elser et al. 2007). Several studies suggested that biotic processes such as primary production may be co-limited by multiple nutrients (Davidson et al. 2007; Saito et al. 2008; Harpole et al. 2011; Bracken et al. 2015), especially in the community levels where several different kinds of species co-exist (Arrigo 2005; Danger et al. 2008). This can be also true in case of soil microbial activity. Different groups of microbes can be limited by different nutrients. Also, additions of different nutrients can alter microbial communities in different ways. In a nutrient-poor environment, native species are adapted to the situation. If additional nutrient was supplied, the originally-dominant species would be replaced by others which are better competitors in the new situation (Xun et al. 2015). Thus, it is plausible to hypothesize that multiple nutrients limit soil microbial activity. Nevertheless, few researchers have tested nutrient limitations on soil microbial activity in tropical forests, except for limitations of nitrogen (N) (Ilstedt and Singh 2005; Cleveland and Townsend 2006; Teklay et al. 2006; Gnankambary et al. 2008) and P (Cleveland et al. 2002; Ilstedt and Singh 2005; Cleveland and Townsend 2006; Liu et al. 2012; Mori et al. 2013b, 2016c, 2017) (but see a recent criticism by Mori et al. 2018).
Potassium (K), which is a major intracellular cation in all kinds of organisms including bacteria and fungi (Brown 1964; Weed et al. 1969), is a candidate to (co-)limit soil microbial activity in tropical forests, because K is an essential rock derived element that can be depleted in deeply-weathered tropical soils. The importance of K for primary production in tropical forests was reported by Wright et al. (2011) and Santiago et al. (2012), who demonstrated that K addition reduced fine-root biomass at the community level, reduced allocation to roots in seedlings, and increased seedling height growth rates in a Panamanian tropical forest. The stimulatory effects of K addition on plant growth were also reported in various types of ecosystems (see a review by Tripler et al. 2006). The role of K on litter decomposition was also tested in tropical forests (Kaspari et al. 2008; Powers and Salute 2011). Kaspari et al. (2008) demonstrated that decomposition of cellulose (filter paper) was stimulated by K addition in a Panamanian tropical forest, although effects through soil fauna were also included in the result. Meanwhile, litter decomposition was not affected by K addition either in the field (Kaspari et al. 2008) or the laboratory (Powers and Salute 2011). To our knowledge, direct tests on the response of soil microbial activity to K addition are still rare.
Turner and Wright (2014) reported P addition but not K addition increased microbial biomass C in a tropical lowland forest in Panama. They suggested that microbial biomass was limited by P, and that K was less important in the forest. However, to understand whether K limits microbial activity, it is essential to test the effects of K addition on microbial respiration, not only on microbial biomass. Recent review suggested that the response of soil microbial biomass to nutrient addition cannot necessarily identify a limiting nutrient (Mori et al. 2018). This is because standing microbial biomass is not always an indicator of microbial activity. For example, boreal and temperate forest soils have much larger amount of microbial biomass compared with tropical forest soils, where microbial activity is higher (Xu et al. 2013). In mountain ecosystems, soils at higher elevations support greater microbial biomass than do lower areas (Wagai et al. 2011). These facts indicate that a higher microbial activity, which leads to a quicker soil organic matter decomposition, can result in less standing microbial biomass. Therefore only measuring microbial biomass might incorrectly identify the limiting nutrients of soil microbial activity. Indeed, Mori et al. (2016b) demonstrated that soil respiration and microbial biomass responded in contrasting ways to exogenous nutrient addition.
We conducted an incubation experiment to examine the effects of K addition on soil microbial respiration as well as soil microbial biomass. According to the copiotrophic hypothesis (Ramirez et al. 2012), nutrient addition can reduce soil microbial respiration by suppressing recalcitrant organic matter decomposition because of the microbial community shift from more oligotrophic to more copiotrophic conditions. In our experiment, labile C was simultanousely added to provide sufficient C and to reduce the impacts of nutrient addition on any microbial community shift and accompanying changes in reculcitrant C decomposition. Although the addition of a limiting nutrient can suppress organic matter decomposition by reducing microbial mining of the limiting nutrient from organic matter (Craine et al. 2007), this is not a case for K because K does not combine with organic C. Thus, our incubation experiment with and without K addition provided us an opportunity to tested whether K limits microbial activity in the condition of sufficient labile C supply.
Materials and methods
Study site and soil sampling
The experiment was conducted at a research site in the Shimentai National Nature Reserve (24°22′–24°31′N, 113°05′–113°31′E), Guangdong Province, southern China. The climate is subtropical monsoon with wet and dry seasons. Mean temperature is 20.8 °C and mean annual rainfall is 1700 mm (Shi et al. 2016). The vegetation type at the study site was broadleaved evergreen forest that was around 50 years old at the time of the study. The dominant canopy tree species were Cryptocarya concinna, Schima superba, Machilus chinensis, Castanea henryi (Skan) Rehd., and Engelhardtia roxburghiana. Basic characteristics of the forest stand are presented in Table 1. The soil type in the study site was latosolic red clay-loam soil.
We took soil samples (0–10 cm depth) from four permanent ecological research plots, after removing litter layers. The radius for each circular plot was 17 m, having an area of 907 m2. In each plot, soil samples were taken from six randomly-selected points, by using a soil core (4 cm diameter). The six cores were composited and passed through a 2-mm sieve after fine roots and organic matter were removed. Basic soil chemical properties are presented in Table 2. Exchangeable K+, Ca2+, Mg2+, and Na+ contents were determined after extraction with 1 N ammonium acetate at pH 7. Exchangeable Al3+ was extracted by 1-M KCl. Soil pH(H2O) was measured using a soil to water ratio of 1:2.5. Exchangeable cations and soil pH(H2O) were determined by using air-dry soil. Dissolved and microbial forms of C and N were determined using fresh soils with the same methods described later.
Incubation
Soil samples with 20 g oven-dry equivalent weight were placed in 700 mL-plastic bottles with lids equipped with a CO2 analyzer (GMP43, Vaisala). For dissolved organic matter (both C and N) and microbial biomass analysis, 5 g samples were placed in 50 mL bottles. We provided C to both control and K-added soils in the form of glucose (1.2 mg g−1) (Ilstedt and Singh 2005; Mori et al. 2013a) because no C was provided by the litter layer or root exudates in the incubation experiment. Potassium was added in the form of KCl (Wright et al. 2011) at 0.1 mg g−1. The soil water content was adjusted to 42% (mass%). The samples were incubated for 142.6 h at 20 °C in the dark. At the start of the incubation, all bottles were covered with polyethylene plastic wrap to prevent water evaporation (Mori et al. 2016a).
CO2 flux measurement
CO2 fluxes were measured at 8, 24.3, 36, 48.3, 60, 72.3, 84, 108.2, and 142.6 h after the start of the incubation. After the polyethylene plastic wrap was removed, the upper air of the plastic bottles was mixed well so that the accumulated CO2 was removed. CO2 fluxes were measured by monitoring the changes in CO2 concentrations after the closure of lid equipped with a CO2 analyzer (GMP43, Vaisala). We recorded the changes in CO2 concentration 13 times during 6–7 min measurements. The recording started several minutes after the closure of the lids so that the disturbance by the manipulation was minimized. Gas fluxes were determined by linear regression model. The R value of regression line for every gas flux measurement was higher than 0.9 (more than 75% of the R values were higher than 0.99).
Soil chemical and microbial properties
At the end of the incubation, dissolved organic carbon (DOC) and dissolved N (DN) in the soil were extracted by adding 50 ml of 0.5 mol/L K2SO4 and shaking for 60 min. DOC and DN were analyzed by a total organic C analyzer (TOC-VCHN analyzer, SHIMADZU, Kyoto, Japan). Soil microbial biomass C (MBC) and N (MBN) were determined by using the chloroform fumigation extraction method (Vance et al. 1987). Incubated soils were exposed to CHCl3 vapor for 24 h in a vacuum desiccator. After residual CHCl3 was removed, fumigated soils were shaken with 50 ml of 0.5 mol/L K2SO4 for 60 min and DOC and DN were extracted. Soil MBC and MBN contents were calculated from the differences between the fumigated and un-fumigated samples using a conversion factor of 0.45 (Jenkinson et al. 2004).
Statistical analysis and calculations
Statistical analysis was performed using the Excel software package (version 2013; Microsoft Corp.; Redmond, WA, USA) with statistical add-in software (Excel statistics version 2015 and its updates; Social Survey Research Information Co., Ltd.; Tokyo, Japan). The level of significance was examined by two-way repeated ANOVA (K addition versus sampling time) for CO2 fluxes and paired t test for cumulative CO2 emissions and soil properties, assuming the normality and homoscedasticity of the data.
The cumulative CO2 emissions were estimated using the linear trapezoidal method (Mori et al. 2013c). The CO2 fluxes at 0 h were estimated as the crossing point of the y-axis and the line connecting fluxes of 8 h and 24.3 h in the figure (Fig. 1). If the estimated flux was lower than zero, we assumed the flux at 0 h was zero. The timing of extraction of DOC and DN (at 142.0 h) differed slightly from that of gas sampling (at 142.6 h), but we assumed the error was ignorable.
Results and discussion
In contrast with the copiotrophic hypothesis, we did not observe any effects of K addition on soil microbial activity. Potassium addition had no effects either on CO2 fluxes (P = 0.86, two-way repeated ANOVA, Fig. 1) or on cumulative CO2 emissions during the incubation period (0.53 ± 0.05 and 0.55 ± 0.04 mg C g soil−1 in control and K-added soil, respectively, P = 0.31, paired t-test). Microbial biomass and dissolved forms of C and N were also unaffected by addition of K (P > 0.05, paired t-test, Fig. 2). These results suggest that at our study site K did not limit soil microbial activity in the condition of sufficient labile C supply.
The available K content at our study site (0.86 ± 0.10 mmol kg −1, Table 2) was lower than a tropical lowland forest in Panama (1.4–3.4 mmol kg−1), secondary forests and monoculture plantations in Indonesia (2–5 mmol kg−1) (Yamashita et al. 2008), and a dry evergreen forest in Thailand (5.4–11.9 mmol kg−1) (Yamashita et al. 2011). The values were in the range of 71 different forests in the Amazonian basin (0.3–2.4 mmol kg−1, Quesada et al. 2010). Therefore, we assume that soil microbes in many tropical forest ecosystems are not limited by K availability. Indeed, our results are consistent with a report by Turner and Wright (2014), who suggested that K did not limit the microbial biomass in a lowland tropical forest in Panama (but note that a response of microbial biomass to nutrient addition does not necessarily indicate a nutrient limitation of microbial activity). At the same research site in Panama, Kaspari et al. (2008) reported that K addition had no effects on leaf-litter decomposition. In a laboratory microcosm experiment, Powers and Salute (2011) demonstrated that K addition had no impacts on decomposition of two types of leaf litter taken from tropical dry forest trees. These reports all support the idea that K is not a limiting factor of microbial activity in soil and/or litter. However, at the present stage, we cannot conclude absolutely that K is not a limiting factor of soil microbial activity in tropical forest ecosystems, because of the heterogeneity of tropical forest ecosystems and few observations. The hypothesis needs to be tested in larger numbers of tropical forests. Now we are trying to test this question in various types of tropical forests.
The lack of microbial response to added K in our study site can be attributed to physical and chemical characteristics of K in forest ecosystems, which may have provided sufficient K to microbes in our soil samples (already provided at the beginning of the incubation). It is well known that K has high mobility in the soil compared with other nutrients (Sayer and Tanner 2010). In addition, K is readily leached from organic matter. Recent research reported that 100% of K was water-extracted from leaf litter (Schreeg et al. 2013). Due to the high mobility of K in forest ecosystems, microbes might easily re-use K from organic matter (Tobon et al. 2004). This direct pathway contrasts with the indirect pathways for uptake of N and P, both of which require various kinds of enzymes to be converted to available forms (Marklein and Houlton 2012; Kitayama 2013; Turner and Wright 2014).
The high mobility of K would also enable plants to easily access K, but research has clearly shown a stimulatory effect of K on primary production in tropical forests (Wright et al. 2011; Santiago et al. 2012). If microbes in tropical forest soils are not limited by K but plants are, the difference could have a practical meaning. For example, in tree plantations in the tropics, K fertilization has potential to elevate C sequestration by trees without accelerating the loss of soil C via soil respiration. The contrasting responses to K addition can be explained by the following two possibilities: (i) microbes compete more aggressively for K than do plants; and (ii) microbes require less K than do plants. Further research will be needed to clarify these possibilities.
Although we demonstrated that K did not stimulate soil microbial activity in our laboratory experiment, the incubation might contain some limitations. Since we provided C in the form of glucose (Duah-Yentumi et al. 1998; Ilstedt and Singh 2005; Gnankambary et al. 2008; Mori et al. 2013a), stimulatory effects of K addition on several microbial groups might have been masked in our experimental setup. It is possible that K addition stimulates cellulose decomposers if cellulose (instead of glucose) is supplied. Kaspari et al. (2008) reported cellulose decomposition was stimulated in K-fertilized plots. It is also possible that our results were biased to identify a nutrient limitation of copiotrophic microbes rather than one of oligotrophs: copiotrophs become stronger in a resource-rich conditions. Additional incubation experiments are needed to test the effects of K addition on soil respiration with amendments of various forms of C including cellulose and recalcitrant organic matter. Despite its limitations, the present study demonstrated that K addition did not stimulate soil microbial activity when labile C was amended.
References
Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437:343–348. https://doi.org/10.1038/nature04158
Bracken MES, Hillebrand H, Borer ET, Seabloom EW, Cebrian J, Cleland EE, Elser JJ, Gruner DS, Harpole WS, Ngai JT, Smith JE (2015) Signatures of nutrient limitation and co-limitation: responses of autotroph internal nutrient concentrations to nitrogen and phosphorus additions. Oikos 124:113–121. https://doi.org/10.1111/oik.01215
Brown AD (1964) Aspects of bacterial response to the ionic environment. Bacteriol Rev 28:296–329
Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci USA 103:10316–10321. https://doi.org/10.1073/pnas.0600989103
Cleveland CC, Townsend AR, Schmidt SK (2002) Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems 5:0680–0691. https://doi.org/10.1007/s10021-002-0202-9
Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113. https://doi.org/10.1890/06-1847.1
Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214
Danger M, Daufresne T, Lucas F, Pissard S, Lacroix G (2008) Does Liebig’s law of the minimum scale up from species to communities? Oikos 117:1741–1751. https://doi.org/10.1111/j.1600-0706.2008.16793.x
Davidson EA, de Carvalho CJR, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Sabá RT, Hayashi SN, Leal EC, Vieira ICG, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–998. https://doi.org/10.1038/nature05900
Duah-Yentumi S, Ronn R, Christensen S (1998) Nutrients limiting microbial growth in a tropical forest soil of Ghana under different management. Appl Soil Ecol 8:19–24. https://doi.org/10.1016/S0929-1393(97)00070-X
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Gnankambary Z, Ilstedt U, Nyberg G, Hien V, Malmer A (2008) Nitrogen and phosphorus limitation of soil microbial respiration in two tropical agroforestry parklands in the south-Sudanese zone of Burkina Faso: the effects of tree canopy and fertilization. Soil Biol Biochem 40:350–359. https://doi.org/10.1016/j.soilbio.2007.08.015
Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862. https://doi.org/10.1111/j.1461-0248.2011.01651.x
Ilstedt U, Singh S (2005) Nitrogen and phosphorus limitations of microbial respiration in a tropical phosphorus-fixing acrisol (ultisol) compared with organic compost. Soil Biol Biochem 37:1407–1410. https://doi.org/10.1016/j.soilbio.2005.01.002
Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7. https://doi.org/10.1016/j.soilbio.2003.10.002
Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43. https://doi.org/10.1111/j.1461-0248.2007.01124.x
Kitayama K (2013) The activities of soil and root acid phosphatase in the nine tropical rain forests that differ in phosphorus availability on Mount Kinabalu, Borneo. Plant Soil 367:215–224. https://doi.org/10.1007/s11104-013-1624-1
Quesada CA, Lloyd J, Schwarz M, Patiño S, Baker TR, Czimczik C, Fyllas NM, Martinelli L, Nardoto GB, Schmerler J, Santos AJB, Hodnett MG, Herrera R, Luizão FJ, Arneth A, Lloyd G, Dezzeo N, Hilke I, Kuhlmann I, et al. (2010) Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7:1515–1541. https://doi.org/10.5194/bg-7-1515-2010
Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38. https://doi.org/10.1016/j.soilbio.2011.08.017
Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704. https://doi.org/10.1111/j.1469-8137.2011.03967.x
Mori T, Ohta S, Konda R, Ishizuka S, Wicaksono A (2010) Phosphorus limitation on CO2, N2O, and NO emissions from a tropical humid forest soil of South Sumatra, Indonesia. Int Conf Environ Eng Appl (ICEEA) 2010:18–21. https://doi.org/10.1109/ICEEA.2010.5596085
Mori T, Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A (2013a) Effects of phosphorus addition with and without ammonium, nitrate, or glucose on N2O and NO emissions from soil sampled under Acacia mangium plantation and incubated at 100% of the water-filled pore space. Biol Fertil Soils 49:13–21. https://doi.org/10.1007/s00374-012-0690-5
Mori Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A (2013b) Effects of phosphorus and nitrogen addition on heterotrophic respiration in an Acacia mangium plantation soil in South Sumatra, Indonesia. Tropics 22:83–87. https://doi.org/10.1111/j.1747-0765.2010.00501.x
Mori Ohta S, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A (2013c) Effects of phosphorus application on root respiration and heterotrophic microbial respiration in Acacia mangium plantation soil. Tropics 22:113–118. https://doi.org/10.1111/j.1747-0765.2010.00501.x
Mori T, Ishizuka S, Konda R, Wicaksono A, Heriyanto J, Hardjono A, Ohta S (2016a) Effects of phosphorus addition on N2O emissions from an Acacia mangium soil in relatively aerobic condition. Tropics 25:117–125
Mori T, Wachrinrat C, Staporn D, Meunpong P, Suebsai W, Matsubara K, Boonsri K, Lumban W, Kuawong M, Phukdee T, Srifai J, Boonman K (2016b) Contrastive effects of inorganic phosphorus addition on soil microbial respiration and microbial biomass in tropical monoculture tree plantation soils in Thailand. Agric Nat Resour 50:327–330. https://doi.org/10.1016/j.anres.2016.04.004
Mori T, Yokoyama D, Kitayama K (2016c) Contrasting effects of exogenous phosphorus application on N2O emissions from two tropical forest soils with contrasting phosphorus availability. Springer Plus 5:1237. https://doi.org/10.1186/s40064-016-2587-5
Mori T, Imai N, Yokoyama D, Mukai M, Kiyatama K (2017) Effects of selective logging and application of phosphorus and nitrogen on fluxes of CO2, CH4, and N2O in lowland tropical rainforests of Borneo. J Trop For Sci 29:248–256
Mori T, Lu X, Aoyagi R, Mo J (2018) Reconsidering the phosphorus limitation of soil microbial activity in tropical forests. Funct Ecol 32:1145–1154
Powers JS, Salute S (2011) Macro- and micronutrient effects on decomposition of leaf litter from two tropical tree species: inferences from a short-term laboratory incubation. Plant Soil 346:245–257. https://doi.org/10.1007/s11104-011-0815-x
Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Global Change Biol 18:1918–1927. https://doi.org/10.1111/j.1365-2486.2012.02639.x
Saito MA, Goepfert TJ, Ritt JT (2008) Some thoughts on the concept of colimitation: three definitions and the importance of bioavailability. Limnol Oceanogr 53:276–290. https://doi.org/10.4319/lo.2008.53.1.0276
Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316. https://doi.org/10.1111/j.1365-2745.2011.01904.x
Sayer EJ, Tanner EVJ (2010) Experimental investigation of the importance of litterfall in lowland semi-evergreen tropical forest nutrient cycling. J Ecol 98:1052–1062. https://doi.org/10.1111/j.1365-2745.2010.01680.x
Schreeg LA, Mack MC, Turner BL (2013) Nutrient-specific patterns in leaf litter solubility across 41 lowland tropical woody species. Ecology 94:94–105. https://doi.org/10.1890/11-1958.1
Shi L, Zhang H, Liu T, Zhang W, Shao Y, Ha D, Li Y, Zhang C, Cai X, Rao X, Lin Y, Zhou L, Zhao P, Ye Q, Zou X, Fu S (2016) Consistent effects of canopy vs. understory nitrogen addition on the soil exchangeable cations and microbial community in two contrasting forests. Sci Total Environ 553:349–357. https://doi.org/10.1016/j.scitotenv.2016.02.100
Teklay T, Nordgren A, Malmer A (2006) Soil respiration characteristics of tropical soils from agricultural and forestry land-uses at Wondo Genet (Ethiopia) in response to C, N and P amendments. Soil Biol Biochem 38:125–133. https://doi.org/10.1016/j.soilbio.2005.04.024
Tobon C, Sevink J, Verstraten J (2004) Litter ow chemistry and nutrient uptake from the forest oor in northwest Amazonian forest ecosystems ´. Biogeochemistry 69:315–339
Tripler CE, Kaushal SS, Likens GE, Todd Walter M (2006) Patterns in potassium dynamics in forest ecosystems. Ecol Lett 9:451–466. https://doi.org/10.1111/j.1461-0248.2006.00891.x
Turner BL, Wright SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130. https://doi.org/10.1007/s10533-013-9848-y
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Wagai R, Kitayama K, Satomura T, Fujinuma R, Balser T (2011) Interactive influences of climate and parent material on soil microbial community structure in Bornean tropical forest ecosystems. Ecol Res 26:627–636. https://doi.org/10.1007/s11284-011-0822-7
Weed SB, Davey CB, Cook MG (1969) Weathering of mica by fungi. Soil Sci Soc Am J 33:702–706
Wright SJ, Yavitt JB, Wurzburger N, Turner BI, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625. https://doi.org/10.1890/10-1558.1
Xu X, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749. https://doi.org/10.1111/geb.12029
Xun W, Huang T, Zhao J, Ran W, Wang B, Shen Q (2015) Soil biology & biochemistry environmental conditions rather than microbial inoculum composition determine the bacterial composition, microbial biomass and enzymatic activity of reconstructed soil microbial communities. Soil Biol Biochem 90:10–18. https://doi.org/10.1016/j.soilbio.2015.07.018
Yamashita N, Ohta S, Hardjono A (2008) Soil changes induced by Acacia mangium plantation establishment: comparison with secondary forest and Imperata cylindrica grassland soils in South Sumatra, Indonesia. For Ecol Manage 254:362–370. https://doi.org/10.1016/j.foreco.2007.08.012
Yamashita N, Ohta S, Sase H, Kievuttinon B, Luangjame J, Vsaratana T, Grivait H (2011) Seasonal changes in multi-scale spatial structure of soil pH and related parameters along a tropical dry evergreen forest slope. Geoderma 165:31–39. https://doi.org/10.1016/j.geoderma.2011.06.020
Zhang W, Shen W, Zhu S et al (2015) CAN canopy addition of nitrogen better illustrate the effect of atmospheric nitrogen deposition on forest ecosystem? Sci Rep 5:11245. https://doi.org/10.1038/srep11245
Acknowledgements
We appreciate four anonymous reviewers who gave us constructive comments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Project funding: This study was financially supported by National Natural Science Foundation of China (NO. 41731176, 41650110484,), Grant-in-Aid for JSPS Postdoctoral Fellowships for Research Abroad (28 601), and the Youth Innovation Promotion Association, CAS (No. 2015287).
The online version is available at http://www.springerlink.com
Corresponding editor: Zhu Hong.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Mori, T., Wang, S., Wang, Z. et al. Testing potassium limitation on soil microbial activity in a sub-tropical forest. J. For. Res. 30, 2341–2347 (2019). https://doi.org/10.1007/s11676-018-0836-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11676-018-0836-x