Ecol Res (2017) 32: 145–156 DOI 10.1007/s11284-016-1425-0
O R I GI N A L A R T IC L E
Kei-ichi Okada
•
Shin-ichro Aiba • Kanehiro Kitayama
Influence of temperature and soil nitrogen and phosphorus availabilities on fine-root productivity in tropical rainforests on Mount Kinabalu, Borneo
Received: 20 February 2016 / Accepted: 9 December 2016 / Published online: 24 December 2016 The Ecological Society of Japan 2016
Abstract We investigated how temperature and nutrient availability regulate fine-root productivity in nine tropical rainforest ecosystems on two altitudinal gradients with contrasting soil phosphorus (P) availabilities on Mount Kinabalu, Borneo. We measured the productivity and the nutrient contents of fine roots, and analyzed the relationships between fine-root parameters and environmental factors. The fine-root net primary productivity (NPP), total NPP, and ratio of fine-root NPP to total NPP differed greatly among the sites, ranging from 72 to 228 (g m2 year1), 281–2240 (g m2 year1), and 0.06–0.30, respectively. A multiple-regression analysis suggested a positive effect of P availability on total NPP, whereas fine-root NPP was positively correlated with mean annual temperature and with P and negatively correlated with N. The biomass and longevity of fine roots increased in response to the impoverishment of soil P. The carbon (C) to P ratio (C/ P) of fine roots was significantly and positively correlated with the P-use efficiency of above-ground litter production, indicating that tropical rainforest trees dilute P in fine roots to maintain the C allocation ratio to these roots. We highlighted the mechanisms regulating the fine-root productivity of tropical rainforest ecosystems in relation to the magnitude of nutrient deficiency. Electronic supplementary material The online version of this article (doi:10.1007/s11284-016-1425-0) contains supplementary material, which is available to authorized users. K. Okada (&) Æ K. Kitayama Graduate School of Agriculture, Kyoto University, Kyoto, Japan E-mail:
[email protected] Tel.: +81-45-3394370 K. Okada Graduate School of Environment and Information Sciences, Yokohama National University, Yokohama, Japan S. Aiba Graduate School of Science and Engineering, Kagoshima University, Kagoshima, Japan
The trees showed C-conservation mechanisms rather than C investment as responses to decreasing soil P availability, which demonstrates that the below-ground systems at these sites are strongly limited by P, similar to the above-ground systems. Keywords Altitudinal gradient Æ Carbon allocation Æ Above- and below-ground interaction Æ Soil P depletion Æ Fine-root turnover
Introduction Fine roots play an essential role in nutrient acquisition to sustain the structure and function of forest ecosystems (Wright et al. 2011). Fine-root productivity is the major component of below-ground net primary productivity (NPP) (Malhi et al. 2011), indicating that tree species allocate a disproportionately greater amount of carbon (C) to construct fine roots than to construct coarse ones. The mean ratio of fine-root NPP to coarseroot NPP is 8.9 (ranging from 2.0 to 19.2) in tropical forests (Araga˜o et al. 2009; Malhi et al. 2009; Girardin et al. 2010; Moser et al. 2011). Fine-root NPP is the product of two factors; the total NPP multiplied by the ratio of C allocated to fine-root production to the C of the total NPP. The amount of C trees allocate to fineroot production probably depends on the availability of assimilated C (i.e., total NPP per se) and on strategies for mining resources such as mineral nutrients (i.e., the demand for minerals). Carbon allocation to fine roots is considered to be an investment in nutrient acquisition, and it is probably a trade-off against C allocation to leaf production, which is an investment in C assimilation (Bloom et al. 1985; Ericsson 1995; Dybzinski et al. 2011; Malhi et al. 2011). Hendricks et al. (1993) suggested two models of C allocation to fine-root production per total NPP in response to nitrogen (N) availability to explain the com-
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monly observed patterns of increasing fine-root biomass with decreasing N availability. The first model assumes an increasing ratio of C allocation to fine-root production to total NPP and a constant turnover rate of fine roots with decreasing N availability (hereafter called the ‘differential allocation hypothesis’). The second model assumes a constant ratio of C allocation to fine-root production to total NPP and a decreasing turnover rate of fine roots with decreasing N availability (hereafter called the ‘constant allocation hypothesis’). In both models, fine-root biomass increases in N-deficient sites. These models are based on N deficiency, whereas the responses of fine-root biomass to deficiencies of other nutrients, such as phosphorus (P), have never been tested. Many studies on tropical rainforest ecosystems have focused on fine-root dynamics in relation to nutrient availability, and an increase in fine-root biomass has been observed at some nutrient-deficient sites (e.g. Vitousek and Sanford 1986; Araga˜o et al. 2009), as reported by Hendricks et al. (1993). However, the dependence of total NPP and C allocation to fine-root production on resource availability, especially nutrients, has not been systematically investigated in the tropics, especially Southeast Asia. The altitudinal-transect approach has been extensively and intensively used to investigate the environmental factors regulating the NPP in tropical forest ecosystems. Altitudinal transects on tropical mountains are particularly useful to investigate the effect of air temperature on ecosystem processes, because the mean temperature reduces linearly on tropical mountain slopes without the effects of winter coldness (Raich 1998; Kitayama and Aiba 2002; Graefe, Hertel and Leuschner 2008; Girardin et al. 2010; Moser et al. 2011). Belowground processes on altitudinal transects on tropical mountains should be interpreted with caution, because the soil nutrient availabilities are strongly affected by temperature and can co-vary with altitude (Graefe et al. 2008). The regulation of organic matter decomposition and mineralization, and hence the availability of inorganic nutrients such as N, are dependent on temperature (Pregitzer and King 2005). Furthermore, thermal effects on soil weathering can form an altitudinal pattern in the availability of elements such as P, which are derived from mineral weathering. Consequently, P is generally limiting at low altitudes because of the geochemical constraints associated with soil weathering, whereas N is limiting at high altitudes on tropical mountains (Tanner et al. 1998). Two studies have reported on fine-root productivity along such tropical altitudinal transects (Girardin et al. 2010; Moser et al. 2011). However, they showed inconsistent trends in fine-root productivity in relation to altitude. The ratio of C allocation to fine-root production to total NPP was found to increase with increasing altitude on an Ecuadorian altitudinal transect (Moser et al. 2011), consistent with the differential allocation hypothesis. Consequently, both the NPP and biomass of fine roots were found to increase upslope. However, no significant trend was found in the ratio of C allocation to
fine-root production to total NPP on an Andes–Amazon transect (Girardin et al. 2010). Instead, the data indicated that there was an increasing C residence time in fine roots, suggesting that the turnover rate of fine roots became slower and that the fine-root biomass increased with increasing altitude, consistent with the constant allocation hypothesis. The non-significant trend in the ratio of C allocation to fine-root production on the Andes–Amazon transect (Girardin et al. 2010) may reflect the antagonistic effects of N and P along the altitudinal transect. Trees may respond to decreased P availability downslope, and to decreased N availability upslope. In addition, the total NPP per se must depend on altitude via temperature and nutrients. However, it is unknown how total NPP and the ratio of C allocation to fine-root production respond to temperature and to N and P availabilities independently. In this study, we investigated the independent effects of the mean annual air temperature (MAT) and N and P availabilities and their interactions on fine-root NPP using altitudinal transects on Mount Kinabalu. In general, N availability varies as a function of altitude (Hall et al. 2004). In addition, the soils derived from ultrabasic rocks, which are distributed across all altitudes on Mount Kinabalu (Aiba and Kitayama 1999; Kitayama and Aiba 2002), have much lower P availability compared with other geological substrates. Therefore, one can test the interaction of altitude and P (N) availabilities in this setting (Kitayama and Aiba 2002). We particularly focused on the effects of P availability on fineroot NPP because P is known to limit ecosystem processes in forests on deeply weathered soils, which are widespread in the tropics (Vitousek 1984; Elser et al. 2007; Hidaka and Kitayama 2009; Lambers et al. 2009). Second, we determined how trees adjust N and P investments in fine roots in relation to N and P availabilities. Trees commonly dilute P in the leaves in response to decreased P availabilities, which is a mechanism of increasing P-use efficiency; however, they do not dilute N in the leaves in response to reduced N availabilities, suggesting that there are divergent patterns of N versus P investment (Wright et al. 2004; Hidaka and Kitayama 2009; Reich et al. 2010). Several studies have also suggested a divergent pattern in N versus P investment in fine roots. A fertilization experiment on a natural fertility gradient along a soil chronosequence revealed a remarkable increase in the P concentration in fine roots after P fertilization; but there was no change N concentration in fine roots after N fertilization (Ostertag 2001). In a latitudinal meta-analysis of fine-root nutrient concentrations, the P concentration increased with increasing latitude, whereas the N concentration remained relatively constant, although soil P availability increased and soil N availability decreased (Yuan et al. 2011). The differential pattern of P versus N investment in fine roots needs to be substantiated in relation to the in situ availabilities of both P and N. Consequently, we addressed the dynamics of, and nutrient investment in, fine roots along two parallel
MAT mean annual air temperature, MAP mean annual precipitation, AGB above-ground biomass, ANPP above-ground net primary productivity, NUEabove-ground litter N-use efficiency in above-ground litter production, PUEabove-ground litter P-use efficiency in above-ground litter production
Lower montane rain forest 8.36 4.70 1418 31.8 1 2714 17.3
32.1
4.67 5.17 5.26 5.32 1873 903 681 197 67.7 24.3 13.1 5.5 1 0.2 0.2 0.06 2509 2714 2085 3285 23.7 17.3 12.3 10.7
65.4 22.6 14.2 6.1
4.59 4.89 4.85 4.89 2101 1141 819 879 40.5 29.4 28.0 19.5 1 1 0.25 0.2 46.8 30 20.6 15 2509 2714 2085 3285 23.9 18.9 13.3 10.6
NUEabove-ground (Ln) ANPP (g m2 year1) AGB (kg m2) Plot size (ha) Canopy (m) MAP (mm) MAT (C) Exact altitude (m)
Sedimentary site 700 650 1700 1560 2700 2590 3100 3080 Ultrabasic site 700 700 1700 1860 2700 2700 3100 3050 Quaternary site 1700 1860
For soil N availability, we referred to published values of the pool size and the mineralization rate of soil inorganic N at these sites (Kitayama et al. 1998; Kitayama and Aiba
Common altitude (m)
Soil N and P availabilities
Table 1 Description of nine forest sites in this study on Mount Kinabalu, Borneo
A total of nine tropical evergreen rainforests were selected from an altitudinal range of 650 m to 3080 m on Mount Kinabalu (4095 m, 65¢N, 11633¢E), Borneo, with another montane forest in addition to the eight matrix forests (Table 1). The climate at the study sites is humid equatorial with little seasonality in monthly mean air temperature. The annual mean air temperature on the mountain changes predictably with the lapse rate of 0.55 C per 100 m (Kitayama 1992). The mountain is non-volcanic and largely consists of Tertiary sedimentary rocks of sandstone and/or mudstone below 3000 m and of granitic rock above 3000 m. Ultrabasic rocks protrude from the sedimentary rocks as mosaics. Four forests were selected on each substrate (sedimentary and ultrabasic soils) at 700, 1700, 2700, and 3100 m, at the same environmental setting as that studied by Aiba and Kitayama (1999), yielding a total of eight forests in a matrix of four altitudes and two substrates. The ninth forest was located at 1700 m on sedimentary substrate originating from Quaternary tilloid deposits of mostly sedimentary rocks (hereafter referred to as Quaternary substrate) (Kitayama et al. 2004). This ninth site on the Quaternary substrate was more fertile than those on Tertiary sedimentary rocks because of the younger geological age and less weathered rock. This site on the Quaternary substrate was selected to compare the ecosystem structure over a wide fertility gradient. All sites were located on gentle slopes to avoid the effects of topography. We used these nine forests to address our two research questions. A description of the study sites is provided in Table 1. The vegetation, ecosystem properties, and location map of the sites can be found in Aiba and Kitayama (1999), Kitayama and Aiba (2002), and Kitayama et al. (2004).
litter
Site description
8.42 9.73 9.62 10.23
Materials and methods
8.47 8.83 8.53 8.6
PUEabove-ground (Ln)
litter
Forest type
1. How do the ratio of C allocation to fine roots to total NPP and the turnover rate and biomass of the fine roots vary with air temperature and availabilities of N and P? 2. How do the N and P investments in fine roots change with different N and P availabilities?
Lowland dipterocarp rain forest Lower montane rain forest Upper montane rain forest Subalpine scrub
transects that constitute an altitudinal–geological matrix at four elevations (700, 1700, 2700, 3100 m) and on two geological substrates (sedimentary and ultrabasic rock) on Mount Kinabalu, Borneo. We addressed the following two questions:
Lowland dipterocarp rain forest Lower montane rain forest Upper montane rain forest Subalpine forest
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13.55 Data cited from Kitayama et al. (1998, 2000, 2004), Takyu et al. (2002), Kitayama and Aiba (2002), and Kitayama (2013) Labile Po, Labile organic P ND not detectable
0.19 7.79 19.3 0.56 12.95
11.5
4.71 0.82 0.67 0.63 0.14 0.04 0.09 0.07 8.5 1.6 0.4 2.2 7.2 0.8 0.8 ND 0.21 0.28 0.35 0.26 11.4 12.1 9.9 13.3
8.9 26.6 7.3 5.2
2.23 3.5 2.79 2.94 0.18 0.14 0.36 0.35 19.9 0.01 1.3 5.5 10.2 1.8 2.9 8.4 3.9 23 29.9 4.8 0.21 0.32 0.92 0.6
Soluble P (g m2) N mineralization (lg g1 10 days1) NO3-N (lg g1) NH4-N (lg g1) Total N (%) C/N ratio
13.8 13.7 19.2 14.3
Sedimentary site 700 4.1 1700 4 2700 3.4 3100 4.9 Ultrabasic site 700 4.5 1700 5.4 2700 5.1 3100 5.3 Quaternary site 1700 4.2
In this study, the above-ground biomass was estimated by the equations of Chave et al. (2005) incorporating wood density and tree height. Moist-forest equations were used for the lowland plots and wet-forest equations were used for the montane and subalpine plots. The wood density,
PH (H2O)
Estimation of above-ground biomass and net primary productivity
Table 2 Soil chemical properties and soil N and P availability indices at nine study sites on Mount Kinabalu, Borneo
2002; Takyu et al. 2002; Kitayama et al. 2004) (Table 2; sampling year of analyzed soil is shown in Table S1). The N availability as indexed by these values in the topsoil (0–15 cm) varied with altitude and geological substrate. The net N mineralization rate in situ, which was measured using the buried bag method (Kitayama et al. 1998), decreased from 700 to 2700 m and then increased slightly at 3100 m on the sedimentary substrate. On the ultrabasic substrate, the net N mineralization rate decreased linearly with altitude. The pool size and mineralization rate of the soil inorganic N may vary with time, reflecting meteorological conditions. However, several more recent studies, including Hall et al. (2004), Ushio et al. (2015) and an unpublished study conducted at the same sites indicate consistent patterns, as reported by Kitayama et al. (1998). Therefore, the N values based on Kitayama et al. (1998) legitimately represent N availability of these sites, despite having been reported more than 15 years ago (Table S1). For soil P availability, we also referred to the values of the pool size of soluble inorganic P and labile organic P at these sites published by Aiba and Kitayama (1999) and Kitayama et al. (2004) (sampling year of the analyzed soil is shown in Table S1). The soluble inorganic P was extracted with a hydrochloric-ammonium fluoride solution, and the labile organic P was extracted by a 0.5 M NaHCO3 solution (CO3-Po; Tiessen and Moir 1993). The size of the soluble inorganic P pools varied greatly among the study sites due to the differences in geology and weathering as a function of altitude (Wagai et al. 2008). The soluble inorganic P pool was always larger on the sedimentary substrate than on the ultrabasic substrate at the same altitude (Kitayama et al. 2000; Kitayama and Aiba 2002; Table 2). Among the three forests at 1700 m, the soluble inorganic P pool was larger on the Quaternary substrate than on the other two substrates, reflecting the relatively young age of the Quaternary substrate; Table 2). We used indexes of both the inorganic and organic soil P pools to develop models to explain the fine-root biomass and productivity (as described in the paragraph on GLMs in the statistical analysis). Labile organic P is an important P resource for trees because the CO3-Po pool is significantly correlated with root acid phosphatase activity at these sites (Kitayama 2013). In our case, the variation in the soil P fractions reflects the soil types and geology; thus, the between-site variation in soil P must be stable and consistent over time. Therefore, we believe that the indexes of soil P availabilities based on these previous studies are still valid.
Labile Po (g m2)
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which is defined as oven-dry mass divided by sample volume (fresh weight) (Cornelissen et al. 2003), was measured for the dominant species using wood samples collected by an increment borer (Seino, Okada and Tsujii, unpublished data). The number of samples per species ranged from one to seven, and the length of the sample also varied. For other species, the data (average if two or more values are reported) were extracted from the database of Chave et al. (2009); the genus-average value was used for species that were not found in the database. For indeterminate species, the plot-specific average value was used. The tree height (H, in m) was estimated from DBH (D, cm) using the following rectangular hyperbola equation (Kitayama and Aiba 2002): H ¼ 1=ðADÞ þ 1=H where A and H* are plot-specific parameters and H* is the asymptotic tree height. The two parameters of the equation were determined by non-linear regressions, as reported by Kitayama and Aiba (2002) and Kitayama et al. (2004), based on subsamples of trees for which both tree height and DBH were measured. The aboveground biomass increment (g m2 year1) was calculated for the surviving trees in August–September in 2011 and in August–September 2013 as the biomass difference divided by the census interval (days) multiplied by 365. Small contributions by newly recruited trees in 2013 were neglected. The above-ground NPP (ANPP) was calculated as the sum of the above-ground biomass increment and the above-ground litterfall (Table 1). The above-ground litterfall at each site was derived from the mean value of the 10-year observations between 1996 and 2006, as reported in Kitayama et al. (2015). Measurements of fine-root biomass and productivity We determined the fine-root biomass and productivity in the topsoils to a depth of 15 cm at all sites. The adequacy of the sampling depth (15 cm) was investigated previously by Kitayama and Aiba (2002), who found that the root density was highest in the upper layer (0–5 cm deep) at all study sites except for the 1700-m ultrabasic site. Moreover, the bulk (61.8–90.9%) of the fine-root biomass within 30-cm depth occurred in the upper 0–15 cm layer (Table S2) at all sites. Therefore, we investigated the fine-root biomass and productivity within a 15-cm depth at all sites for consistency. From August to September 2013, ten soil cores to a 15-cm depth (32 mm in diameter) were collected at 10-m intervals along a transect that started from a random point at each site. The soil cores were immediately transported to the laboratory. The soil samples were gently rinsed with tap water to remove soil particles, and all live roots
