matrix of elevations and geological substrates on Mount ... Mt Kinabalu, Borneo, is characterized by a deep elevational gradient and mosaics of geological ...
Ecological Research (1998) 13, 301±312
Soil nitrogen mineralization rates of rainforests in a matrix of elevations and geological substrates on Mount Kinabalu, Borneo KANEHIRO KITAYAMA,1* SHIN-ICHIRO AIBA,2 NOREEN MAJALAP-LEE3 OHSAWA4
AND
MASAHIKO
1
Japanese Forestry and Forest Products Research Institute, PO Box 16, Tsukuba Norin Kenkyu Danchi, Ibaraki 305-8687, Japan, 2Graduate School of Environmental Earth Science, Hokkaido University, Sapporo 060-0810, Japan, 3Forest Research Center, Forestry Department, PO Box 1407, 90715 Sandakan, Sabah, Malaysia and 4Faculty of Natural Sciences, Chiba University, Chiba 263-8522, Japan
Mt Kinabalu, Borneo, is characterized by a deep elevational gradient and mosaics of geological substrates. We chose a pair of two geological substrates (sedimentary vs ultrabasic) at ®ve altitudes (800, 1400, 2100, 2700 and 3100 m a.s.l.). We investigated soil nitrogen (N) mineralization and nitri®cation rates using an incubation technique to assay the pattern and control of soil N status in this environmental matrix. In situ net mineralization rates decreased with elevation on both substrates. The decreasing pattern was linear across altitudes on ultrabasic rock, whereas on sedimentary rock it was depressed in the middle slope wet cloud zone. Sedimentary sites in this zone had low soil redox potential values and this anoxic soil condition might be related to slow N mineralization. The in situ rates were signi®cantly greater (P < 0.05, ANOVA) on sedimentary than on ultrabasic rock at the same altitudes except in the cloud zone. Net mineralization rates of the soils that were collected from different elevations and incubated in the same conditions were statistically invariable (P > 0.05) among the original elevations for sedimentary rock, but were variable (P < 0.05) for ultrabasic rock. Those of the soils that were collected from the same elevation and incubated at different elevations decreased signi®cantly across altitudes (P < 0.05) for sedimentary rock, while they were invariable (P > 0.05) for ultrabasic rock. Thus, temperature had stronger effects on net N mineralization on sedimentary rock, whereas inherent soil quality had stronger effects on ultrabasic rock. Controls of soil N mineralization might be different between the two substrates, leading to diverse biogeochemical site conditions on Kinabalu. Key words: geological substrates; net N mineralization; redox potential; temperature gradient, tropical rainforest.
INTRODUCTION Slopes of tropical high mountains represent a steep elevational gradient without marked thermal seasonality. If extreme moisture or soil conditions are not limiting, the vegetation generally decreases in species diversity, stature, biomass and produc-
*Email: Present address: Environmental Sciences, Faculty of Science, Kagoshima University, Kagoshima 890-0065, Japan. Received 12 January 1998. Accepted 28 May 1998.
tivity with increasing elevation (Whitmore 1975; Ohsawa et al. 1985; Heaney & Proctor 1990; Kitayama 1992, 1994). Although most studies presume that elevation represents decreasing temperature, which may explain these vegetation changes, in reality elevational gradients consist of a complex of factors. Thus, discussing the causes of vegetation patterns on such a gradient often becomes paradoxical, while correlating the patterns with factors is less dif®cult. For instance, the diminished availability of soil nitrogen (N) due to the cooler temperatures at higher elevations has been hypothesized to be a cause of the stunting of tropical montane forests (Grubb 1977; Tanner 1985; Vitousek & Sanford 1986; Marrs et al. 1988).
302
K. Kitayama et al.
By contrast, Leigh (1975) claims that the suppressed uptake of soil N due to humid air limits plant growth more strongly than the slow rate of N supply in the soil. Mount Kinabalu (4101 m a.s.l.; in the Bornean state of Sabah, Malaysia) is a tropical mountain where climatic factors change in a variable manner to each other with increasing elevation (Kitayama 1992, 1994). Different geological substrates add to the complexity of Kinabalu's gradient (Jacobson 1970). The Mount Kinabalu area demonstrates the mosaics of discrete serpentine plant communities at various altitudes within `zonal' vegetation on sedimentary rock (Kitayama 1991). Serpentine or serpentinized ultrabasic rocks contain high concentrations of Fe, Mg, Ni, Cr and Co, but low concentrations of Ca, K and P (Brooks 1987; Brunotte & Kitayama 1987; Proctor et al. 1988). Excessive elements (particularly Ni) are potentially toxic to plants and this, together with the de®ciency of Ca, K and P, may explain the stunted vegetation and high species endemism on ultrabasic rock (Brooks 1987). A few accounts, however, indicate that serpentine vegetation is similar to zonal vegetation at lower elevations, but becomes more distinct with increasing elevation (Corner 1978; Proctor et al. 1988; Bruijnzeel et al. 1993). Thus, interactions between climate and substrate may operate differently on vegetation processes at different altitudes. Mount Kinabalu presents a rare case where one can study biogeochemical processes under relatively well-controlled temperature and substrate conditions, because the two substrates (sediTable 1
mentary and ultrabasic) occur side by side at a range of altitudes. We analyzed the pattern and control of net soil N mineralization and nitri®cation rates (hereafter collectively N transformation rates) in this controlled environmental setting. The purpose was to assay the nature of altitude±substrate interactions by translocation treatments rather than to investigate the net N supplying potentials per se. METHODS Study areas A full description of Kinabalu's environments is given by Kitayama (1992). Brie¯y, Kinabalu (4101 m a.s.l., 6°5¢N, 116°33¢E) is the highest mountain in South-East Asia. The main massif and adjacent areas are designated as state park and contain a continuum of pristine vegetation. Rainforests occur from 300 m a.s.l. to the forest limit at about 3700 m a.s.l. Climate is humid tropical with weak in¯uences of Asiatic monsoon. Mean annual air temperature is 27.5°C at 0 m with a mean lapse rate of 0.0055°C m)1. Mean annual precipitation is relatively invariable across altitudes, and ranges from 2300 to 2900 mm (Table 1; year 1996±1997; K. Kitayama, unpubl. data). However, mean saturation de®cits decrease with increasing altitude as a function of decreasing air temperature. The middle slope from 2000 to 2800 m corresponds to a cloud zone and its air and soils are wetter than expected from the air temperature alone (Table 1).
Description of sites studied
Estimated air temperature (°C) Annual rainfall (mm) Mean saturation de®cit (kPa) Mean vapor pressure (kPa) Mean soil-water potential (kPa) Exact altitude (m) Sedimentary rock Ultrabasic rock
800
1400
23.1 2389 0.53 2.58 )32.26
19.8 NA NA NA NA 1380 1470
800 860
Altitude (m) 2100
2700
3100
15.9 2376* 0.23* 1.89* ±5.89*
12.6 2253 0.14 1.27 ±3.81
10.4 2887 0.23 0.97 NA
2170 2010
2670 2800
3140à 3110
Climatic values are the means measured in two years from 1996 to 1997. *Altitude from 1700 m. Altitude from 3300 m. àSite underlain by granite, not sedimentary rock. NA, not available.
Soil N mineralization on Kinabalu The geological substrates below about 2700 m are mostly tertiary sedimentary rock with mosaics of ultrabasic rocks (Jacobson 1970). Granite rock dominates above about 3000 m. Within this array of substrates, we chose a pair of two contrasting sites (sedimentary vs ultrabasic rocks) at each of 800, 1400, 2100, 2700 and 3100 m (Table 1). Rock types were identi®ed based on nearby outcrops. We could not ®nd a sedimentary site at 3100 m and this site was substituted for one on granite rock. Sedimentary rock consists largely of sandstone and mudstone of the Eocene Trusmadi Formation, ultrabasic rock largely of serpentinized peridotite on this mountain (Jacobson 1970). Peridotite is remarkably high in Mg, and very low in P (SiO2 40.94%, TiO2 0.14%, Al2O3 3.97%, Fe2O3 3.87%, FeO 4.28%, MnO 0.12%, MgO 36.28%, CaO 2.63%, Na2O 0.08%, K2O 0.03%, H2O & CO2 7.51%, P2O5 0.02%; Jacobson 1970). Chemical composition of granite is given as: SiO2 59.39%, TiO2 0.60%, Al2O3 14.19%, Fe2O3 3.28%, FeO 4.68%, MnO 0.11%, MgO 3.66%, CaO 5.85%, Na2O 3.70%, K2O 3.18%, H2O & CO2 1.12%, P2O5 0.35%. Analysis of sedimentary rock is not available, but it generally contains > 50% quartz (Jacobson 1970). All sites were on gentle slopes or broad ridge tops. Controlling elevation was not always possible and the difference in elevation between paired sites ranged up to 160 m (e.g. 2100 m, Table 1), corresponding to a temperature difference of 0.88°C. These differences were not corrected in statistical procedures. Vegetation analysis We characterized aboveground vegetation by using the point-centered quarter method (Mueller-Dombois & Ellenberg 1974), a rapid inventory method without a bounded quadrat. We placed several line transects in each of the ®ve sites on ultrabasic rock. Sampling points were placed in 10 m intervals along the transects, and diameter at breast height (d.b.h.) of the tree (P 10 cm d.b.h.) closest to each point was measured in each quarter. A voucher specimen (mostly infertile) was collected from each tree. The inventory was terminated after 100 trees were measured in each site. In addition, the height of the tallest canopy tree was measured in each site.
303
Comparable data were collected for the forests on sedimentary rock using the same method by Kitayama (1992). We adopted these data for a comparison. Details of the structure and species composition of these forests are described by Aiba & Kitayama (in press). Soil analyses General procedures of soil analyses and incubation follow Vitousek et al. (1983, 1992). Four 20±50 m transects were laid out, each from a random point, in each of the 10 sites in May 1995. We collected 10 15-cm-deep soil cores beneath the litter layer by forcing a core sampler (37 mm diameter) systematically along each transect, and combined the 10 cores into one composite. This resulted in four composites per site. The collected samples were then stored in a refrigerator. The fresh composite samples were homogenized manually within 48 h, the visible ®ne to coarse roots and stones (> 2 mm) were removed, and weighed. A subsample of each composite was oven-dried at 105°C for 48 h to determine water content gravimetrically. The rest of each composite was divided into four subsamples and approximately 10 g (fresh weight) of each subsample was placed in a 10 ´ 15 cm sealable polyethylene bag. The ®rst set of subsamples was used for initial extraction, the second set to determine net N transformation rate in each site (called `in situ' treatment), the third set to investigate in¯uences of substrate on rate by placing all under the same temperature (`common site' treatment), and the fourth set to investigate the in¯uences of phosphate fertilization on the rate (`phosphate' treatment). In addition, subsamples of each composite (10 g fresh weight) from the 800 m sedimentary and ultrabasic sites were prepared to investigate in¯uences of temperature by placing the same soils at different altitudes (`common soil' treatment). Initial extraction
One of the four subsamples was extracted with 100 ml 1.5 N KCl for initial NO3 and NH4, and extractable Ca, Mg and Mn. The soil solution mixture was shaken vigorously for 0.5 h, equilibrated for 12 h, and ®ltered through Whatman no. 2 ®lter paper (Whatman International, Maidstone, Kent, UK). The ®lter paper was
304
K. Kitayama et al.
rinsed beforehand with about 50 ml blank KCl. The soil ®ltrate was immediately stored in a refrigerator for up to 14 days. In situ treatment
A set of sub/samples, loosely sealed to permit aeration, was returned to the original sites. The samples in each site were kept in a large, untied polyethylene bag to protect them from rain, and buried under litter. Common site treatment
A set of subsamples was incubated in the dark in the laboratory at 1700 m (mean air temperature of 20.5 0.4°C). The samples were loosely sealed, and kept in a large polyethylene bag with watersaturated cotton to maintain constant soilmoisture. Phosphate treatment
Another set of subsamples received phosphate at the rate of 50 lg P g)1 oven-dry soil as NaH2PO4 solution. The NaH2PO4 solution was adjusted to an appropriate concentration (approximately 0.01 N) so that the applied solution was always less than 0.5 ml so as not to saturate the soils. The phosphate-treated samples were incubated together with the common site samples, the latter being used as controls for the phosphate treatment. Common soil
Sub-samples from the 800 m sites were translocated to two different altitudes (2700 and 3100 m), and were compared with the 800 m in situ samples. Similarly, the common site samples from 800 m served as the common soil of 1700 m. In addition, one set of the 800 m subsamples was incubated at 27.0 0.5°C, the predicted average air temperature at 0 m. After 10 days of incubation, all samples were collected, stored in a refrigerator, and ®nal NO3 and NH4 extracted within 48 h using the same method as the initial extraction. Extracts and bulk samples of fresh soils were analyzed at the Chemistry Laboratory of the Sabah Forestry Research Center. NO3- and NH4-N concentrations were determined colorimetrically using a Burkard SFA-2 autoanalyzer (Burkard Scienti®c, Middx, UK). Net nitri®cation rate was calculated as ®nal minus initial NO3-N, and net mineral-
ization rate was calculated as ®nal minus initial (NO3 + NH4)-N. Concentrations of exchangeable Ca and Mg were determined on each initial extract by atomic absorption spectrometry. Organic C was determined on fresh soil by the Walkley-Black wet digestion method. Total N was digested by the micro Kjeldahl procedure with concentrated sulfuric acid, and determined colourimetrically on the autoanalyzer. Soluble P was extracted with hydrochloric-ammonium ¯uoride solution, and determined colorimetrically. Soil pH was measured on a 1:1 fresh soil to deionized water solution. Soil redox potential was determined in situ to estimate the effects of soil moisture on N transformation using platinum electrodes, a calomel reference electrode and a portable pH/mV meter (D12, Horiba, Kyoto, Japan). A platinum electrode consisted of a platinum rod (10 mm long, 1.2 mm diameter) soldered to a copper rod (Faulkner et al. 1989). Ten platinum electrodes were inserted to 15-cm depth at 5-m intervals along a 50-m transect, and allowed to stand for 50 min before measurement. Readings were corrected to standard hydrogen reference electrode values (+248 mV) at pH 7.0 (Eh7) (± 59 mV per unit pH increase).
RESULTS Forest properties Vegetation changed with elevation on both substrates (Table 2). Canopy height and basal area were similar at 800 m between the substrates, indicating that aboveground biomass should also be similar. The number of species per 100 trees, basal area and canopy height decreased upslope more on ultrabasic than on sedimentary rock. Canopy trees were shorter, slender and included fewer species at high elevations on ultrabasic than on sedimentary rocks. Tree density at 3100 m on ultrabasic rock was reduced more than would be expected from an elevational pattern alone; this is due to the artifact of applying the same threshold criterion (P10 cm d.b.h.) to small trees, the majority of which fall below the criterion in the ultrabasic site.
Soil N mineralization on Kinabalu Table 2
305
Vegetation properties investigated in the sites on Mount Kinabalu 800
No. species per 100 trees Sedimentary rock Ultrabasic rock Total basal area (m2 ha)1) Sedimentary rock Ultrabasic rock Upper canopy height (m) Sedimentary rock Ultrabasic rock Density (trees ha)1) Sedimentary rock Ultrabasic rock
1400
Altitude (m) 2100
2700
3100
90 68
60 42
23* 26
12 14
15 2
33.4 39.1
34.0 47.5
59.5* 36.6
49.2 31.6
55.4 11.7
50 50
30 21
20* 22
20 15
10 6
333 551
447 1326
778* 1071
659 1098
1950 634
*Values are from the site located at 2350 m. Approximate values.
Soil properties Water content increased from 27% at 800 m to 70% at 2100 m, and then declined upslope on sedimentary rock (Table 3). The middle-slope increase in water content was less distinct on ultrabasic rock. These patterns were closely associated with soil redox potential (Fig. 1). Redox values were signi®cantly variable across altitudes on sedimentary rock (P < 0.00001, one-way ANOVA), while invariable on ultrabasic rock (P > 0.05). Redox values on sedimentary rather than on ultrabasic rock were signi®cantly lower at all altitudes (P < 0.05, one-way ANOVA) except at 800 m. The 2700-m sedimentary site demonstrated the lowest mean redox value with a wide standard deviation (189 262 mV), suggesting that the site was heterogeneous, but relatively anoxic. All other sites had relatively aerated soil conditions. The mass of topsoils (15 cm) ranged widely from 13.7 to 124.2 kg m±2, re¯ecting different amounts of organic matter incorporated (Table 3). Topsoils (15 cm) were acidic at all altitudes on sedimentary rock, and weakly acidic on ultrabasic rock (Table 3). Organic matter accumulated at middle altitudes (2100 and 2700 m) on sedimentary rock as indicated by the high concentrations of organic C and total N (Table 3). The high C/N ratio in excess of 25 was found at 2100 m on sedimentary rock. By contrast, the concentrations of organic C and total N were consistently low on ultrabasic rock.
Soluble P was always low in ultrabasic soils whereas on sedimentary soils it increased from low to middle altitudes and decreased at the highest elevation. The concentration of exchangeable Mg was consistently greater in ultrabasic than in sedimentary soils at comparable altitudes (except for 1400 m, Table 3). Similarly, that of Ca was always greater in ultrabasic soils (except for 3100 m). The altitudinal pattern in the initial pool of inorganic N was marked by a strong contrast between NH4 and NO3; NH4 concentration was greatest at a middle elevation on both substrates, while NO3 showed either the reversed pattern of NH4 (on sedimentary rocks) or a reduction with altitude (on ultrabasic rocks) (Table 3). Net soil N transformation rates Both in situ net soil nitri®cation and mineralization rates (on a weight basis) varied signi®cantly (P < 0.05, one-way ANOVA) across altitudes on both substrates (Fig. 2). Both rates were signi®cantly (P < 0.05, one-way ANOVA) greater in sedimentary than in ultrabasic soils except for middle elevations (Fig. 2); the rate was not signi®cantly different between the substrates at 2100 m for nitri®cation, and at 2100 and 2700 m for mineralization. Net mineralization rates of the soils which were collected from different altitudes and incubated at the constant temperature of 20.5°C (the common site treatment) were contrasting
306
K. Kitayama et al.
Table 3 Soil mass to 15-cm depth, soil pH (H2O) and concentrations of organic C, total N, easily soluble P, inorganic N (NH4-N and NO3-N) and exchangeable cations (Ex.) on an oven-dried weight basis 800
1400
Altitude (m) 2100
2700
3100
)2
Soil mass £ 15 cm (kg m ) Sedimentary rock 116.5 (2.4) Ultrabasic rock 124.2 (11.4) pH (H2O) Sedimentary rock 4.1 (0.1) Ultrabasic rock 4.5 (0.2) Organic C (%) Sedimentary rock 2.9 (0.1) Ultrabasic rock 2.4 (0.2) Total N (%) Sedimentary rock 0.21 (0.01) Ultrabasic rock 0.21 (0.02) C/N ratio Sedimentary rock 13.8 Ultrabasic rock 11.4 NH4-N (lg g)1) Sedimentary rock 3.9 (0.6) Ultrabasic rock 8.9 (2.1) NO3-N (lg g)1) Sedimentary rock 10.2 (1.8) Ultrabasic rock 7.2 (5.6) Inorganic N (NH4 + NO3 ± N) (lg g)1) Sedimentary rock 14.1 (2.0) Ultrabasic rock 16.1 (3.6) Soluble P (lg g)1) Sedimentary rock 1.56 (0.56) Ultrabasic rock 1.18 (0.45) Ex. Ca (lg g)1) Sedimentary rock 17 (10) Ultrabasic rock 29 (12) Ex. Mg (lg g)1) Sedimentary rock 31 (21) Ultrabasic rock 84 (16) Soil water contents (w/w percentage) Sedimentary rock 27.4 (1.2) Ultrabasic rock 22.4 (0.5)
27.7 (13.2) 86.6 (11.2)
13.7 (4.0) 47.2 (5.4)
18.2 (5.4) 53.7 (12.2)
3.6 (0.1) 4.9 (0.1)
3.1 (0.2) 5.4 (0.1)
3.4 (0.2) 5.1 (0.1)
4.9 (0.1) 5.34 (0.1)
10.6 (3.8) 4.6 (0.04)
20.0 (4.3) 3.4 (0.3)
17.7 (4.0) 3.5 (0.6)
8.6 (2.1) 3.5 (0.2)
0.63 (0.18) 0.33 (0.02)
0.77 (0.16) 0.28 (0.02)
0.92 (0.18) 0.35 (0.02)
16.7 13.9
26.0 12.1
19.2 9.9
28.7 (4.9) 16.3 (3.8)
27.9 (12.4) 26.6 (3.8)
29.9 (14.3) 7.3 (1.5)
2.0 (2.0) 0.2 (0.1)
ND 0.8 (0.7)
30.6 (5.2) 16.5 (3.8)
27.9 (12.4) 27.3 (4.4)
4.70 (1.62) 0.41 (0.08)
8.85 (1.63) 0.84 (0.06)
57.2 (6.3) 82.5 (9.3)
0.60 (0.02) 0.26 (0.02) 14.3 13.3 4.8 (1.5) 5.2 (0.7)
2.9 (1.5) 0.8 (1.1)
8.4 (.9.0) ND
32.9 (14.8) 8.1 (2.5)
13.2 (2.1) 5.2 (0.7)
20.93 (4.46) 1.89 (1.15)
6.23 (0.68) 0.80 (0.42)
87 (23) 128 (65)
79 (47) 630 (132)
61 (18) 299 (147)
734 (336) 375 (147)
138 (49) 60 (26)
131 (54) 284 (108)
336 (119) 401 (120)
80 (22) 276 (34)
56.2 (5.9) 38.5 (0.5)
70.1 (5.7) 42.9 (1.1)
66.3 (6.5) 48.7 (3.3)
47.7 (1.8) 30.2 (1.2)
Values are means ( SD). ND, not detected.
between sedimentary and ultrabasic rocks (Fig. 3). Although the mean mineralization rates of the soils from sedimentary rock were variable, they were not signi®cantly different among altitudes due to wide standard deviations (P 0.05, Tukey's HSD test). By contrast, the mineralization rates of ultrabasic soils from different altitudes were signi®cantly different and the rates
decreased with increasing altitude, more or less following the pattern of in situ mineralization rates (cf. Fig. 2). Effects of the common site treatment were less distinct in the case of nitri®cation for both substrates, because common site nitri®cation rates varied signi®cantly (P < 0.05) across altitudes (Fig. 3) with similar patterns as in situ rates (cf. Fig. 2).
Soil N mineralization on Kinabalu
307
Fig. 1. Soil redox potentials corrected for standard hydrogen electrode values at pH 7.0 (Eh7), at 15 cm depth on Mt Kinabalu. Values are means ( SD) of 10 replicates. Sites sharing the same letters on sedimentary rock do not differ signi®cantly at P 0.05 (Tukey HSD); ultrabasic sites were statistically invariable across altitudes (P > 0.05, one-way ANOVA). Signi®cant effects of substrate at comparable altitudes are indicated with *P < 0.05, **P < 0.01 (one-way ANOVA). s, sedimentary rock; d, ultrabasic rock. The two sites at 1400 m were excluded, and the 2100-m sedimentary site was replaced with one at 1700 m for logistic reasons.
The net nitri®cation and N mineralization rates in the common soils which were translocated to different altitudes signi®cantly decreased with increasing altitude on sedimentary rock (P < 0.00001 for both rates, one-way ANOVA), but were invariable on ultrabasic rock (P > 0.05 for both rates) (Fig. 4). Both rates were signi®cantly greater in sedimentary than in ultrabasic soils at all altitudes (P < 0.05, except for mineralization at 3100 m). The bulk of net inorganic N produced was contributed by NO3 in both rock types at nearly all altitudes. The reduction rate across altitudes in net mineralization was approximately four times greater in sedimentary than in ultrabasic soils (x coef®cient 0.93 in sedimentary [r2 0.91] vs 0.23 in ultrabasic [r2 0.39]). Phosphorus addition reduced both net nitri®cation and mineralization rates in almost all cases (by 3±6 lg g)1 10 days)1 in the case of mineralization) (Table 4). The difference between P-
Fig. 2. In situ net soil N mineralization and nitri®cation rates (lg g)1 10 days)1) on Mount Kinabalu. Values are means ( SD). Sites sharing the same letter(s) across each substrate type do not differ signi®cantly at P 0.05 (Tukey HSD). # denotes non-signi®cant effects (P > 0.05, ANOVA) of substrate at comparable altitudes. s, sedimentary rock; d, ultrabasic rock.
zapplied versus control (i.e common site) soils in net mineralization rate was statistically signi®cant (P < 0.05, paired t-test) at all altitudes in ultrabasic soils except at 1400 m; the statistical signi®cance P at 1400 m was 0.08 and, thus, the reduction was also marginally signi®cant. By contrast, a signi®cant reduction occurred only at 800 m on sedimentary rock.
308
K. Kitayama et al.
Fig. 3. Common site net soil N mineralization and nitri®cation rates (lg g)1 10 days)1) plotted against the altitudes of origin. Soils were collected from each site and incubated under the same conditions at 20.5 ( 0.4°)C in the dark. Values are means ( SD). Sites sharing the same letter(s) across each substrate do not differ signi®cantly at P 0.05 (Tukey HSD). # denotes no signi®cant effects (P > 0.05, ANOVA) of substrate at comparable altitudes. s, sedimentary rock; d, ultrabasic rock.
DISCUSSION Factors affecting N transformation In situ net soil N transformation rate decreased with increasing altitude for both substrates, in-
Fig. 4. Common soil net N mineralization and nitri®cation rates (lg g)1 10 days)1). Soils from the sedimentary and ultrabasic sites at 800 m were translocated at different elevations on sedimentary and ultrabasic substrates, respectively. Values are means ( SD) of four replicates. Sites sharing the same letter(s) across each substrate do not differ signi®cantly at P 0.05 (Tukey HSD). # denotes no signi®cant effects (P > 0.05, ANOVA) of substrates at comparable altitudes. s, sedimentary rock; d, ultrabasic rock.
dicating that temperature primarily controlled the transformation rate irrespective of substrate. However, mechanisms regulating the N transformation appear to be different between the two substrates.
Soil N mineralization on Kinabalu
309
Table 4 Effects of P fertilization on net soil N transformation rate, which are determined by the amount of N produced under the P treatment minus that of the controls (the common site treatment)
)1
Altitude (m) 2100
00
1400
)1.8 (0.8)* )0.7 (1.6)
)2.8 (1.7) )0.1 (0.08)
)2.5 (0.8)* )2.9 (1.5)*
)3.1 (3.9) )3.4 (2.2)
2700
3100
)0.4 (0.2)* 1.2 (2.5)
)0.5 (0.8) )0.6 (0.1)
)1.7 (1.1) )0.1 (0.1)
)6.4 (3.7) )4.7 (1.0)
)3.7 (7.6) )2.8 (0.7)
)2.3 (1.4) 1.2 (0.6)*
)1
Net nitri®cation (lg g 10 days ) Sedimentary rock Ultrabasic rock Net mineralization (lg g)1 10 days)1) Sedimentary rock Ultrabasic rock
Values are means ( SD). Signi®cant effects are denoted by *P < 0.05 and P < 0.01 (paired t-test). P was applied to each sample at a rate of 50 lg NaH2PO4-P per g oven-dried soil.
The common site incubation in comparison to the in situ incubation indicated that the in¯uence of temperature on net N mineralization in sedimentary soils was more pronounced than the in¯uence of substrate soil quality. By contrast, the in¯uence of inherent substrate soil quality was more pronounced than that of temperature in ultrabasic soils; this pattern was apparent because signi®cant variations were still found in the net mineralization rates of ultrabasic soils that were incubated under the same temperature condition. Nevertheless, results of the common-site incubation show a distinct altitudinal decline in net mineralization in ultrabasic soils, suggesting that substrate soil quality is determined as a function of altitude (i.e. the original in situ temperatures). Greater temperature sensitivity of sedimentary than of ultrabasic soils in net mineralization is also obvious from the common soil incubation (Fig. 4). Given that the temperature coef®cients as expected from Fig. 4 should hold for all sites, the magnitude of the in¯uence of elevated temperature on soil N transformation will be greater at lower elevations on both substrates (particularly on sedimentary rock). This is because the in situ soil N transformation rate is higher at lower elevations. To demonstrate the effects of soil moisture and temperature on net N mineralization in relation to organic matter quality, the fractions (ratios) of mineralized N (based on in situ net values, mg) to the initial total N (g) were plotted against their C/ N ratios in Fig. 5. Higher C/N ratios are related to greater soil moisture contents on sedimentary rock because the sites of differing soil-water
Fig. 5. Relationships between soil C/N ratios and the fractions of soil total N which were mineralized. The fractions are calculated as the ratios of in situ N mineralized (mg) per 10 days to the initial total N (g). s, sedimentary rock; d ultrabasic rock. Numbers without parentheses in the diagram indicate altitudes, and those inside parentheses indicate percentage soil moisture.
contents (i.e. 2100, 2700 and 3100 m sites) are horizontally placed over a range of C/N ratios. Among these three sites, the fraction of mineralized N does not signi®cantly change with altitude, suggesting that the effect of temperature is masked by moisture. The high soil moisture content appears to suppress the decomposition of soil organic matter at 2100 and 2700 m on sedimentary rock. These altitudes correspond to a cloud belt with saturated air (Kitayama 1992, 1994). We speculate that the reduced net miner-
310
K. Kitayama et al.
alization rates in these montane sites may be due to the effects of anaerobiosis on microbial oxidation or due to denitri®cation (Robertson & Vitousek 1981). We do not know the mechanism as to why the sedimentary sites are affected by high moisture more strongly than the ultrabasic sites. Probably, ultrabasic soils are rich in such secondary clay minerals as aluminum and iron oxides (Brooks 1987), which are much permeable to water, rendering aerated conditions. When the soil organic matter quality in terms of C/N ratio is constant, temperature appears to determine the fraction of N to be mineralized. The 800, 1400 and 3100 m sites on sedimentary rock are vertically dispersed at about 15 C/N ratio (Fig. 5). Approximately 1% of total N was net-mineralized per 10 days in the 800 m site (high temperature), whereas only 0.1% was mineralized in the 3100 m site (low temperature). Ultrabasic sites are clustered at lower C/Nvalues. Nevertheless, the fractions of total N giving rise to net mineralization are lower than in comparable sedimentary sites. This pattern (low net mineralization rates in spite of low C/Nvalues) does not conform to the logic of C/N interactions, because net release of mineralized N will be greater at lower C/N-values due to less severe competition of soil microbes for inorganic N. We speculate that there are mechanisms other than soil microbes in converting organic to inorganic N in these ultrabasic sites. Results suggest that moisture may regulate soil N transformation intricately with temperature, which agrees with the ®ndings of Marrs et al. (1988) and Kitayama (1996). Marrs et al. (1988) found that elevated temperature alone showed no increase in the net N mineralization rate on a relatively young volcanic mountain in Costa Rica (Volcan Barva). However, a signi®cant increase was shown when the increase in temperature was accompanied with reduction in moisture content. The de®ciency of P might limit soil N transformation on ultrabasic rock because P fertilization resulted in statistically signi®cant net immobilization at nearly all elevations on ultrabasic rock. We suggest that soil microbes respond to added P, and immobilize N in the P de®cient soils. Alternatively, Na which is added as NaH2PO4 solution in fertilization may suppress N transformation. Results of P fertilization
(Table 4) are, however, not convincing due to larger standard deviations in sedimentary soils. The magnitude of P limitation on soil N transformation across altitudes and substrates needs to be substantiated in the future. Marrs et al. (1988) suggested that P addition had no effects on net soil N transformation. However, their data demonstrate that net N immobilization occurs in response to P addition in lowland sites where the amount of soluble P is low (< 2 lg g)1), but does not occur in montane sites where soluble P is relatively high (approximately 55 lg g)1). Thus, whether the limitation of aboveground vegetation processes by P can occur through retarded soil N transformation and whether the limitation is widely occurring deserves to be tested (cf. Walker & Syers 1976; Crews et al. 1995). Implication for aboveground processes The availability of N to vegetation apparently becomes lesser with increasing elevation on both rock types. Our analysis may support the hypothesis that montane in comparison to lowland forests are limited by reduced availability of soil N (Grubb 1977; Tanner 1977, 1985; Vitousek 1984; Mars et al. 1988; Tanner et al. 1990; Weaver & Murphy 1990); however, this hypothesis can be veri®ed by a long-term fertilization experiment only. Moreover, our results cannot be directly transcribed to aboveground processes because we do not know if the processes are limited by N or something else. Here, our primary purpose was to describe the interactions of physical environments by analyzing the pattern and control of soil N transformation. The supply of N seems to be more strongly constrained by temperature and moisture on sedimentary rock, whereas by temperature and possibly P de®ciency on ultrabasic rock. Other toxic elements (e.g. Ni; Brooks 1987; Proctor et al. 1988, 1989) may add to ultrabasic sites, but we have no evidence. There are other factors (in addition to N) which can synergistically affect aboveground vegetation processes along the altitudinal transects (e.g. direct temperature and moisture effects on physiology, toxicity of excessive soil minerals, and species interactions). Indeed, the magnitude
Soil N mineralization on Kinabalu of the reduction in canopy height and total basal area is greater on ultrabasic than on sedimentary rock, despite that the latter shows a greater magnitude of altitudinal decline in in-situ N production. We observed that the appearance of the two forests are very similar at 800 m despite the substrate difference, but become increasingly dissimilar with altitude, as Corner (1978) and Proctor et al. (1988) noted. This suggests that factors other than soil N availability are involved in controlling the vegetation. In summary, our results show that temperature is primarily responsible for N mineralization rate on both substrates. The effects of linearly decreasing temperature across altitudes may be differently modi®ed on sedimentary versus ultrabasic rocks. Temperature and substrate act together and their combinations seem to contribute to high habitat diversity, and hence to diverse rainforest types on Mt Kinabalu. ACKNOWLEDGEMENTS We are indebted to Datuk Lamri Ali, Francis Liew, Jamili Nais and Rimi Repin of Sabah Parks for their generous support in many respects, and to one anonymous reviewer for helpful comments on the earlier manuscripts. This study was supported by a grant (Global Environmental Research B52±4) from the Japanese Environmental Agency to KK, and supplemented by a Research Fellowship of the Japan Society for the Promotion of Science for Young Scientists to SA. This paper is a contribution to the TEMA Project of the Japanese IGBP-GCTE committee. REFERENCES AIBA S. & KITAYAMA K. (in press) Structure, composition and species diversity in an altitudesubstrate matrix of rain forest tree communities on Mount Kinabalu, Borneo. Plant Ecology. BROOKS R. R. (1987) Serpentine and Its Vegetation, a Multidisciplinary Approach. Dioscorides Press, Portland, OR. BRUIJNZEEL L. A., WATERLOO M. J., PROCTOR J., KUITERS A. T. & KOTTERINK B. (1993) Hydrological observations in montane rain forests on Gunung Silam, Sabah, Malaysia, with special reference to the
311
`Massenerhebung' effect. Journal of Ecology 81: 145± 167. BRUNOTTE D. & KITAYAMA K. (1987) The relationship between vegetation and ultrabasic bedrock on the upper slopes of Mount Kinabalu, Sabah. Warta Geologi 13: 9±12. CORNER E. J. H. (1978) Plant life. In: Kinabalu, Summit of Borneo. Sabah Society Monograph. pp. 113±178. The Sabah Society, Kota Kinabalu, Malaysia. CREWS T. E., KITAYAMA K., FOWNES J. H. et al. (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76: 1407±1424. FAULKNER S. P., PATRICK W. H. JR & GAMBRELL R. P. (1989) Field techniques for measuring wetland soil parameters. Soil Science Society of America Journal 51: 362±365. GRUBB P. J. (1977) Control of forest growth and distribution on wet tropical mountains: with special reference to mineral nutrition. Annual Review of Ecology and Systematics 8: 83±107. HEANEY A. & PROCTOR J. (1990) Preliminary studies on forest structure and ¯oristics on Volcan Barva, Costa Rica. Journal of Tropical Ecology 6: 307±320. JACOBSON G. (1970) Gunung Kinabalu Area, Sabah, Malaysia. Geological Survey Malaysia, Report 8 (with a colored geological map on a scale of 1:50 000), Geological Survey Malaysia, Kuching, Malaysia. KITAYAMA K. (1991) Vegetation of Mount Kinabalu Park, Sabah, Malaysia, Map of Physiognomically Classi®ed Vegetation. Project Paper. Protected Area and Biodiversity, the Environment and Policy Institute, East±West Center, Honolulu. KITAYAMA K. (1992) An altitudinal transect study of the vegetation on Mount Kinabalu. Vegetatio 102: 149±171. KITAYAMA K. (1994) Biophysical conditions of the montane cloud forests of Mount Kinabalu, Sabah, Malaysia. In: Tropical Montane Cloud Forests (eds L. S. Hamilton, J. O. Juvik & F. N. Scatena) pp. 183±197. Springer-Verlag, New York. KITAYAMA K. (1996) Soil nitrogen dynamics along a gradient of long-term soil development in a Hawaiian wet montane rainforest. Plant and Soil 183: 253±262. LEIGH E. G. (1975) Structure and climate in tropical rainforest. Annual Review of Ecology and Systematics 6: 67±86. MARRS R. H., PROCTOR J., HEANEY A. & MOUNTFORD M. D. (1988) Changes in soil nitrogenmineralization and nitri®cation along an altitudinal transect in tropical rain forest in Costa Rica. Journal of Ecology 76: 466±482.
312
K. Kitayama et al.
MUELLER-DOMBOIS D. & ELLENBERG H. (1974) Aims and Methods of Vegetation Ecology. John Wiley and Sons, New York. OHSAWA M., NAINGGOLAN P. H. J., TANAKA N. & ANWAR C. (1985) Altitudinal zonation of forest vegetation on Mount Kerinci, Sumatra: with comparisons to zonation in the temperate region of east Asia. Journal of Tropical Ecology 1: 193±216. PROCTOR J., LEE Y. F., LANGLEY A. M., MUNRO W. R. C. & NELSON T. (1988) Ecological studies on Gunung Silam, a small ultrabasic mountain in Sabah, Malaysia. 1. Environment, forest structure and ¯oristics. Journal of Ecology 76: 320±340. PROCTOR J., PHILLIPPS C., DUFF G. K., HEANEY A. & ROBERTSON F. M. (1989) Ecological studies on Gunung Silam, a small ultrabasic mountain in Sabah, Malaysia. II. Some forest processes. Journal of Ecology 77: 317±331. ROBERTSON G. P. & VITOUSEK P. M. (1981) Nitri®cation potentials in primary and secondary succession. Ecology 62: 376±386. TANNER E. V. J. (1977) Four montane rain forests of Jamaica: A quantitative characterization of the ¯oristics, the soils and the foliar mineral levels, and a discussion of the interrelationships. Journal of Ecology 65: 883±918.
TANNER E. V. J. (1985) Jamaican montane forests: nutrient capital and cost of growth. Journal of Ecology 73: 553±568. TANNER E. V. J., KAPOS V., FRESKOS S., HEALEY J. R. & THEOBALD A. M. (1990) Nitrogen and phosphorus fertilization of Jamaican montane forest trees. Journal of Tropical Ecology 6: 231±238. VITOUSEK P. M. (1984) Litterfall, nutrient cycling, and nutrient limitations in tropical forests. Ecology 65: 285±298. VITOUSEK P. M., APLET G., TURNER D. & LOCKWOOD J. J. (1992) The Mauna Loa environment matrix: foliar and soil nutrients. Oecologia 89: 372±382. VITOUSEK P. M. & SANFORD JR R. L. (1986) Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics 17: 137±167. VITOUSEK P. M., VAN CLEVE K., BALAKRISHNAN N. & MUELLER-DOMBOIS D. (1983) Soil development and nitrogen turnover in montane rainforest soils on Hawaii. Biotropica 15: 268±274. WALKER T. W. & SYERS J. K. (1976) The fate of phosphorus during pedogenesis. Geoderma 15: 1±19. WEAVER P. L. & MURPHY P. G. (1990) Forest structure and productivity in Puerto Rico's Luquillo Mountains. Biotropica 22: 69±82. WHITMORE T. C. (1975) Tropical Rain Forests of the Far East. Oxford University Press, London.
