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Microbial properties and soil respiration in submontane forests of Venezuelian Guyana: characteristics and response to fertilizer treatments
Soil Biology & Biochemistry 33 (2001) 503±509
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Microbial properties and soil respiration in submontane forests of Venezuelian Guyana: characteristics and response to fertilizer treatments J.A. Priess*, H. FoÈlster Institute of Soil Science and Forest Nutrition, University of GoÈttingen, BuÈsgenweg 2, D-37077 GoÈttingen, Germany Received 7 June 1999; received in revised form 14 February 2000; accepted 27 July 2000
Abstract The distribution of vegetation types in Venezuelan Guyana (in the `Canaima' National Park) represents a transitional stage in a long term process of savannization, a process considered to be conditioned by a combined chemical and intermittent drought stress. All types of woody vegetation in this environment accumulate large amounts of litter and soil organic carbon (SOC). We hypothesized that this accumulation is caused by low microbial activity. During 1 year we measured microbial biomass carbon (Cmic), microbial respiration and soil respiration of stony Oxisols (Acrohumox) at a tall, a medium and a low forest and with three chemical modi®cations of site conditions by the addition of 21 21 NO2 and PO32 in the mineral topsoil and 3 ; Ca 4 as possible limiting elements. Due to high SOC contents, mean Cmic was 1 mg g soil 21 3 mg g soil in the forest ¯oor. Mean microbial respiration in the mineral topsoil and the forest ¯oor were 165 and 192 mg CO2C g soil 21 d 21, respectively. We calculated high mean metabolic quotients (qCO2) of 200 mg CO2-C g Cmic 21 d 21 in the litter layer and 166 mg CO2-C g Cmic 21 d 21 in the mineral topsoil, while the Cmic-to-SOC ratios were as low as 1.0% in the litter layer and 0.8% in the mineral topsoil. Annual soil respiration was 9, 12 and 10 Mg CO2-C ha 21 yr 21 in the tall, medium and low forest, respectively. CO2 production was signi®cantly increased by CaHPO4 fertilization, but no consistent effects were caused by Ca 21 and NO2 3 ; fertilization. Our ®ndings indicate that Cmic and microbial respiration are reduced by low nutrient concentrations and low litter and SOC quality. Reduced microbial decomposition may have contributed to SOC accumulation in these forests. q 2001 Elsevier Science Ltd. All rights reserved. Keywords: Microbial biomass; Microbial respiration; Substrate induced respiration; Respiratory quotient (qCO2); Soil nutrients; Tropical rain forest; Oxisol
1. Introduction The `Gran Sabana' represents a substantial part of the Venezuelan Guyana highlands (800±1500 m a.s.l.). Its vegetation cover is characterized by a mosaic of tall to low forests, secondary bush and savanna. According to FoÈlster (1986, 1992), Hernandez (1992) and Dezzeo (1994), this mosaic represents a transitional stage of a long-term autochthonous process of savannization. Destabilization of forests may be triggered by ®res, but is essentially conditioned by a combined effect of chemical stress caused by Ca-de®ciency and Al-toxicity and hydrological stress due to shallow rooting in stony soils and drought periods. Previous studies in the region have provided insights into vegetation types, carbon and nutrient * Corresponding author. Present address: Laboratory of Soil Science and Geology, Wageningen Agricultural University, P.O. Box 37, 6700 AA Wageningen, The Netherlands. Fax: 131-317-482419. E-mail address: [email protected] (J.A. Priess).
stocks (Dezzeo, 1994; FoÈlster, 1986, 1992; Hernandez, 1987, 1992). Aboveground litter production falls within the range reported for tropical forests, but high ®ne-root production was measured in these forests by Priess et al. (1999). The latter authors found consistently high fractions of root necromass and concluded that the accumulation of dead roots was caused by slow mineralization. All forest types in the region (Dezzeo, 1994, Hernandez, 1999), have accumulated large amounts of organic carbon in the litter layer and the mineral soil. We hypothesized that soil acidity and nutrient de®ciency limit the activity or ef®ciency of soil microorganisms. We tested our hypotheses by modifying soil chemical conditions by addition of Ca 21, 32 NO2 3 and PO4 ; which were considered the most likely de®cient elements (FoÈlster, 1986, 1992), using quantitative measurements of Cmic, microbial respiration and soil respiration. The studies were carried out at three forest sites, differing in tree biomass and productivity (Dezzeo, 1990; Priess et al., 1999).
0038-0717/01/$ - see front matter q 2001 Elsevier Science Ltd. All rights reserved. PII: S 0038-071 7(00)00191-7
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Table 1 Selected soil chemical properties of the forest ¯oor and the mineral topsoil 0±10 cm; values represent means ^ standard deviation n 5 Forest type Forest ¯oor Tall Medium Low
pHKCl
N
C-to-N
21
3.3 ^ 0.1 3.3 ^ 0.1 3.1 ^ 0.1
mg g 251 ^ 28 268 ^ 31 329 ^ 8.0
4.3 ^ 0.1 4.2 ^ 0.1 4.4 ^ 0.1
118 ^ 12 115 ^ 31 119 ^ 12
Ptotal
K 21
10.1 ^ 5.8 12.7 ^ 1.8 15.4 ^ 0.9
19.1 ^ 2.0 21.3 ^ 1.7 21.4 ^ 0.9
mg g 21
Mineral soil Tall Medium Low
C
7.6 ^ 0.7 6.7 ^ 1.6 6.3 ^ 0.6
15.4 ^ 0.6 16.9 ^ 0.8 19.0 ^ 0.4
2. Materials and methods 2.1. Site description The geology of the Guyana highland is dominated by the Precambrian Roraima formations, which consist of an alteration of clay- and sandstones giving rise to a cuesta landscape (Schubert, 1986). The study site `La Sabanita' (approximately 580 0 N; 6180 0 W; 1150±1200 m asl.) in the southern part of the Gran Sabana, about 5 km east of the village San Francisco de YuruanõÂ, is a ridge topped by a savanna patch with fringes of bushland. On the upper slope, the vegetation changes gradually from a single storey forest (`low forest') of about 10 m height via a medium high forest (`medium forest') to a higher multi-storey forest of up to 35 m height (`tall forest'). Aboveground biomass was estimated at 143, 360 and 342 Mg ha 21, and ®ne-root biomass at 9.6, 12.2 and 11.4 Mg ha 21 in the low, medium and tall forest, respectively (Dezzeo, 1990). The sites are within the `submontane moist forest zone' (Holdridge, 1947). Annual precipitation during the study was 2200 mm in 1990/91 (Priess and FoÈlster, 1994). The dry season usually lasts from January to March, but rainfall may decrease during December and increase in late April. Mean annual air temperature was 20.68C with small seasonal variations. During the experiments, monthly precipitation was within one standard deviation of the long-term average of the weather-station in San Ignacio located 12 km away (Priess et al., 1999). Soils were classi®ed as Acrohumox (Soil taxonomy, USDA, 1975). They are consistently covered by an organic horizon of 6±12 cm corresponding to 50±100 Mg ha 21 with a dense root mat, which contains up to 50% of the ®ne roots of the entire pro®le (Dezzeo, 1990). Root penetration of the mineral soil remains shallow. Despite the high organic matter content of 12% at 0±10 cm depth, the CEC of the topsoils averaged only 100 mmol g soil 21 due to the low pH. The clay content of the ®ne soils is approximately 40%, but the CEC of the kaolinitic clay is extremely low (20 mmol g clay 21). The exchangeable cations are dominated by Al n1 with 80±90% of CEC. Concentrations of 1 21 NH1 are always higher than those of Ca 21 4 ; K and Mg (Table 1). From the tall via the medium to the low forest,
Ca
Mg
Al
0.20 ^ 0.08 0.15 ^ 0.03 0.18 ^ 0.02
1.53 ^ 0.10 1.05 ^ 0.13 0.36 ^ 0.02
120 ^ 8.0 129 ^ 15.8 89 ^ 5.1
2.51 ^ 0.66 2.10 ^ 0.53 1.97 ^ 0.23
94.0 ^ 15.9 87.9 ^ 25.4 74.6 ^ 7.7
21
mg g 366 ^ 27 362 ^ 15 552 ^ 29
mg g 4.7 ^ 0.5 3.0 ^ 0.4 0.7 ^ 0.1
mg g 21
mmol g 21 exchangeable cations
25.3 ^ 2.4 23.0 ^ 1.6 47.2 ^ 3.1
2.55 ^ 0.52 2.32 ^ 0.66 2.09 ^ 0.41
1.60 ^ 0.37 1.40 ^ 0.54 1.29 ^ 0.44
soil nutrient concentrations, except for PO32 4 ; decrease both in the organic layer and in the mineral soil (Table 1). The water storage of the soils is reduced by their high stone content (stones in the low forest: 60±65%; tall and medium forest: 30±35%). We found considerable admixtures of mineral soil in the forest ¯oor (relatively low C and high Al contents). 2.2. Experimental design We set up a factorial design of four treatments (control, CaCl2, NaNO3, CaHPO4) on three forest sites with ®ve replicates per treatment. At each site tall forest (2500 m 2), medium forest (900 m 2) and low forest (2500 m 2) we marked 20 randomly chosen treatment-plots of 1 m 2 at a minimum distance of 1 m from footpaths and trees. The frames for soil respiration measurements were placed permanently in the center of each treatment-plot. Fertilizer application of the treatment-plots was 450 kg Ca ha 21, 300 kg N ha 21, and 350 kg P ha 21 in the tall and medium forest. In the low forest, we applied only 50% of fertilizer, because the amount of ®ne soil was approximately 50% of the ®ne soils at the tall and medium forest. Fertilizers were applied in liquid form, except for phosphate, which was applied as granulate two weeks before the experiments began. 2.3. Microbial C and microbial respiration Cmic was measured in the forest ¯oor and the mineral soil 0±10 cm depth separately, using the SIR method (Anderson and Domsch, 1978). Alternately every 3±4 weeks we collected 15 samples per treatment of the 1 m 2 fertilizer plots either from the forest ¯oor (20 g each) or the mineral soil (100 g each) and pooled them as one composite sample. We added 1% solid glucose and incubated samples for 6 h in gas tight syringes (Heilmann and Beese, 1992). Microbial respiration was measured in two replicates of composite samples in gas tight syringes at 228C for 6 h. CO2 concentrations were measured every hour and microbial respiration was calculated as mean value of six consecutive measurements. Soil moisture was expected to be the main driver for seasonal variation of microbial respiration. For
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Table 2 Microbial C and microbial respiration; ®gures represent annual means ^ standard deviation n 5; different letters indicate signi®cant differences between treatments P 0:05 Treatment
Tall forest Forest ¯oor
Medium forest
Low forest
Mineral soil (0±10 cm)
Forest ¯oor
Mineral soil (0±10 cm)
Forest ¯oor
Mineral soil (0±10 cm)
0.94 ^ 0.10a 1.20 ^ 0.15b 1.30 ^ 0.28b
2.84 ^ 0.65 2.40 ^ 0.42 2.81 ^ 0.48
1.17 ^ 0.31 1.30 ^ 0.33 1.25 ^ 0.33
3.32 ^ 0.65 3.53 ^ 1.24 3.13 ^ 1.21
1.18 ^ 0.38a 1.53 ^ 0.27b 1.45 ^ 0.23b
200 ^ 30 200 ^ 20 190 ^ 40
160 ^ 50 200 ^ 60 160 ^ 50
180 ^ 10 160 ^ 30 190 ^ 20
180 ^ 20 170 ^ 20 140 ^ 30
21
Cmic (mg C g soil ) Control 2.78 ^ 0.64 CaCl2 2.61 ^ 0.05 NaNO3 2.94 ^ 0.34
Microbial respiration (mg CO2-C g soil 21 d 21) Control 240 ^ 140 150 ^ 40 CaCl2 200 ^ 10 170 ^ 40 NaNO3 210 ^ 20 150 ^ 50
that reason, we measured microbial respiration at actual soil moisture, rather than adjusting moisture to standard conditions. Measurements of Cmic and microbial respiration included three treatments (control, Ca and NO2 3 and were repeated three times in the rainy and twice in the dry season. 2.4. Soil respiration We used the static chamber method (Loft®eld et al., 1992) with ®ve replicates per treatment. Cylindric plastic frames (dia: 25 cm) were installed 3±5 cm in the soil or organic layer. The depth of insertion was restricted to the surface layer, to reduce cutting of lateral roots. The area inside the frames was kept free of vegetation. During the measurements, plastic chambers of 4.3 dm 3 were ®xed airtight on the frames, and gas samples were taken with gastight syringes 1.0, 3.5, 6.0 and 8.5 min after closing the chamber. Total sampling volume was less than 1% of the chamber's volume to avoid the effect of accelerated mass ¯ow (Freijer and Bouten, 1991). During 14 months, soil respiration was measured every 3±4 weeks from 09.00± 11.00 h. Samples were analyzed on the same day using a gas chromatograph equipped with a thermal conductivity detector. Measurements started two months after the insertion of the frames to reduce the effects of soil disturbance on C mineralization. For a correct assessment of annual CO2 production we also measured nighttime soil respiration. During a measuring campaign in August 1990, the three forest sites n 15 frames of the control plots) showed no signi®cant difference between daytime (09.00±11.00 h: 3:2 ^ 1:0 g CO2C m 22 d 21) and nighttime (21.00±23.00 h: 3:1 ^ 1:1 g CO2-C m 22 d 21) respiration. In consequence, only daytime measurements were continued. At the end of the experiments we wanted to ®nd out, whether the permanent installation of measurement frames affected ®ne-root density. For that reason we cut 1000 cm 3 soil-blocks within and outside (30 cm distance) of all frames of the control plots, separated and weighed the roots. Root densities (inside 6:0 ^ 2:2 g dm23 ; outside 6:5 ^ 2:3 g dm 2 3; n 15 did not differ signi®cantly.
2.5. Statistics We used the SAS 6.12 statistics package for Windows to analyze the principle effects with nested multi-factorial (repeated measure) ANOVA. Soil respiration data were tested with two factorial repeated measure ANOVA (sites, treatments) and three factorial ANOVA (sites, treatments, season). Microbial biomass C and basal respiration data were tested with three factorial repeated measure ANOVA (sites, treatments, soil depth). For comparisons of paired samples the T-test was used. Linear regressions were calculated with ms-excel 97.
3. Results 3.1. Microbial properties The highest concentrations of Cmic were measured in the low forest and the lowest concentrations in the tall forest (Table 2). The ANOVA revealed a highly signi®cant effect of sites P , 0:0001: At all sites Cmic was signi®cantly lower during the dry season and higher during the rainy season. The seasonal effect was more pronounced in the forest ¯oor, where seasonal variation in soil moisture was larger than in the mineral soil (soil moisture differences: forest ¯oor: 47 vol.%; mineral soil: 12 vol.%). According to ANOVA results, fertilizer treatments did not affect Cmic signi®cantly P , 0:27: However, the ANOVA results were in¯uenced by a signi®cant interaction between the factors treatment and soil depth. Pairwise comparisons of Cmic of different sites showed that Cmic of the control and the Ca treatment in the forest ¯oor of the low forest was signi®cantly larger than in the other two forests P , 0:05: Pairwise comparisons of treatments revealed signi®cantly larger Cmic in the fertilized mineral soils of the tall and the low forest P , 0:05: Cmic concentrations in the forest ¯oor of all sites were 2- to 3-fold higher than in the mineral topsoil (ANOVA: soil depth: P , 0:0001: The ratios of Cmic-to-SOC did not differ between sites or treatments, but were signi®cantly higher P , 0:05 in the forest ¯oor (1.0%) than in the mineral topsoil (0.8%).
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Table 3 Mean annual and mean seasonal soil respiration of control, Ca 21, NO2 3 and CaHPO4 treatment in tall, medium and low forest; ®gures represent annual or seasonal means ^ standard deviation n 5 Period
Forest type
Treatment Control
Ca
NO2 3
CaHPO4
8.96 ^ 2.46 12.41 ^ 3.19 10.24 ^ 3.43
9.80 ^ 2.38 11.30 ^ 2.81 10.63 ^ 4.08
10.96 ^ 2.92 9.90 ^ 3.17 9.72 ^ 3.46
13.17 ^ 3.75 16.34 ^ 5.59 11.65 ^ 3.17
Rainy season (g CO2-C m 22 d 21) a Tall Medium Low
2.69 ^ 0.57 3.75 ^ 0.73 3.13 ^ 0.92
2.85 ^ 0.59 3.33 ^ 0.63 3.21 ^ 1.06
3.23 ^ 0.72 2.88 ^ 0.87 2.98 ^ 0.92
3.87 ^ 0.91 4.70 ^ 1.54 3.67 ^ 0.64
Dry season (g CO2-C m 22 d 21) a Tall Medium Low
2.01 ^ 0.66 2.73 ^ 0.75 2.16 ^ 0.58
2.35 ^ 0.67 2.65 ^ 0.86 2.39 ^ 1.07
2.56 ^ 0.78 2.37 ^ 0.78 2.04 ^ 0.66
3.09 ^ 1.10 4.05 ^ 1.45 2.24 ^ 0.31
21
21
Year (Mg CO2-C ha yr ) Tall Medium Low
a
We measured 10 times during the rainy (275 d) and three times during the dry season (90 d).
Average microbial respiration was 192 ^ 27 mg CO2C g soil 21 d 21 in the forest ¯oor and 165 ^ 42 mg CO2C g soil 21 d 21 in the mineral soil (ANOVA: P , 0:01; but was not signi®cantly different between sites or treatments. Regression analysis showed contrasting relationships between soil moisture and microbial respiration P , 0:05 in the forest ¯oor resporg 0:0003 £ moisture% 1 0:164; r 0:35 and in the mineral soil r 20:49: respmin 20:0017 £ moisture% 1 0:273; That means during the dry season microbial respiration was reduced in the forest ¯oor, while in the mineral soil it was enhanced. The metabolic quotients (qCO2), i.e. microbial respiration per unit microbial biomass were signi®cantly different P , 0:01; n 33 between forest ¯oor 200 ^ 53 mg CO2-C g microbial C 21 d 21) and mineral soil 166 ^ 44 mg CO2-C g microbial C 21 d 21). No signi®cant differences were detected between sites or treatments. 3.2. Soil respiration Annual soil respiration rates in the tall, medium and low forest were 9.0, 12.4 and 10.2 Mg CO2-C ha 21 yr 21 (Table 3) and were all signi®cantly different from each other. Fertilizer treatments caused a signi®cant effect (ANOVA P , 0:005 and variability was comparable to the variability of the control plots. All plots treated with CaHPO4 had a significantly higher soil respiration, compared to the other treatments. No consistent trends were observed for the plots that were fertilized with Ca or NO2 3 : The CaHPO4 plots were the only ones where the pH value of the topsoil increased significantly during the experiments (10.5 units). Soil respiration followed a clear seasonal trend, with higher CO2 production in the rainy season and lower CO2 production during the dry season (Fig. 1). On average 20%
of the carbon ¯ux occurred during the dry season (90 d) and 80% during the rainy season (275 d).
4. Discussion 4.1. Microbial variables The values of microbial biomass measured in this study 0:9±1:5 mg Cmic g soil 21 in the mineral soil and 2.4± 3.5 mg Cmic g soil 21 in the forest ¯oor) are high compared to other tropical forests (0.27±0.79 mg Cmic g soil 21; Jordan, 1989; Srivastava and Singh, 1991; Yang and Insam, 1991; Mao et al., 1992) but fall within the range reported for some temperate forests (Wolters and Joergensen, 1991; Joergensen et al., 1995). They re¯ect the very high SOC contents of our forest soils, as Cmic is closely related to SOC (Brookes et al., 1990; Bauhus and Khanna, 1999). However, if this relationship is quanti®ed as Cmicto-SOC ratio, it is obvious that microbial biomass does not increase in line with soil organic matter. The low ratios of 1.0% in the forest ¯oor and 0.8% in the top mineral soil we measured, are below the range recorded in literature for tropical soils of 1±5% (Srivastava and Singh, 1991; Yang and Insam, 1991; Mao et al., 1992; Prasad et al., 1994). As Cmic-to-SOC ratios are explained by SOC quality, (Bauhus and Khanna, 1999), low ratios should indicate adverse substrate properties. The low Cmic-to-SOC ratios we found in our study might be conditioned on the one hand by a low N content of the scleromorphous leaf litter, and on the other hand by the effects of soil acidity and low nutrient availability (Wolters and Joergensen, 1991; Joergensen et al., 1995; Bauhus and Khanna, 1999). Both seasonal increases (Singh et al., 1991) and decreases (Marumoto et al., 1982; Sparling and Williams, 1986; Prasad et al., 1994) in Cmic have been reported from agricultural and
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Fig. 1. Soil respiration (g CO2-C m 22 d 21) in the tall forest, medium forest and low forest soil respiration was measured with static chambers over 1 yr. Datapoints represent means n 5; error bars represent standard deviation. X-axis presents day and month.
forest ecosystems depending on substrate availability or drying and rewetting effects. We measured a signi®cant decrease of Cmic during the dry season. Because of the larger seasonal moisture differences, the reduction in biomass C was more pronounced in the forest ¯oor than in the mineral soil. Our ®nding of an inverse relationship of soil moisture and microbial respiration in the mineral soil means that a lower amount of active microbes produced more CO2 in drier soils. As this effect is signi®cant but not very strong, it does not indicate prolonged periods of water saturation or lack of oxygen in the rapidly draining forest soils. The values of microbial respiration and qCO2 measured in our study are high, when compared to the data that have been published. Few studies of microbial respiration and qCO2 have been reported from tropical forests. Mao et al. (1992) reported microbial respiration of 4.91 mg CO2-C g soil21 d 21 and qCO2 of 18.4 mg CO2-C g microbial C 21 d 21 from an old secondary forest in South China. Prasad et al. (1994) calculated microbial respiration of 8.66 mg CO2-C g soil21 d 21 and qCO2 of 13.5 mg CO2-C g microbial C 21 d 21 from a natural forest in Orissa, India. Both forests had lower Corg (85±90% lower) and Cmic (35±75% lower) contents than the forest sites we studied, as well as much lower microbial respiration (94±97% lower). Thus, in our present study the qCO2 or carbon use ef®ciency of the soil microbes was considerably lower than reported for other tropical forests. In recent years, the qCO2 has been used as bioindicator for ecosystem succession (Insam and Haselwandter, 1989) and environmental stress (Wolters and Joergensen, 1991; Anderson and Domsch, 1993; Joergensen et al., 1995) in temperate ecosystems. Following the hypothesis that environmental stresses like low pH, high Al, low SOM quality or nutrient de®ciency reduce carbon use ef®ciency, the high qCO2 values we measured in our study would indicate a stressed soil microbial community. However, the use of qCO2
as bioindicator has been criticized, because it fails to distinguish between disturbance and stress effects (Wardle and Ghani, 1995). In our study we can exclude human disturbance in recent decades. We conclude that the high qCO2 values are probably related to chemical stress. This interpretation is supported by ®ndings of Priess et al. (1999) from the same forests, who reported low nutrient concentrations in ®ne roots and high fractions of ®ne root necromass. The author's assume that the accumulation of root necromass is caused by the slow mineralization of the nutrient poor substrate. We had hypothesized that besides P, Ca and NO2 3 also might be de®cient elements in the system. Their addition, however, did not produce a consistent effect. Tropical forests growing on nutrient poor soils are supposed to establish an almost closed nutrient cycle (Jordan, 1989), i.e. roots and soil microorganisms are very ef®cient in the uptake of sparse nutrients. However, FoÈlster (1986) repeatedly found relatively high concentrations of Ca 21 and NO2 3 in the soil solution below the rooting zone of forests in the Gran Sabana. Element uptake from soil solution is possibly not so ef®cient when compared to element drainage, so we consider the fertilizer aspect in regard to these two elements as inconclusive. 4.2. Soil respiration The static chamber method has been criticized for underestimating C-¯uxes, because lateral roots can be cut or their growth into the chambers could be inhibited by the inserted frames. However, we found no differences in root densities inside and outside the frames. In various studies, diurnal cycles of respiration have been reported (Venezuela: Medina and Zelwer, 1972; India: Singh and Gupta, 1977; USA: Grahammer et al., 1991). However, no such diurnal
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variation was detected in a tropical rainforest by Kursar (1989) or in our experiments. In the present study soil temperatures were typically 1±28C lower at night. Assuming a Q10 1.4±2 (Holland et al., 1995) or 2.5 (Kirschbaum, 1995), a temperature reduction of 28C would cause a reduction of soil respiration by 7±16% in our study. According to Raich and Nadelhoffer (1989) annual soil respiration in tropical forests ranges from 2.2 to 15.1 Mg CO2-C ha 21 yr 21. Our premontane forest sites (tall: 8.96, medium: 12.41 and low: 10.24 Mg CO2-C ha 21 yr 21) fall within this range, but are below the mean of 12:6 ^ 0:6 Mg CO2-C ha 21 yr 21 calculated for tropical moist forests by Raich and Schlesinger (1992). The ANOVA revealed highly signi®cant effects of site, season and fertilizer treatments. Rerunning the ANOVA without the CaHPO4-treatment showed that neither the Ca nor the NO2 3 treatments had an effect on soil respiration. Pairwise comparisons resulted in some signi®cant fertilizer effects, but without a consistent trend. While the seasonal variation in soil respiration was clearly related to soil moisture, the origin of the fertilizer effects was less clear. In all experiments but the CaHPO4-treatment, the pH of soil and soil solution remained almost unchanged. The CaHPO4treatment caused the pH to increase signi®cantly by 0.5 units, thus producing presumably a combined pH-fertilizer effect. The interpretation is further complicated by the fact, that the pH shift resulted in an increased cation exchange capacity (150%) and a lower Al-solubility, which could bias soil respiration. We cannot identify whether root or microbial respiration was responsible for the increased soil respiration. However, as ®ne root growth at the same sites doubled in the CaHPO4-fertilized plots (Priess, 1996), we assume that root respiration also increased strongly. Soil moisture content and temperature are key factors in the regulation of soil and litter respiration (Kursar, 1989; Raich and Nadelhoffer, 1989; Cavelier and PenÄuela, 1990; Maggs and Hewett, 1990; Jurik et al., 1991). Soil respiration during the rainy season was about 50% higher than during the dry season (Table 2). In two rainforests in north-east Queensland seasonal pattern as well as annual CO2 release (13.6 and 14.4 Mg CO2-C ha 21 yr 21) were comparable with our results (Maggs and Hewett, 1990). Davidson and Trumbore (1995) measured a 20% higher surface ¯ux of CO2 during the rainy season in a rainforest of East Amazonia compared to the dry season. A reduction of soil respiration during the rainy season and a sharp decline of 40% immediately after rain events were observed by Buchmann et al. (1997) in a rainforest in French Guiana. Buchmann et al. (1997) assume that oxygen de®ciency was responsible for this effect. We also observed a pronounced decline of CO2 production directly following rainfall (data not shown). However, the reduced CO2 emissions were followed by strongly enhanced emissions, suggesting that diffusion was limited only for some minutes in the rapidly draining soils. Due to the extremely variable effects on soil respiration, measurements affected by rainfalls were omitted and repeated.
Acknowledgements This study was partly supported by the German Research Foundation (DFG). We gratefully acknowledge the scienti®c and logistic support of CVG-EDELCA gerencia de estudios e ingenerõÂa. We thank E. Veldkamp, H. Flessa, W. Borken and two anonymous reviewers for critically revising earlier versions of the manuscript. References Anderson, J.P.E., Domsch, K.H., 1978. A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biology & Biochemistry 10, 215±221. Anderson, T.H., Domsch, K.H., 1993. The metabolic quotient for CO2 (qCO2) as a speci®c activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biology & Biochemistry 25, 393±395. Bauhus, J., Khanna, P.K., 1999. The signi®cance of microbial biomass in forest soils. In: Rastin, N., Bauhus, J. (Eds.). Going Underground Ð Ecological Studies in Forest Soils, Research Signpost, Trivandrum, pp. 77±110. Brookes, P.C., Ocio, J.A., Wu, J., 1990. The soil microbial biomass: its measurement, properties and role in soil nitrogen and carbon dynamics following substrate incorporation. Soil Biology & Biochemistry 35, 39±51. Buchmann, N., Guehl, J.M., Barigah, T.S., Ehleringer, J.R., 1997. Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110, 120±131. Cavelier, J., PenÄuela, M.C., 1990. Soil respiration in the cloud forest and dry deciduous forest of Cerrania de Macuira, Colombia. Biotropica 22, 346±352. Davidson, E.A., Trumbore, S.E., 1995. Gas diffusivity and production of CO2 in deep soils of the Eastern Amazon. Tellus 47B, 550±565. Dezzeo, N., 1990. Bodeneigenschaften und NaÈhrstoffvorratsentwicklung in autochton degradierenden WaÈldern SO-Venezuelas. GoÈttinger BeitraÈge zur Land- und Forstwirtschaft in den Tropen und Subtropen, vol. 53. Liddy Halm, GoÈttingen. Dezzeo, N. (Ed.), 1994. EcologõÂa de la altiplanicie de la Gran Sabana (Guayana Venezolana). I. Investigaciones sobre la dinaÂmica bosquesabana en el sector SE: Subcuencas de los RõÂos YuruanõÂ, ArabopoÂ, y Alto KukenaÂn. Sciencia Guaianae, vol. 4. FoÈlster, H., 1986. Forest-savanna dynamics and deserti®cation processes in the Gran Sabana. Interciencia 11, 311±316. FoÈlster, H., 1992. Holocene autochthonous forest degradation in southeast Venezeula. In: Goldammer, J.G. (Ed.). Tropical Forests in Transition, BirkhaÈuser, Basel, pp. 25±44. Freijer, J., Bouten, W., 1991. A comparison of ®eld methods for measuring soil carbon dioxide evolution: experiments and simulation. Plant and Soil 135, 133±142. Grahammer, K., Jawson, M.D., Skopp, J., 1991. Day and night soil respiration from a grassland. Soil Biology & Biochemistry 23, 77±81. Heilmann, B., Beese, F., 1992. Miniaturized method to measure carbon dioxide production and biomass of soil microorganisms. Soil Science Society of America Journal 56, 596±598. Hernandez, L., 1987. DegradacioÂn de los bosques de la Gran Sabana. Pantepui 3, 11±25. Hernandez, L., 1992. Gliederung Struktur und ¯oristische Zusammensetzung von WaÈldern und ihrer Degradations- und Regradationsphasen im Guayana-Hochland, Venezuela. GoÈttinger BeitraÈge zur Land und Forstwirtschaft in den Tropen und Subtropen, vol. 70. Goltze, GoÈttingen (198pp.). Hernandez, L. (Ed.), 1999. EcologõÂa de la Altiplanicie de la Gran Sabana
J.A. Priess, H. FoÈlster / Soil Biology & Biochemistry 33 (2001) 503±509 (Guayana Venezolana). II. Estructura, diversidad, crecimiento y adaptacioÂn en bosques de las subcuencas de los rõÂos YuruanõÂ y Alto KukenaÂn. Sciencia Guaiance, 9, 160 p. Holdridge, L.R., 1947. Determination of plant formation from simple climatic data. Science 105, 367±368. Holland, E.A., Townsend, A.R., Vitousek, P.M., 1995. Variability in temperature regulation of CO2 ¯uxes and N mineralization from ®ve Hawaiian soils: implications for a changing climate. Global Change Biology 1, 115±123. Insam, H., Haselwandter, K., 1989. Metabolic quotient of the soil micro¯ora in relation to plant succession. Oecologia 79, 174±178. Joergensen, R.G., Anderson, T.H., Wolters, V., 1995. Carbon and nitrogen relationships in the microbial biomass of soils in beech (Fagus sylvatica L.) forests. Biology and Fertility of Soils 19, 141±147. Jordan, C.F. (Ed.), 1989. An Amazonian Rainforest MAB, vol. 2. UNESCO and Parthenon, Paris/Casterton Hall/Park Ridge. Jurik, T.W., Briggs, G.M., Gates, D.M., 1991. Soil respiration of ®ve aspen stands in northern Lower Michigan. American Midland Naturalist 126, 68±75. Kirschbaum, M.U.F., 1995. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biology & Biochemistry 27, 753±760. Kursar, T.A., 1989. Evaluation of soil respiration and soil CO2 concentration in a lowland moist forest in Panama. Plant and Soil 113, 21±29. Loft®eld, N.S., Brumme, R., Beese, F., 1992. Automated monitoring of nitrous oxide and carbon dioxide ¯ux from forest soils. Soil Science Society of America Journal 56, 1147±1150. Maggs, J., Hewett, B., 1990. Soil and litter respiration in rainforests of contrasting nutrient status and physiognomic structure near lake Eacham, north-east Queensland. Australian Journal of Ecology 15, 329±336. Mao, D.M., Min, Y.W., Yu, L.L., Martens, R., Insam, H., 1992. Effect of afforestation on microbial biomass and activity in soils of tropical China. Soil Biology & Biochemistry 24, 865±872. Marumoto, T., Anderson, J.P.E., Domsch, K.H., 1982. Mineralisation of nutrients from soil microbial biomass. Soil Biology & Biochemistry 14, 469±475. Medina, E., Zelwer, M., 1972. Soil respiration in tropical plant communities. In: Golley, P.M., Golley, F.B. (Eds.). Tropical Ecology, Athens, USA, pp. 245±267. Prasad, P., Basu, S., Behera, N., 1994. A comparative account of the microbial characteristics of soils under natural forest, grassland and crop®eld from Eastern India. Plant and Soil 175, 85±91.
509
Priess, J.A., 1996. Wurzeldynamik und ZersetzeraktivitaÈt in Ca-de®zitaÈren BoÈden unter tropischem Feuchtwald, Venezuela. GoÈttinger BeitraÈge zur Land- und Forstwirtschaft in den Tropen und Subtropen, vol. 110. Goltze, GoÈttingen (151 p.). Priess, J., FoÈlster, H., 1994. Carbon cycle dynamics and soil respiration of forests under natural degradation in the Gran Sabana. Interciencia 19, 317±322. Priess, J., FoÈlster, H., Then, C., 1999. Litter and ®ne-root production in three types of tropical premontane rain forest in SE Venezuela. Plant Ecology 143, 171±187. Raich, J.W., Nadelhoffer, K., 1989. Belowground carbon allocation in forest ecosystems: global trends. Ecology 70, 1346±1354. Raich, J.W., Schlesinger, W.H., 1992. The global carbon dioxide ¯ux in soil respiration and ist relationship to vegetation and climate. Tellus 44B, 81±99. Schubert, C., 1986. Terrazas aluviales en el escudo de Guayana: informe preliminar. Acta Scienti®ca Venezolana 37, 226±228. Singh, J.S., Gupta, S.R., 1977. Plant decomposition and soil respiration in terrestrial ecosystems. Botanical Reviews 43, 449±528. Singh, R.S., Srivastava, S.C., Raghubanshi, A.S., Singh, J.S., Singh, S.P., 1991. Microbial C, N and P in dry tropical savanna: effects of burning and grazing. Journal of Applied Ecology 28, 869±878. Sparling, G.P., Williams, B.L., 1986. Microbial biomass in organic soils: estimation of biomass C, and effect of glucose or cellulose amendments on the amounts of N and P released by fumigation. Soil Biology & Biochemistry 18, 507±513. Srivastava, S.C., Singh, J.S., 1991. Microbial C, N and P in dry tropical forest soils: effects of alternate land-uses and nutrient ¯ux. Soil Biology & Biochemistry 23, 117±124. USDA, 1975. Soil taxonomy; a basic system of soil classi®cation for making and interpreting soilsurveys. Agriculture Handbook No. 436. Soil Survey Staff/USDA, Washington DC (pp. 323±332). Wardle, D.A., Ghani, A., 1995. Why is the strength of relationships between pairs of methods for estimating soil microbial biomass often so variable? Soil Biology & Biochemistry 27, 821±828. Wolters, V., Joergensen, R.G., 1991. Microbial carbon turnover in beech forest soils at different stages of acidi®cation. Soil Biology & Biochemistry 23, 897±902. Yang, J.C., Insam, H., 1991. Microbial biomass and relative contributions of bacteria and fungi in soil beneath tropical rainforest, Hainan Island, China. Journal of Tropical Ecology 7, 385±393.
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Microbial properties and soil respiration in submontane forests of Venezuelian Guyana: characteristics and response to fertilizer treatments J.A. Priess*, H. FoÈlster Institute of Soil Science and Forest Nutrition, University of GoÈttingen, BuÈsgenweg 2, D-37077 GoÈttingen, Germany Received 7 June 1999; received in revised form 14 February 2000; accepted 27 July 2000
Abstract The distribution of vegetation types in Venezuelan Guyana (in the `Canaima' National Park) represents a transitional stage in a long term process of savannization, a process considered to be conditioned by a combined chemical and intermittent drought stress. All types of woody vegetation in this environment accumulate large amounts of litter and soil organic carbon (SOC). We hypothesized that this accumulation is caused by low microbial activity. During 1 year we measured microbial biomass carbon (Cmic), microbial respiration and soil respiration of stony Oxisols (Acrohumox) at a tall, a medium and a low forest and with three chemical modi®cations of site conditions by the addition of 21 21 NO2 and PO32 in the mineral topsoil and 3 ; Ca 4 as possible limiting elements. Due to high SOC contents, mean Cmic was 1 mg g soil 21 3 mg g soil in the forest ¯oor. Mean microbial respiration in the mineral topsoil and the forest ¯oor were 165 and 192 mg CO2C g soil 21 d 21, respectively. We calculated high mean metabolic quotients (qCO2) of 200 mg CO2-C g Cmic 21 d 21 in the litter layer and 166 mg CO2-C g Cmic 21 d 21 in the mineral topsoil, while the Cmic-to-SOC ratios were as low as 1.0% in the litter layer and 0.8% in the mineral topsoil. Annual soil respiration was 9, 12 and 10 Mg CO2-C ha 21 yr 21 in the tall, medium and low forest, respectively. CO2 production was signi®cantly increased by CaHPO4 fertilization, but no consistent effects were caused by Ca 21 and NO2 3 ; fertilization. Our ®ndings indicate that Cmic and microbial respiration are reduced by low nutrient concentrations and low litter and SOC quality. Reduced microbial decomposition may have contributed to SOC accumulation in these forests. q 2001 Elsevier Science Ltd. All rights reserved. Keywords: Microbial biomass; Microbial respiration; Substrate induced respiration; Respiratory quotient (qCO2); Soil nutrients; Tropical rain forest; Oxisol
1. Introduction The `Gran Sabana' represents a substantial part of the Venezuelan Guyana highlands (800±1500 m a.s.l.). Its vegetation cover is characterized by a mosaic of tall to low forests, secondary bush and savanna. According to FoÈlster (1986, 1992), Hernandez (1992) and Dezzeo (1994), this mosaic represents a transitional stage of a long-term autochthonous process of savannization. Destabilization of forests may be triggered by ®res, but is essentially conditioned by a combined effect of chemical stress caused by Ca-de®ciency and Al-toxicity and hydrological stress due to shallow rooting in stony soils and drought periods. Previous studies in the region have provided insights into vegetation types, carbon and nutrient * Corresponding author. Present address: Laboratory of Soil Science and Geology, Wageningen Agricultural University, P.O. Box 37, 6700 AA Wageningen, The Netherlands. Fax: 131-317-482419. E-mail address: [email protected] (J.A. Priess).
stocks (Dezzeo, 1994; FoÈlster, 1986, 1992; Hernandez, 1987, 1992). Aboveground litter production falls within the range reported for tropical forests, but high ®ne-root production was measured in these forests by Priess et al. (1999). The latter authors found consistently high fractions of root necromass and concluded that the accumulation of dead roots was caused by slow mineralization. All forest types in the region (Dezzeo, 1994, Hernandez, 1999), have accumulated large amounts of organic carbon in the litter layer and the mineral soil. We hypothesized that soil acidity and nutrient de®ciency limit the activity or ef®ciency of soil microorganisms. We tested our hypotheses by modifying soil chemical conditions by addition of Ca 21, 32 NO2 3 and PO4 ; which were considered the most likely de®cient elements (FoÈlster, 1986, 1992), using quantitative measurements of Cmic, microbial respiration and soil respiration. The studies were carried out at three forest sites, differing in tree biomass and productivity (Dezzeo, 1990; Priess et al., 1999).
0038-0717/01/$ - see front matter q 2001 Elsevier Science Ltd. All rights reserved. PII: S 0038-071 7(00)00191-7
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504
Table 1 Selected soil chemical properties of the forest ¯oor and the mineral topsoil 0±10 cm; values represent means ^ standard deviation n 5 Forest type Forest ¯oor Tall Medium Low
pHKCl
N
C-to-N
21
3.3 ^ 0.1 3.3 ^ 0.1 3.1 ^ 0.1
mg g 251 ^ 28 268 ^ 31 329 ^ 8.0
4.3 ^ 0.1 4.2 ^ 0.1 4.4 ^ 0.1
118 ^ 12 115 ^ 31 119 ^ 12
Ptotal
K 21
10.1 ^ 5.8 12.7 ^ 1.8 15.4 ^ 0.9
19.1 ^ 2.0 21.3 ^ 1.7 21.4 ^ 0.9
mg g 21
Mineral soil Tall Medium Low
C
7.6 ^ 0.7 6.7 ^ 1.6 6.3 ^ 0.6
15.4 ^ 0.6 16.9 ^ 0.8 19.0 ^ 0.4
2. Materials and methods 2.1. Site description The geology of the Guyana highland is dominated by the Precambrian Roraima formations, which consist of an alteration of clay- and sandstones giving rise to a cuesta landscape (Schubert, 1986). The study site `La Sabanita' (approximately 580 0 N; 6180 0 W; 1150±1200 m asl.) in the southern part of the Gran Sabana, about 5 km east of the village San Francisco de YuruanõÂ, is a ridge topped by a savanna patch with fringes of bushland. On the upper slope, the vegetation changes gradually from a single storey forest (`low forest') of about 10 m height via a medium high forest (`medium forest') to a higher multi-storey forest of up to 35 m height (`tall forest'). Aboveground biomass was estimated at 143, 360 and 342 Mg ha 21, and ®ne-root biomass at 9.6, 12.2 and 11.4 Mg ha 21 in the low, medium and tall forest, respectively (Dezzeo, 1990). The sites are within the `submontane moist forest zone' (Holdridge, 1947). Annual precipitation during the study was 2200 mm in 1990/91 (Priess and FoÈlster, 1994). The dry season usually lasts from January to March, but rainfall may decrease during December and increase in late April. Mean annual air temperature was 20.68C with small seasonal variations. During the experiments, monthly precipitation was within one standard deviation of the long-term average of the weather-station in San Ignacio located 12 km away (Priess et al., 1999). Soils were classi®ed as Acrohumox (Soil taxonomy, USDA, 1975). They are consistently covered by an organic horizon of 6±12 cm corresponding to 50±100 Mg ha 21 with a dense root mat, which contains up to 50% of the ®ne roots of the entire pro®le (Dezzeo, 1990). Root penetration of the mineral soil remains shallow. Despite the high organic matter content of 12% at 0±10 cm depth, the CEC of the topsoils averaged only 100 mmol g soil 21 due to the low pH. The clay content of the ®ne soils is approximately 40%, but the CEC of the kaolinitic clay is extremely low (20 mmol g clay 21). The exchangeable cations are dominated by Al n1 with 80±90% of CEC. Concentrations of 1 21 NH1 are always higher than those of Ca 21 4 ; K and Mg (Table 1). From the tall via the medium to the low forest,
Ca
Mg
Al
0.20 ^ 0.08 0.15 ^ 0.03 0.18 ^ 0.02
1.53 ^ 0.10 1.05 ^ 0.13 0.36 ^ 0.02
120 ^ 8.0 129 ^ 15.8 89 ^ 5.1
2.51 ^ 0.66 2.10 ^ 0.53 1.97 ^ 0.23
94.0 ^ 15.9 87.9 ^ 25.4 74.6 ^ 7.7
21
mg g 366 ^ 27 362 ^ 15 552 ^ 29
mg g 4.7 ^ 0.5 3.0 ^ 0.4 0.7 ^ 0.1
mg g 21
mmol g 21 exchangeable cations
25.3 ^ 2.4 23.0 ^ 1.6 47.2 ^ 3.1
2.55 ^ 0.52 2.32 ^ 0.66 2.09 ^ 0.41
1.60 ^ 0.37 1.40 ^ 0.54 1.29 ^ 0.44
soil nutrient concentrations, except for PO32 4 ; decrease both in the organic layer and in the mineral soil (Table 1). The water storage of the soils is reduced by their high stone content (stones in the low forest: 60±65%; tall and medium forest: 30±35%). We found considerable admixtures of mineral soil in the forest ¯oor (relatively low C and high Al contents). 2.2. Experimental design We set up a factorial design of four treatments (control, CaCl2, NaNO3, CaHPO4) on three forest sites with ®ve replicates per treatment. At each site tall forest (2500 m 2), medium forest (900 m 2) and low forest (2500 m 2) we marked 20 randomly chosen treatment-plots of 1 m 2 at a minimum distance of 1 m from footpaths and trees. The frames for soil respiration measurements were placed permanently in the center of each treatment-plot. Fertilizer application of the treatment-plots was 450 kg Ca ha 21, 300 kg N ha 21, and 350 kg P ha 21 in the tall and medium forest. In the low forest, we applied only 50% of fertilizer, because the amount of ®ne soil was approximately 50% of the ®ne soils at the tall and medium forest. Fertilizers were applied in liquid form, except for phosphate, which was applied as granulate two weeks before the experiments began. 2.3. Microbial C and microbial respiration Cmic was measured in the forest ¯oor and the mineral soil 0±10 cm depth separately, using the SIR method (Anderson and Domsch, 1978). Alternately every 3±4 weeks we collected 15 samples per treatment of the 1 m 2 fertilizer plots either from the forest ¯oor (20 g each) or the mineral soil (100 g each) and pooled them as one composite sample. We added 1% solid glucose and incubated samples for 6 h in gas tight syringes (Heilmann and Beese, 1992). Microbial respiration was measured in two replicates of composite samples in gas tight syringes at 228C for 6 h. CO2 concentrations were measured every hour and microbial respiration was calculated as mean value of six consecutive measurements. Soil moisture was expected to be the main driver for seasonal variation of microbial respiration. For
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505
Table 2 Microbial C and microbial respiration; ®gures represent annual means ^ standard deviation n 5; different letters indicate signi®cant differences between treatments P 0:05 Treatment
Tall forest Forest ¯oor
Medium forest
Low forest
Mineral soil (0±10 cm)
Forest ¯oor
Mineral soil (0±10 cm)
Forest ¯oor
Mineral soil (0±10 cm)
0.94 ^ 0.10a 1.20 ^ 0.15b 1.30 ^ 0.28b
2.84 ^ 0.65 2.40 ^ 0.42 2.81 ^ 0.48
1.17 ^ 0.31 1.30 ^ 0.33 1.25 ^ 0.33
3.32 ^ 0.65 3.53 ^ 1.24 3.13 ^ 1.21
1.18 ^ 0.38a 1.53 ^ 0.27b 1.45 ^ 0.23b
200 ^ 30 200 ^ 20 190 ^ 40
160 ^ 50 200 ^ 60 160 ^ 50
180 ^ 10 160 ^ 30 190 ^ 20
180 ^ 20 170 ^ 20 140 ^ 30
21
Cmic (mg C g soil ) Control 2.78 ^ 0.64 CaCl2 2.61 ^ 0.05 NaNO3 2.94 ^ 0.34
Microbial respiration (mg CO2-C g soil 21 d 21) Control 240 ^ 140 150 ^ 40 CaCl2 200 ^ 10 170 ^ 40 NaNO3 210 ^ 20 150 ^ 50
that reason, we measured microbial respiration at actual soil moisture, rather than adjusting moisture to standard conditions. Measurements of Cmic and microbial respiration included three treatments (control, Ca and NO2 3 and were repeated three times in the rainy and twice in the dry season. 2.4. Soil respiration We used the static chamber method (Loft®eld et al., 1992) with ®ve replicates per treatment. Cylindric plastic frames (dia: 25 cm) were installed 3±5 cm in the soil or organic layer. The depth of insertion was restricted to the surface layer, to reduce cutting of lateral roots. The area inside the frames was kept free of vegetation. During the measurements, plastic chambers of 4.3 dm 3 were ®xed airtight on the frames, and gas samples were taken with gastight syringes 1.0, 3.5, 6.0 and 8.5 min after closing the chamber. Total sampling volume was less than 1% of the chamber's volume to avoid the effect of accelerated mass ¯ow (Freijer and Bouten, 1991). During 14 months, soil respiration was measured every 3±4 weeks from 09.00± 11.00 h. Samples were analyzed on the same day using a gas chromatograph equipped with a thermal conductivity detector. Measurements started two months after the insertion of the frames to reduce the effects of soil disturbance on C mineralization. For a correct assessment of annual CO2 production we also measured nighttime soil respiration. During a measuring campaign in August 1990, the three forest sites n 15 frames of the control plots) showed no signi®cant difference between daytime (09.00±11.00 h: 3:2 ^ 1:0 g CO2C m 22 d 21) and nighttime (21.00±23.00 h: 3:1 ^ 1:1 g CO2-C m 22 d 21) respiration. In consequence, only daytime measurements were continued. At the end of the experiments we wanted to ®nd out, whether the permanent installation of measurement frames affected ®ne-root density. For that reason we cut 1000 cm 3 soil-blocks within and outside (30 cm distance) of all frames of the control plots, separated and weighed the roots. Root densities (inside 6:0 ^ 2:2 g dm23 ; outside 6:5 ^ 2:3 g dm 2 3; n 15 did not differ signi®cantly.
2.5. Statistics We used the SAS 6.12 statistics package for Windows to analyze the principle effects with nested multi-factorial (repeated measure) ANOVA. Soil respiration data were tested with two factorial repeated measure ANOVA (sites, treatments) and three factorial ANOVA (sites, treatments, season). Microbial biomass C and basal respiration data were tested with three factorial repeated measure ANOVA (sites, treatments, soil depth). For comparisons of paired samples the T-test was used. Linear regressions were calculated with ms-excel 97.
3. Results 3.1. Microbial properties The highest concentrations of Cmic were measured in the low forest and the lowest concentrations in the tall forest (Table 2). The ANOVA revealed a highly signi®cant effect of sites P , 0:0001: At all sites Cmic was signi®cantly lower during the dry season and higher during the rainy season. The seasonal effect was more pronounced in the forest ¯oor, where seasonal variation in soil moisture was larger than in the mineral soil (soil moisture differences: forest ¯oor: 47 vol.%; mineral soil: 12 vol.%). According to ANOVA results, fertilizer treatments did not affect Cmic signi®cantly P , 0:27: However, the ANOVA results were in¯uenced by a signi®cant interaction between the factors treatment and soil depth. Pairwise comparisons of Cmic of different sites showed that Cmic of the control and the Ca treatment in the forest ¯oor of the low forest was signi®cantly larger than in the other two forests P , 0:05: Pairwise comparisons of treatments revealed signi®cantly larger Cmic in the fertilized mineral soils of the tall and the low forest P , 0:05: Cmic concentrations in the forest ¯oor of all sites were 2- to 3-fold higher than in the mineral topsoil (ANOVA: soil depth: P , 0:0001: The ratios of Cmic-to-SOC did not differ between sites or treatments, but were signi®cantly higher P , 0:05 in the forest ¯oor (1.0%) than in the mineral topsoil (0.8%).
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Table 3 Mean annual and mean seasonal soil respiration of control, Ca 21, NO2 3 and CaHPO4 treatment in tall, medium and low forest; ®gures represent annual or seasonal means ^ standard deviation n 5 Period
Forest type
Treatment Control
Ca
NO2 3
CaHPO4
8.96 ^ 2.46 12.41 ^ 3.19 10.24 ^ 3.43
9.80 ^ 2.38 11.30 ^ 2.81 10.63 ^ 4.08
10.96 ^ 2.92 9.90 ^ 3.17 9.72 ^ 3.46
13.17 ^ 3.75 16.34 ^ 5.59 11.65 ^ 3.17
Rainy season (g CO2-C m 22 d 21) a Tall Medium Low
2.69 ^ 0.57 3.75 ^ 0.73 3.13 ^ 0.92
2.85 ^ 0.59 3.33 ^ 0.63 3.21 ^ 1.06
3.23 ^ 0.72 2.88 ^ 0.87 2.98 ^ 0.92
3.87 ^ 0.91 4.70 ^ 1.54 3.67 ^ 0.64
Dry season (g CO2-C m 22 d 21) a Tall Medium Low
2.01 ^ 0.66 2.73 ^ 0.75 2.16 ^ 0.58
2.35 ^ 0.67 2.65 ^ 0.86 2.39 ^ 1.07
2.56 ^ 0.78 2.37 ^ 0.78 2.04 ^ 0.66
3.09 ^ 1.10 4.05 ^ 1.45 2.24 ^ 0.31
21
21
Year (Mg CO2-C ha yr ) Tall Medium Low
a
We measured 10 times during the rainy (275 d) and three times during the dry season (90 d).
Average microbial respiration was 192 ^ 27 mg CO2C g soil 21 d 21 in the forest ¯oor and 165 ^ 42 mg CO2C g soil 21 d 21 in the mineral soil (ANOVA: P , 0:01; but was not signi®cantly different between sites or treatments. Regression analysis showed contrasting relationships between soil moisture and microbial respiration P , 0:05 in the forest ¯oor resporg 0:0003 £ moisture% 1 0:164; r 0:35 and in the mineral soil r 20:49: respmin 20:0017 £ moisture% 1 0:273; That means during the dry season microbial respiration was reduced in the forest ¯oor, while in the mineral soil it was enhanced. The metabolic quotients (qCO2), i.e. microbial respiration per unit microbial biomass were signi®cantly different P , 0:01; n 33 between forest ¯oor 200 ^ 53 mg CO2-C g microbial C 21 d 21) and mineral soil 166 ^ 44 mg CO2-C g microbial C 21 d 21). No signi®cant differences were detected between sites or treatments. 3.2. Soil respiration Annual soil respiration rates in the tall, medium and low forest were 9.0, 12.4 and 10.2 Mg CO2-C ha 21 yr 21 (Table 3) and were all signi®cantly different from each other. Fertilizer treatments caused a signi®cant effect (ANOVA P , 0:005 and variability was comparable to the variability of the control plots. All plots treated with CaHPO4 had a significantly higher soil respiration, compared to the other treatments. No consistent trends were observed for the plots that were fertilized with Ca or NO2 3 : The CaHPO4 plots were the only ones where the pH value of the topsoil increased significantly during the experiments (10.5 units). Soil respiration followed a clear seasonal trend, with higher CO2 production in the rainy season and lower CO2 production during the dry season (Fig. 1). On average 20%
of the carbon ¯ux occurred during the dry season (90 d) and 80% during the rainy season (275 d).
4. Discussion 4.1. Microbial variables The values of microbial biomass measured in this study 0:9±1:5 mg Cmic g soil 21 in the mineral soil and 2.4± 3.5 mg Cmic g soil 21 in the forest ¯oor) are high compared to other tropical forests (0.27±0.79 mg Cmic g soil 21; Jordan, 1989; Srivastava and Singh, 1991; Yang and Insam, 1991; Mao et al., 1992) but fall within the range reported for some temperate forests (Wolters and Joergensen, 1991; Joergensen et al., 1995). They re¯ect the very high SOC contents of our forest soils, as Cmic is closely related to SOC (Brookes et al., 1990; Bauhus and Khanna, 1999). However, if this relationship is quanti®ed as Cmicto-SOC ratio, it is obvious that microbial biomass does not increase in line with soil organic matter. The low ratios of 1.0% in the forest ¯oor and 0.8% in the top mineral soil we measured, are below the range recorded in literature for tropical soils of 1±5% (Srivastava and Singh, 1991; Yang and Insam, 1991; Mao et al., 1992; Prasad et al., 1994). As Cmic-to-SOC ratios are explained by SOC quality, (Bauhus and Khanna, 1999), low ratios should indicate adverse substrate properties. The low Cmic-to-SOC ratios we found in our study might be conditioned on the one hand by a low N content of the scleromorphous leaf litter, and on the other hand by the effects of soil acidity and low nutrient availability (Wolters and Joergensen, 1991; Joergensen et al., 1995; Bauhus and Khanna, 1999). Both seasonal increases (Singh et al., 1991) and decreases (Marumoto et al., 1982; Sparling and Williams, 1986; Prasad et al., 1994) in Cmic have been reported from agricultural and
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Fig. 1. Soil respiration (g CO2-C m 22 d 21) in the tall forest, medium forest and low forest soil respiration was measured with static chambers over 1 yr. Datapoints represent means n 5; error bars represent standard deviation. X-axis presents day and month.
forest ecosystems depending on substrate availability or drying and rewetting effects. We measured a signi®cant decrease of Cmic during the dry season. Because of the larger seasonal moisture differences, the reduction in biomass C was more pronounced in the forest ¯oor than in the mineral soil. Our ®nding of an inverse relationship of soil moisture and microbial respiration in the mineral soil means that a lower amount of active microbes produced more CO2 in drier soils. As this effect is signi®cant but not very strong, it does not indicate prolonged periods of water saturation or lack of oxygen in the rapidly draining forest soils. The values of microbial respiration and qCO2 measured in our study are high, when compared to the data that have been published. Few studies of microbial respiration and qCO2 have been reported from tropical forests. Mao et al. (1992) reported microbial respiration of 4.91 mg CO2-C g soil21 d 21 and qCO2 of 18.4 mg CO2-C g microbial C 21 d 21 from an old secondary forest in South China. Prasad et al. (1994) calculated microbial respiration of 8.66 mg CO2-C g soil21 d 21 and qCO2 of 13.5 mg CO2-C g microbial C 21 d 21 from a natural forest in Orissa, India. Both forests had lower Corg (85±90% lower) and Cmic (35±75% lower) contents than the forest sites we studied, as well as much lower microbial respiration (94±97% lower). Thus, in our present study the qCO2 or carbon use ef®ciency of the soil microbes was considerably lower than reported for other tropical forests. In recent years, the qCO2 has been used as bioindicator for ecosystem succession (Insam and Haselwandter, 1989) and environmental stress (Wolters and Joergensen, 1991; Anderson and Domsch, 1993; Joergensen et al., 1995) in temperate ecosystems. Following the hypothesis that environmental stresses like low pH, high Al, low SOM quality or nutrient de®ciency reduce carbon use ef®ciency, the high qCO2 values we measured in our study would indicate a stressed soil microbial community. However, the use of qCO2
as bioindicator has been criticized, because it fails to distinguish between disturbance and stress effects (Wardle and Ghani, 1995). In our study we can exclude human disturbance in recent decades. We conclude that the high qCO2 values are probably related to chemical stress. This interpretation is supported by ®ndings of Priess et al. (1999) from the same forests, who reported low nutrient concentrations in ®ne roots and high fractions of ®ne root necromass. The author's assume that the accumulation of root necromass is caused by the slow mineralization of the nutrient poor substrate. We had hypothesized that besides P, Ca and NO2 3 also might be de®cient elements in the system. Their addition, however, did not produce a consistent effect. Tropical forests growing on nutrient poor soils are supposed to establish an almost closed nutrient cycle (Jordan, 1989), i.e. roots and soil microorganisms are very ef®cient in the uptake of sparse nutrients. However, FoÈlster (1986) repeatedly found relatively high concentrations of Ca 21 and NO2 3 in the soil solution below the rooting zone of forests in the Gran Sabana. Element uptake from soil solution is possibly not so ef®cient when compared to element drainage, so we consider the fertilizer aspect in regard to these two elements as inconclusive. 4.2. Soil respiration The static chamber method has been criticized for underestimating C-¯uxes, because lateral roots can be cut or their growth into the chambers could be inhibited by the inserted frames. However, we found no differences in root densities inside and outside the frames. In various studies, diurnal cycles of respiration have been reported (Venezuela: Medina and Zelwer, 1972; India: Singh and Gupta, 1977; USA: Grahammer et al., 1991). However, no such diurnal
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variation was detected in a tropical rainforest by Kursar (1989) or in our experiments. In the present study soil temperatures were typically 1±28C lower at night. Assuming a Q10 1.4±2 (Holland et al., 1995) or 2.5 (Kirschbaum, 1995), a temperature reduction of 28C would cause a reduction of soil respiration by 7±16% in our study. According to Raich and Nadelhoffer (1989) annual soil respiration in tropical forests ranges from 2.2 to 15.1 Mg CO2-C ha 21 yr 21. Our premontane forest sites (tall: 8.96, medium: 12.41 and low: 10.24 Mg CO2-C ha 21 yr 21) fall within this range, but are below the mean of 12:6 ^ 0:6 Mg CO2-C ha 21 yr 21 calculated for tropical moist forests by Raich and Schlesinger (1992). The ANOVA revealed highly signi®cant effects of site, season and fertilizer treatments. Rerunning the ANOVA without the CaHPO4-treatment showed that neither the Ca nor the NO2 3 treatments had an effect on soil respiration. Pairwise comparisons resulted in some signi®cant fertilizer effects, but without a consistent trend. While the seasonal variation in soil respiration was clearly related to soil moisture, the origin of the fertilizer effects was less clear. In all experiments but the CaHPO4-treatment, the pH of soil and soil solution remained almost unchanged. The CaHPO4treatment caused the pH to increase signi®cantly by 0.5 units, thus producing presumably a combined pH-fertilizer effect. The interpretation is further complicated by the fact, that the pH shift resulted in an increased cation exchange capacity (150%) and a lower Al-solubility, which could bias soil respiration. We cannot identify whether root or microbial respiration was responsible for the increased soil respiration. However, as ®ne root growth at the same sites doubled in the CaHPO4-fertilized plots (Priess, 1996), we assume that root respiration also increased strongly. Soil moisture content and temperature are key factors in the regulation of soil and litter respiration (Kursar, 1989; Raich and Nadelhoffer, 1989; Cavelier and PenÄuela, 1990; Maggs and Hewett, 1990; Jurik et al., 1991). Soil respiration during the rainy season was about 50% higher than during the dry season (Table 2). In two rainforests in north-east Queensland seasonal pattern as well as annual CO2 release (13.6 and 14.4 Mg CO2-C ha 21 yr 21) were comparable with our results (Maggs and Hewett, 1990). Davidson and Trumbore (1995) measured a 20% higher surface ¯ux of CO2 during the rainy season in a rainforest of East Amazonia compared to the dry season. A reduction of soil respiration during the rainy season and a sharp decline of 40% immediately after rain events were observed by Buchmann et al. (1997) in a rainforest in French Guiana. Buchmann et al. (1997) assume that oxygen de®ciency was responsible for this effect. We also observed a pronounced decline of CO2 production directly following rainfall (data not shown). However, the reduced CO2 emissions were followed by strongly enhanced emissions, suggesting that diffusion was limited only for some minutes in the rapidly draining soils. Due to the extremely variable effects on soil respiration, measurements affected by rainfalls were omitted and repeated.
Acknowledgements This study was partly supported by the German Research Foundation (DFG). We gratefully acknowledge the scienti®c and logistic support of CVG-EDELCA gerencia de estudios e ingenerõÂa. We thank E. Veldkamp, H. Flessa, W. Borken and two anonymous reviewers for critically revising earlier versions of the manuscript. References Anderson, J.P.E., Domsch, K.H., 1978. A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biology & Biochemistry 10, 215±221. Anderson, T.H., Domsch, K.H., 1993. The metabolic quotient for CO2 (qCO2) as a speci®c activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biology & Biochemistry 25, 393±395. Bauhus, J., Khanna, P.K., 1999. The signi®cance of microbial biomass in forest soils. In: Rastin, N., Bauhus, J. (Eds.). Going Underground Ð Ecological Studies in Forest Soils, Research Signpost, Trivandrum, pp. 77±110. Brookes, P.C., Ocio, J.A., Wu, J., 1990. The soil microbial biomass: its measurement, properties and role in soil nitrogen and carbon dynamics following substrate incorporation. Soil Biology & Biochemistry 35, 39±51. Buchmann, N., Guehl, J.M., Barigah, T.S., Ehleringer, J.R., 1997. Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110, 120±131. Cavelier, J., PenÄuela, M.C., 1990. Soil respiration in the cloud forest and dry deciduous forest of Cerrania de Macuira, Colombia. Biotropica 22, 346±352. Davidson, E.A., Trumbore, S.E., 1995. Gas diffusivity and production of CO2 in deep soils of the Eastern Amazon. Tellus 47B, 550±565. Dezzeo, N., 1990. Bodeneigenschaften und NaÈhrstoffvorratsentwicklung in autochton degradierenden WaÈldern SO-Venezuelas. GoÈttinger BeitraÈge zur Land- und Forstwirtschaft in den Tropen und Subtropen, vol. 53. Liddy Halm, GoÈttingen. Dezzeo, N. (Ed.), 1994. EcologõÂa de la altiplanicie de la Gran Sabana (Guayana Venezolana). I. Investigaciones sobre la dinaÂmica bosquesabana en el sector SE: Subcuencas de los RõÂos YuruanõÂ, ArabopoÂ, y Alto KukenaÂn. Sciencia Guaianae, vol. 4. FoÈlster, H., 1986. Forest-savanna dynamics and deserti®cation processes in the Gran Sabana. Interciencia 11, 311±316. FoÈlster, H., 1992. Holocene autochthonous forest degradation in southeast Venezeula. In: Goldammer, J.G. (Ed.). Tropical Forests in Transition, BirkhaÈuser, Basel, pp. 25±44. Freijer, J., Bouten, W., 1991. A comparison of ®eld methods for measuring soil carbon dioxide evolution: experiments and simulation. Plant and Soil 135, 133±142. Grahammer, K., Jawson, M.D., Skopp, J., 1991. Day and night soil respiration from a grassland. Soil Biology & Biochemistry 23, 77±81. Heilmann, B., Beese, F., 1992. Miniaturized method to measure carbon dioxide production and biomass of soil microorganisms. Soil Science Society of America Journal 56, 596±598. Hernandez, L., 1987. DegradacioÂn de los bosques de la Gran Sabana. Pantepui 3, 11±25. Hernandez, L., 1992. Gliederung Struktur und ¯oristische Zusammensetzung von WaÈldern und ihrer Degradations- und Regradationsphasen im Guayana-Hochland, Venezuela. GoÈttinger BeitraÈge zur Land und Forstwirtschaft in den Tropen und Subtropen, vol. 70. Goltze, GoÈttingen (198pp.). Hernandez, L. (Ed.), 1999. EcologõÂa de la Altiplanicie de la Gran Sabana
J.A. Priess, H. FoÈlster / Soil Biology & Biochemistry 33 (2001) 503±509 (Guayana Venezolana). II. Estructura, diversidad, crecimiento y adaptacioÂn en bosques de las subcuencas de los rõÂos YuruanõÂ y Alto KukenaÂn. Sciencia Guaiance, 9, 160 p. Holdridge, L.R., 1947. Determination of plant formation from simple climatic data. Science 105, 367±368. Holland, E.A., Townsend, A.R., Vitousek, P.M., 1995. Variability in temperature regulation of CO2 ¯uxes and N mineralization from ®ve Hawaiian soils: implications for a changing climate. Global Change Biology 1, 115±123. Insam, H., Haselwandter, K., 1989. Metabolic quotient of the soil micro¯ora in relation to plant succession. Oecologia 79, 174±178. Joergensen, R.G., Anderson, T.H., Wolters, V., 1995. Carbon and nitrogen relationships in the microbial biomass of soils in beech (Fagus sylvatica L.) forests. Biology and Fertility of Soils 19, 141±147. Jordan, C.F. (Ed.), 1989. An Amazonian Rainforest MAB, vol. 2. UNESCO and Parthenon, Paris/Casterton Hall/Park Ridge. Jurik, T.W., Briggs, G.M., Gates, D.M., 1991. Soil respiration of ®ve aspen stands in northern Lower Michigan. American Midland Naturalist 126, 68±75. Kirschbaum, M.U.F., 1995. The temperature dependence of soil organic matter decomposition, and the effect of global warming on soil organic C storage. Soil Biology & Biochemistry 27, 753±760. Kursar, T.A., 1989. Evaluation of soil respiration and soil CO2 concentration in a lowland moist forest in Panama. Plant and Soil 113, 21±29. Loft®eld, N.S., Brumme, R., Beese, F., 1992. Automated monitoring of nitrous oxide and carbon dioxide ¯ux from forest soils. Soil Science Society of America Journal 56, 1147±1150. Maggs, J., Hewett, B., 1990. Soil and litter respiration in rainforests of contrasting nutrient status and physiognomic structure near lake Eacham, north-east Queensland. Australian Journal of Ecology 15, 329±336. Mao, D.M., Min, Y.W., Yu, L.L., Martens, R., Insam, H., 1992. Effect of afforestation on microbial biomass and activity in soils of tropical China. Soil Biology & Biochemistry 24, 865±872. Marumoto, T., Anderson, J.P.E., Domsch, K.H., 1982. Mineralisation of nutrients from soil microbial biomass. Soil Biology & Biochemistry 14, 469±475. Medina, E., Zelwer, M., 1972. Soil respiration in tropical plant communities. In: Golley, P.M., Golley, F.B. (Eds.). Tropical Ecology, Athens, USA, pp. 245±267. Prasad, P., Basu, S., Behera, N., 1994. A comparative account of the microbial characteristics of soils under natural forest, grassland and crop®eld from Eastern India. Plant and Soil 175, 85±91.
509
Priess, J.A., 1996. Wurzeldynamik und ZersetzeraktivitaÈt in Ca-de®zitaÈren BoÈden unter tropischem Feuchtwald, Venezuela. GoÈttinger BeitraÈge zur Land- und Forstwirtschaft in den Tropen und Subtropen, vol. 110. Goltze, GoÈttingen (151 p.). Priess, J., FoÈlster, H., 1994. Carbon cycle dynamics and soil respiration of forests under natural degradation in the Gran Sabana. Interciencia 19, 317±322. Priess, J., FoÈlster, H., Then, C., 1999. Litter and ®ne-root production in three types of tropical premontane rain forest in SE Venezuela. Plant Ecology 143, 171±187. Raich, J.W., Nadelhoffer, K., 1989. Belowground carbon allocation in forest ecosystems: global trends. Ecology 70, 1346±1354. Raich, J.W., Schlesinger, W.H., 1992. The global carbon dioxide ¯ux in soil respiration and ist relationship to vegetation and climate. Tellus 44B, 81±99. Schubert, C., 1986. Terrazas aluviales en el escudo de Guayana: informe preliminar. Acta Scienti®ca Venezolana 37, 226±228. Singh, J.S., Gupta, S.R., 1977. Plant decomposition and soil respiration in terrestrial ecosystems. Botanical Reviews 43, 449±528. Singh, R.S., Srivastava, S.C., Raghubanshi, A.S., Singh, J.S., Singh, S.P., 1991. Microbial C, N and P in dry tropical savanna: effects of burning and grazing. Journal of Applied Ecology 28, 869±878. Sparling, G.P., Williams, B.L., 1986. Microbial biomass in organic soils: estimation of biomass C, and effect of glucose or cellulose amendments on the amounts of N and P released by fumigation. Soil Biology & Biochemistry 18, 507±513. Srivastava, S.C., Singh, J.S., 1991. Microbial C, N and P in dry tropical forest soils: effects of alternate land-uses and nutrient ¯ux. Soil Biology & Biochemistry 23, 117±124. USDA, 1975. Soil taxonomy; a basic system of soil classi®cation for making and interpreting soilsurveys. Agriculture Handbook No. 436. Soil Survey Staff/USDA, Washington DC (pp. 323±332). Wardle, D.A., Ghani, A., 1995. Why is the strength of relationships between pairs of methods for estimating soil microbial biomass often so variable? Soil Biology & Biochemistry 27, 821±828. Wolters, V., Joergensen, R.G., 1991. Microbial carbon turnover in beech forest soils at different stages of acidi®cation. Soil Biology & Biochemistry 23, 897±902. Yang, J.C., Insam, H., 1991. Microbial biomass and relative contributions of bacteria and fungi in soil beneath tropical rainforest, Hainan Island, China. Journal of Tropical Ecology 7, 385±393.