Plant and Soil 260: 147–154, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.
147
Asynchronous fluctuation of soil microbial biomass and plant litterfall in a tropical wet forest H.H. Ruan1,3 , X.M. Zou2,3,5 , F.N. Scatena4 & J.K. Zimmerman3 1 Faculty
of Forest Resources and the Environment, Nanjing Forestry University, Nanjing, China. 2 Xishuangbanna Tropical Botanical Garden, The Chinese Academy of Sciences, 88 Xuefu Road, Kunming, Yunnan, 650223, China. 3 Institute for Tropical Ecosystem Studies, University of Puerto Rico, P.O. Box 23341, San Juan, PR 00931-3341, USA. 4 Department of Earth and Environmental Science, University of Pennsylvania, 240 South 33rd Street, Philadelphia, PA 19104-6316, USA. 5 Corresponding author∗
Received 2 July 2003. Accepted in revised form 15 October 2003
Key words: annual fluctuation, drying-rewetting cycles, litterfall, microbial biomass, plant-microbial competition, tropical wet forest
Abstract Carbon availability often controls soil microbial growth and there is evidence that at regional scales soil microbial biomass is positively correlated with aboveground forest litter input. We examined the influence of plant litterfall on annual variation of soil microbial biomass in control and litter-excluded plots in a tropical wet forest of Puerto Rico. We also measured soil moisture, soil temperature, and plant litterfall in these treatment plots. Aboveground plant litter input had no effect on soil microbial biomass or on its pattern of fluctuation. Monthly changes in soil microbial biomass were not synchronized with aboveground litter inputs, but rather preceeded litterfall by one month. Soil microbial biomass did not correlate with soil temperature, moisture, or rainfall. Our results suggest that changes in soil microbial biomass are not directly regulated by soil temperature, moisture, or aboveground litter input at local scales within a tropical wet forest, and there were asynchronous fluctuation between soil microbial biomass and plant litterfall. Potential mechanisms for this asynchronous fluctuation include soil microbial biomass regulation by competition for soil nutrients between microorganisms and plants, and regulation by below-ground carbon inputs associated with the annual solar and drying-rewetting cycles in tropical wet forests. Abbreviations: Annual fluctuation of soil microbial biomass and litterfall Introduction Soil microbial biomass is the most active component of soil organic carbon that regulates biogeochemical processes in terrestrial ecosystems (Paul and Clark, 1996). Although total soil microbial biomass carbon worldwide is approximately 1.4% of the world’s total soil organic carbon, its turnover represents a significant contribution to the global carbon cycle (Wardle, 1992). Numerous studies on microbial biomass have been conducted in temperate ecosystems (e.g., Korsaeth et al., 2001; Maxwell and Coleman, 1995; Zak et al., 1994; Vance and Chapin, 2001). However, only ∗ E-mail:
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a few studies on soil microbial biomass have been performed in tropical forests. Our understanding of the fluctuation of soil microbial biomass in the vast area of tropical forest remains very poor. Asynchronous uptake of nutrients by plants and soil microbes has been recognized as a mechanism for retaining nutrients and maintaining ecosystem productivity in temperate deciduous forests with strong temperature seasonality and in tropical forests with drying-rewetting cycles. In temperate deciduous forests, microbial biomass N increases during winter when plant uptake is ceased or reduced, preventing nutrient loss through snow-water or rain leaching when Spring arrives (Muller and Bormann, 1976; Groffman
148 et al., 1993; Zak et al., 1990). In tropical dry forest, microbial biomass and microbial N and P contents increase during the dry season, whereas microbes release N and P at the beginning of the wet season when plant growth and demand for nutrients are high (Singh et al., 1989). The immobilization of soil N and P into microbial biomass during dry season when plant uptake is low prevents soil nutrient accumulation to high levels that are subject to nutrient loss through gaseous emission or water leaching when wet season arrives. However, the mechanisms that govern the annual changes in microbial biomass are not clear. Available soil carbon has been commonly recognized as the driving factor regulating soil microbial biomass growth (Wardle, 1992), although other factors such as temperature, soil moisture, soil physicalchemical conditions, and food web interactions may also influence soil microbial biomass (Coleman and Crossley, 1996; Hassink, 1994; McGill et al., 1986; Van Veen et al., 1984). Gray and Williams (1971) and Zak et al. (1994) suggested that soil microbial biomass is controlled by plant litter production at regional scale. Smith and Paul (1990) further concluded that the maintenance requirements for microbial biomass equal the total carbon input under steady- or near steady-state conditions in terrestrial ecosystems. Plant litter production is often associated with annual solar and drying-rewetting cycles in tropical ecosystems, typically with high litterfall in the dry season and low litterfall in the wet season (Murphy and Lugo, 1986; Wright and Cornejo, 1990). Seasonal variation in soil microbial biomass has also been observed in tropical forests. However, the patterns of seasonal variation of soil microbial biomass are inconsistent. Singh et al. (1989) and Raghubanshi (1991) reported that microbial biomass was the highest in the dry season and lowest in the rainy season in monsoon forests of India. In contrast, Basu et al. (1991) reported that soil microbial biomass was the highest in rainy season and lowest in dry season in Indian deciduous forests. In rain forests of Brazil and China, microbial biomass in the rainy season was significantly higher than in the dry season (Luizão et al., 1998; Yang and Insam, 1991). These studies did not show clear evidence of the mechanisms that drive the annual variation in soil microbial biomass in tropical wet forests. The purpose of this study was to examine plant litter regulation of the annual variation of soil microbial biomass at local scales in tropical wet forests. We hypothesized that changes of soil microbial biomass synchronize with patterns of plant litter input
in tropical wet forests. We carried out this study in a tropical wet forest of Puerto Rico where annual variation in temperature and rainfall was slight, but still with apparent dry seasons between January and April and in the summer months (Scatena, 2001). We estimated soil microbial biomass each month in control and litter-excluded plots located along a catena ranging from ridge top to stream bank, representing the widest soil moisture variation in this forest. We predicted that annual variation in soil microbial biomass would synchronize with plant litterfall in the control plots, and this synchrony would disappear in the litter-exclusion plots.
Materials and method Experimental design, field sampling, and laboratory processing This study was conducted in the Luquillo Experimental Forest (LEF), a tropical Long-Term Ecological Research (LTER) site in northeast Puerto Rico (18◦20 N, 65◦ 49 W). The research area was classified as lower montane wet forest (Ewel and Whitmore, 1973; Odum and Pigeon, 1970), and named after the dominant tabonuco tree (Dacryodes excelsa Vahl) which often comprises as much as 35% of the forest basal area at the breast height (Zou et al., 1995). Elevation of the tabonuco forest ranges from 300 to 600 m above sea level. Mean monthly temperature varies from 20.8 to 24.4 ◦ C and mean annual precipitation is 3456 mm (Brown et al., 1983). Although rainfall occurs throughout the year, average rainfall is the lowest between January and April, but with no less than 200 mm per month. There is often another irregular dry period between July and September during summer (Scatena, 2001). Soils of the area are a complex of well- to poorly-drained Ultisols and Oxisols with pH values of 5.2 (water) and bulk density (0–0.1 m) of 790 kg/m3 (Soil Survey Staff, 1995). The main tree species include Dacryodes excelsa Vahl, Buchenavia capitata (Vahl) Eichl, Homalium racemosum Jacq, Guarea guidonia (L.) Sleumer, Sloanea berteriana Choisy, Prestoea montana (Graham) Nicholson, Inga laurina (Sw.) Willd, and Byrsonima spicata (Cav.) HBK (Thompson et al., 2002; Zou et al., 1995). We employed a randomized block design to carry out this study with eight blocks that were chosen along a catena from riparian to upslope and ridge area in the forest. Two 2 × 2 m plots were established within each
149 block. One plot was randomly selected to be the litterexclusion treatment and the other as control. A tent was constructed about 1.5 m above ground with PVC tubes and covered with 1.0 mm mesh netting for the litter-exclusion plot. Forest floor mass (dead organic materials above minerals soil) was removed in May 1999, the beginning of the experiment. Plant litterfall was collected monthly on the same day when soil samples for microbial biomass analyses were collected. Litterfall was collected from tent roofs (4 m2 ) over the litter-exclusion plots from August 1999 to August 2000. All litter samples were oven-dried at 50 ◦ C for two weeks, and weighed. In this study, wood greater than 20 mm in diameter and palm leaves were not included in the litter weight because they contributed a small fraction to the total litterfall and there was large spatial variation. Soil samples were collected monthly on the 6th to 10th day of each month from August 1999 to July 2000. Six soil cores (18.9 mm in diameter) from each plot were randomly collected to a depth of 100 mm and bulked together to form a composite sample. The soil was not sieved, but was homogenized thoroughly by hand kneading of soil sample bags. Small rocks, roots, macro-fauna, and other dead debris were removed carefully by hand. Each soil sample was then weighed for soil bulk density determination. A subsample of 10 g of soil was oven-dried at 105 ◦ C for 24 h for determining soil moisture. Rainfall data was obtained from a weather station located at the El Verde Field Station within 1 km distance from our study plots. Soil temperature was measured to the depth of 0.1 m with a digital soil thermometer in each plot when soil samples were collected monthly. Soil microbial biomass was measured using a modified chloroform-fumigation-incubation procedure (Jenkison and Powlson, 1976; Liu and Zou, 2002) monthly from August 1999 to July 2000. Microbial biomass was calculated as (Jenkinson and Powlson, 1976): Microbial biomass B = F/K, where B = soil biomass carbon, mg-C/kg soil, F = C-CO2 evolved by fumigated soil, less that evolved by unfumigated soil incubated for the same time under the same conditions, K = 0.45, the fraction of the biomass C mineralization to CO2 following the fumigation. Statistical analyses We employed the repeated-measurement two-way ANOVA to analyze for treatment effects and monthly variations (SAS, 1990). Independent vari-
Table 1. Repeated-measures ANOVA statistics for soil microbial biomass, soil temperature, and soil moisture content in a tropical wet forest of Puerto Rico. Independent variables are treatment (control versus litter-exclusion) and month (August 1999–July 2000) Source
DF
MS
F
P
Microbial Biomass Treatment Month Treatment × Month
1 11 154
0.33 0.37 0.03
0.68 10.54 0.80
0.42
