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: [email protected].
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
<0.0001
0.63
Soil Temperature
Treatment
Month
Treatment × Month
1
11
154
0.85
24.31
0.02
2.93
838.75
0.73
0.11
<0.0001
0.71
Soil Moisture Content
Treatment
Month
Treatment × Month
1
11
154
56.12
340.77
7.14
0.05
15.70
0.33
0.83
<0.0001
0.98
ables are treatments (control versus litter-exclusion)
and months, and dependent variables include soil microbial biomass, soil temperature, and soil moisture
content. We also analyzed the relationships between
soil microbial biomass and plant litterfall, soil temperature and soil moisture using simple linear or exponential regression models. Significance level was set
at alpha = 0.05.
Results
Both plant litterfall and soil microbial biomass
differed among months with pronounced fluctuation
(Figure 1), but litter-exclusion had no overall effect
on soil microbial biomass in the tropical wet forest
(Table 1). There were no interactions between treatments and months. Furthermore, litter-exclusion did
not alter the fluctuation of soil microbial biomass.
Soil microbial biomass fluctuated throughout the oneyear study period with the same magnitude for the
control and litter-exclusion treatments, ranging from
1.08 mg-C/g-soil to 1.71 mg-C/g-soil in the control
plots, and from 1.05 mg-C/g-soil to 1.55 mg-C/g-soil
in the litter-exclusion plots. Microbial biomass peaked
in September 1999 and March 2000 when rainfall
was relatively low (Figure 1). Soil microbial biomass
averaged 1.30 mg-C/g-soil in the control plots and
1.21 mg-C/g-soil in the litter-exclusion plots. Plant
150
Figure 2. An exponential correlation between plant litterfall and
soil microbial biomass of the preceeding one-month in a tropical
wet forest of Puerto Rico.
Figure 1. Fluctuation of soil microbial biomass, plant litterfall, and
rainfall during an annual drying-rewetting cycle between August
1999 and July 2000 in a tropical wet forest of Puerto Rico. Bars
indicate means ± SE.
litterfall also fluctuated throughout the one-year study
period. However, it peaked in October 1999 and April
2000, one month after the peaks in microbial biomass. The October peak was associated with increased
fruitfall and seedfall, whereas the April peak was associated with increased inputs of leaf material. The
lowest value of total litterfall occurred in February
2000. The mean annual litterfall was 1.98 g/m2 /d. The
total annual litter input from August 1999 through July
2000 was 723.8 g/m2 .
Soil microbial biomass did not synchronize with
plant litterfall. Monthly mean values of soil microbial biomass did not linearly or exponentially correlate
with litter input accumulated over the preceeding one-
or two-months for both control and litter-exclusion
treatments. However, there were linear and exponential correlations between the monthly mean values of
soil microbial biomass and the amount of litter input
in the month after the soil samples were collected for
microbial biomass analyses for both treatments (Figure 2). This correlation was not significant for litterfall
of any other months during the one-year cycle.
Soil temperature and moisture content was not affected by the litter-exclusion treatment, but differed
among seasons (Table 1). There were no interactions between treatments and months for both soil
temperature and moisture contents. Mean annual soil
moisture at 0–100 mm depth was 72.2%, ranging from
67.5% in March to 80.6% in January (Figure 3). Mean
annual soil temperature was 22.1 ◦ C, ranging from
20.5 ◦ C in March to 23.7 ◦ C in September. Furthermore, there was no significant correlation between soil
microbial biomass and soil temperature, soil moisture
content, or monthly rainfall for both the control and
litter-exclusion treatments.
151
Figure 3. Monthly variation of soil temperature and moisture
between August 1999 and July 2000 in a tropical wet forest in Puerto
Rico (N = 8, means ± SE).
Discussion
We originally hypothesized a direct correlation of soil
microbial biomass with litter inputs. However, patterns of soil microbial biomass preceeded patterns of
litter input by one month. Furthermore, there was a
lack of influence of plant litter input on soil microbial biomass and on its pattern of monthly variation,
although soil microbial biomass tended to be reduced
in the litter-excluded plots as compared to the control
plots. These results indicated that annual variation in
the aboveground litter input did not drive the large
fluctuation in soil microbial biomass within this tropical wet forest. We therefore rejected our hypothesis.
Jenkinson and Ladd (1981) reported that most soils
contain 30–100 times more dead organic carbon than
live microbial carbon, and suggested that microbial
growth might not be carbon limited. Vance and Chapin
(2001) showed that the highest soil microbial biomass
occurred in unproductive black spruce stand and the
lowest value of soil microbial biomass was from a
productive birch stand in Alaska. Luizão et al. (1992)
found similar values of soil microbial biomass in an
active pasture, a young forest regenerated from a
slashed-burnt site, and an old growth forest in central Amazon with contrasting litter inputs. There was
also no difference in soil microbial biomass between
an abandoned pasture and a mature forest in Puerto
Rico (Liu and Zou, 2002). These studies suggest that
aboveground litter input does not impose an apparent
influence on soil microbial biomass at local scales.
Fluctuation of soil microbial biomass can also be
driven by annual changes in soil water availability.
A negative relationship has been reported between
microbial biomass and soil moisture levels in tropical dry forests of India (Raghubanshi, 1991; Singh
et al., 1989). In contrast, fungal biomass in forest floor
litter was reported to synchronize with the previous
two weeks’ rainfall in this tropical wet forest (Lodge
et al., 1994), showing a positive correlation with water
availability. Furthermore, Wright and Cornejo (1990)
demonstrated that most tree species did not change
patterns of litterfall in the dry season when the forest
was irrigated with sufficient water in Panama, suggesting lack of direct correlation between plant litterfall
and rainfall or soil water levels. Although soil temperature may also influence soil microbial biomass, temperature effects remain unclear across various studies
worldwide (Wardle, 1992). In this study, we found no
correlation between soil microbial biomass and soil
water content, soil temperature, or rainfall, suggesting that annual changes in soil temperature and water
availability did not directly trigger the fluctuation of
microbial biomass in this tropical wet forest. This
lack of correlation could be attributed to the relative
mild weather conditions with narrow range of air temperature (20 ◦ C through 24 ◦ C) and rainfall (mean
minimum monthly rainfall > 200 mm) in this forest
(Scatena, 2001).
However, we detected significant asynchronous
fluctuation where increases in soil microbial biomass
preceeded litterfall by one month. There are two important below-ground processes associated with plant
litterfall. Reduction in plant nutrient uptake and retranslocation of nutrients and carbohydrates from
leaves to stems and roots often occur before trees senesce their leaves. Changes in plant nutrient uptake
or carbon and nutrient retranslocation could trigger
temporal changes in soil microbial biomass. A root
trenching experiment that terminated both plant uptake and root exudate production showed a drastic
decrease in soil microbial activity as indicated by
reduced soil CO2 production (Boone et al., 1998).
Högberg et al. (2001) demonstrated that termination of below-ground carbon supply alone by girdling
152
forest tree trunks (terminating below-ground carbon
input without immediately altering plant uptake) could
drastically reduce soil respiration. Their results indicated that annual variation in soil microbial biomass
might be driven by the fluctuation of root exudate
production in soils. Before leaf and fruit senescence,
trees often retranslocate nutrients and carbohydrates
to stems and roots. Increases in root exudates could
result in elevated microbial growth in soils.
Another mechanism that might explain why the
peak of microbial biomass occurs one month ahead of
the peak for plant litterfall, is through a reduction in
plant nutrient uptake and consequently increased soil
nutrient availability. Plants and soil microbes compete
for nutrients despite having a mutualistic relationship
in which plants provide carbon sources for microbes
and microbes mineralize organic nutrients for plant
use (Harte and Kinzig, 1993; Kaye and Hart, 1997).
This competitive relationship has been demonstrated
experimentally in various ecosystems (e.g., Groffman
et al., 1993; Lipson and Monson, 1998; Lipson et al.,
1999; Schimel et al., 1989). Smolander et al. (1998)
reported that clear-cutting of forest (termination of
plant uptake) caused an immediate increase in soil microbial biomass. Donaldson et al. (1990) found the
extractable NO3 and NH4 in soil of an oak forest were
highest prior to leaffall season. Roy and Singh (1995)
concluded that the temporal variation in soil mineral N
and P was, in part, controlled by plant uptake dynamics in dry tropical forest of India. Microbial biomass
N and P accounted for 4–10% of the total soil N and
9–11% of the total soil P (Raghubanshi et al., 1990).
In this tropical wet forest of Puerto Rico, fungal biomass P alone accounted for 3% to 85% of total P in
the litter layer (Lodge et al., 1994). The high demand
for nutrients by soil microbes may lead to intensive
competition with plants during the growing season.
However, senescing of leaves and fruit can reduce
plant uptake and ease this competitive relationship,
thus stimulating microbial growth. In this study, litterfall peaked in the months of October and April when
fruitfall or leaffall was high, respectively. Reduction
in plant uptake might have occurred in September
and March. This reduction could ease competition for
soil nutrients between plants and microbes and consequently stimulate soil microbial growth, resulting
in asynchronous fluctuation of microbial biomass and
litterfall.
The litterfall in our study consists of leaves,
flowers, fruit, and twigs smaller than 20 mm excluding
large wood. Tree bark was small in quantity and was
not separated out from the miscellaneous category.
Tree bark should be excluded from the litterfall for
analyzing relationships with soil microbial biomass in
forests where they are a significant fraction of litterfall because barkfall is not directly associated with the
processes of plant nutrient uptake or nutrient/carbon
retranslocation.
The lack of correlation between plant litterfall and
soil microbial biomass indicated that annual fluctuation in soil microbial biomass was not driven by
aboveground carbon input as suggested by other studies at the regional scale. The phenomenon of soil
microbial biomass preceeding litterfall by one month
might be explained if microbial growth was either
controlled by the availability of soil nutrients or belowground carbon, both of which could be altered
by the processes of retranslocation of carbohydrate
production and competition for nutrients that are associated with plant litterfall during the annual cycles.
Experimental treatments combining tree girdling, root
trenching, and above-ground litter exclusion can separate the compound influence of nutrient competition,
below-ground carbon input, and above-ground litter
input on soil communities and the associated biogeochemical processes.
Acknowledgements
We thank Maria S. Aponte for field assistance and
Mary J. Sanchez for chemical analyses. We also thank
X. Q. Wang, E. Melendez-Ackerman, J. Thompson,
H. Lugo, and J. Bithon for their help in many ways.
This study was partially supported through an institutional cooperative grant from the International Institute of Tropical Forestry, USDA-Forest Service, and a
grant from the US National Science Foundation (DEB
00805238) to the University of Puerto Rico and the
International Institute of Tropical Forestry.
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