BIOTROPICA 37(3): 397–402 2005
10.1111/j.1744-7429.2005.00052.x
Microbial Biomass, Respiration, and Decomposition of Hura crepitans
L. (Euphorbiaceae) Leaves in a Tropical Stream1
Manuela Abelho2,4 , Claudia Cressa3 , and Manuel A. S. Graça4
2 Departamento
de Ciências Exactas e do Ambiente, Escola Superior Agrária de Coimbra, Bencanta, 3040-316 Coimbra, Portugal
3 Centro
de Biologı́a Celular, Laboratório de Biologı́a Experimental, Universidad Central de Venezuela, Apartado Postal 47114,
Caracas 1041-A, Venezuela
4 IMAR
– Institute of Marine Research, C/O Departamento de Zoologia, Universidade de Coimbra, 3004-517 Coimbra, Portugal
ABSTRACT
The processing of leaves in temperate streams has been the subject of numerous studies but equivalent tropical ecosystems have received little attention. We investigated
leaf breakdown of a tropical tree species (Hura crepitans, Euphorbiaceae), in a tropical stream using leaf bags (0.5 mm mesh) over a period of 24 days. We followed the
loss of mass and the changes in adenosine triphosphate (ATP) concentrations and respiration rates associated with the decomposing leaves. The breakdown rate was
fast (k = −0.0672/d, k d = −0.0031/degree-day), with 81 percent loss of the initial mass within 24 days. This high rate was probably related to the stable and high
water temperature (22◦ C) favoring strong biological activity. Respiration rates increased until day 16 (1.1 mg O 2 /h/g AFDM), but maximum ATP concentrations
were attained at day 9 (725 nmol ATP/g AFDM) when leaf mass remaining was 52 percent. To determine the relative importance of fungi and bacteria during leaf
decomposition, ATP concentrations, and respiration rates were determined in samples treated with antibiotics, after incubation in the stream. The results of the samples
treated with the antifungal or the bacterial antibiotic suggest a higher contribution of the fungal community for total microbial biomass and a higher contribution of
the bacterial community for microbial respiration rates, especially during the later stages of leaf decomposition. However, these results should be analyzed with caution
since both antibacterial and antifungal agents did not totally eliminate microbial activity and biomass.
RESUMEN
La descomposición de hojas en riachuelos de zonas templadas ha sido bien estudiada pero en zonas tropicales se le ha dado poca atención. La descomposición de hojas
de la especie tropical Hura crepitans fue estudiada en un rı́o tropical colocando hojas en bolsas de tela con malla de 0.5 mm por un periodo de 24 dı́as. Se documento
la cantidad de masa pérdida y las fluctuaciónes en las concentraciónes trifosfato de adenina (ATP) y en las tasas respiratorias asociadas con las hojas en descomposición.
La tasa de descomposición fue rápida (k = −0.0672/dı́a, k d = −0.0031/grados-dı́a), con 81por ciento de masa inicial perdida al final de 24 dı́as. La tasa observada
esta probablemente relacionada con la temperatura estable y elevada del agua (22◦ C), favoreciendo una fuerte actividad biológica. Las tasas de respiración aumentaron
hasta el dı́a 16 (1.1 mg O 2 /h/g AFDM), pero la concentración máxima de ATP fue obtenida en el dı́a 9 (725 nmol ATP/g AFDM), cuando la masa restante estaba al
52 por ciento. Para cuantificar la importancia relativa de hongos y bacterias durante la descomposición, las concentraciones de ATP y las tasas de respiración fueron
determinadas en muestras tratadas con antibióticos, después de ser incubadas en lo rı́o. Los resultados individuales de los tratamientos contra las bacterias y contra los
hongos sugieren una mayor contribución de la comunidad de hongos para la biomasa microbiana total y una mayor contribución de la comunidad de bacterias para
las tasas de respiración, principalmente durante las fases más tardı́as de la descomposición. Sin embargo, estos resultados deben ser analizados con cautela ya que los
antibióticos no fueron completamente eficientes para eliminar la actividad y biomasa de los microorganismos.
Key words: ATP; bacteria; fungi; Hura crepitans; leaf decomposition; respiration; tropical stream; Venezuela.
ALLOCHTHONOUS ORGANIC MATTER, such as leaf litter from riparian vegetation, is the most important source of energy in forested
headwater streams (e.g., Fisher & Likens 1973, Abelho 2001). Leaf
litter breakdown is thus a key element of ecosystem function in such
streams (Rowe et al. 1996). Four major mechanisms are responsible
for the decomposition of leaf litter in streams: leaching, microbial
degradation, macroinvertebrate feeding activities, and flow-related
fragmentation (e.g., Boling et al. 1975, Webster & Benfield 1986,
Gessner et al. 1999). Irons et al. (1994) suggested that the relative importance of shredding versus microbial processing increases
at cooler, higher latitudes along the latitudinal thermal gradient.
However, some authors argue that the contribution of macroconsumers, such as decapod crustaceans, has been overlooked in tropical
streams and that these animals may be more important in processing
1 Received
organic matter than are small consumers (Rosemond et al. 1998,
Covich et al. 1999).
The reason for an increased importance of microbes toward
the tropics in litter decomposition is the positive effect of elevated
temperature on biological activity (Benstead 1996, Rosemond et al.
1998, Mathuriau & Chauvet 2002). Fungi, especially aquatic hyphomycetes, are considered the main microbial decomposers of leaf
litter in streams (Bärlocher 1992, Suberkropp 1992, Gessner 1997,
Gessner et al. 1997, Hieber & Gessner 2002). However, some authors argue that bacteria can also play an important role due to
their rapid turnover, especially during later stages of decomposition
(Weyers & Suberkropp 1996, Baldy & Gessner 1997).
Leaf litter decomposition has been the subject of numerous
studies in temperate streams (see review by Abelho 2001), but little is known about the process in the tropics, especially regarding
microbial colonization and activity. The objective of this study was
10 April 2003; revision accepted 15 December 2004.
397
398
Abelho, Cressa, and Graça
to document microbial mediated decomposition of Hura crepitans
leaves in a tropical stream.
METHODS
STUDY SITE.—Fieldwork was conducted in Camurı́ stream, a hardwater stream located 20 km north of Caracas, at the north slope
of the Avila Mountain, North Venezuela (approximately 10◦ 30 N,
66◦ 30 W). At the study site the stream flows through evergreen and
deciduous tree communities that provided year-round shading and
inputs of leaf litter. A riffle area was chosen as the specific site of the
study. The streambed at the study site was 2.0–2.5 m wide and was
composed of bedrock and cobbles with sand.
During the study period, discharge was 0.14 m3 /sec (range =
0.09–0.20 m3 /sec), current velocity at the bags was 31 cm/sec
(range = 22–40 cm/sec), depth at the bags was 26 cm (range = 24–
28 cm), pH was 7.9 (range = 7.7–8.5), conductivity was 109 µS/cm
(range 100–115 µS/cm), dissolved oxygen was 9.5 mg/L (range =
9.3–9.7 mg/L), and mean water temperature was 22◦ C (range =
20–23◦ C).
PREPARATION, COLLECTION AND PROCESSING OF LITTERBAGS.—
Senescent leaves of the deciduous tree Hura crepitans L. (Family
Euphorbiaceae) were collected prior to abscission from trees in
Venezuela. Initial nitrogen and phosphorus content of the leaves
(Graça et al. 2001) was 1.4 percent N and 0.23 percent P. Leaves
were air-dried, and a known amount (3.1 ± 0.1 g) was placed in
0.5 mm mesh-size bags. On 7 March 1997 (during late litterfall period) 35 litterbags were tied to iron rods anchored in the streambed.
The contents of an additional seven bags were oven-dried (60◦ C,
72 h) to calculate a mean humidity factor (oven-dry mass/air-dry
mass). The initial oven-dry mass in the experimental bags was estimated by multiplying initial air-dry mass by the mean humidity
factor (0.91, range 0.89–0.93).
Seven bags were randomly collected after 1, 5, 9, 16, and
24 days, and returned to the laboratory individually in a container
of stream water. The bags were opened and the leaves were gently
washed to remove loosely attached debris. From each bag, five sets
of eight leaf discs (total = 40 discs) were cut with a cork borer
(diameter 14.5 mm). The rest of the leaf material in each bag was
oven-dried (60◦ C, 72 h) to determine dry mass. One set of eight
leaf discs (reference) was oven-dried and ashed (500◦ C, 5 h) to
determine ash-free dry mass (AFDM). The other sets were used to
determine respiration rates and ATP concentrations associated with
the decomposing leaf litter (see below). The dry mass remaining
on each sampling date was calculated as the dry mass of the bulk
material remaining plus five times the dry mass of the eight reference
leaf discs.
RESPIRATION RATES.—Respiration rates were assessed at stream temperature (22◦ C) using a flow-through system described by Wrona
and Davies (1984) and Abelho and Graça (2001). Each set of eight
leaf discs was placed in glass chambers (volume 8 mL) and supplied
with a continuous and unidirectional flow (Manostat Sarah peristaltic pump, position 40) of 100 percent oxygenated and filtered
(Sartorius cellulose nitrate 0.45 µm filters) stream water. Seven
additional chambers without leaf discs (blanks) were used as controls. The mean flow in the chambers was 7.0 mL/h (range =
4.8–9.6 mL/h). After total replacement of the chambers’ volume
(1–2 h), dissolved oxygen was measured by collecting the water
flowing through the chambers (1 mL syringe) and injecting it into
a 100-µL chamber adapted to an oxygen electrode (Strathkelvin
Instruments, Glasgow, UK, model 781). Two to three replicate
measurements were made on each chamber with a time interval of
approximately 1 h.
To assess respiration rates, the difference in oxygen concentration (mg O 2 /L) between the water column (blanks) and the samples
was calculated and multiplied by the flow (L/h) within each chamber. Final values were calculated on the basis of AFDM of the eight
reference leaf discs (mg O 2 /h/g AFDM).
ATP CONCENTRATIONS.—After measuring the respiration rates,
the same sets of eight leaf discs were homogenized (Omni
Mixer Homogenizer, position 6, 60 sec) with 5 mL 1.2 N
H 2 SO 4 containing 8 g/L oxalic acid, and 5 mL 0.05 M HEPES
buffer (N-[2-Hydroxyethyl] piperazine-N -[2-ethanesulfonic acid]:
C 8 H 17 N 2 O 4 SNa), centrifuged (refrigerated centrifuge, 10,000
rpm, 20 min), neutralized (NH 4 OH), and frozen at −20◦ C
(Suberkropp et al. 1983).
ATP was quantified with a luminometer, using the firefly bioluminescence method (Karl 1980). Absolute quantitative determinations of the amount of extracted ATP were made by measuring
relative changes in peak height before and after the addition of internal standards (Holm-Hansen & Karl 1978). At least two readings
were made on each sample. Final values were calculated on the basis
of AFDM of the eight reference leaf discs (nmol ATP/g AFDM).
The values presented have been corrected for extraction efficiency
in each session. Extraction efficiency in each session was determined
by adding a known amount of ATP (500 nmol) to an extra sample of
eight noncolonized, air-dried leaf discs. Mean extraction efficiency
was 65 percent (range = 22–73%).
RELATIVE IMPORTANCE OF FUNGI AND BACTERIA.—After cutting the
discs, each of the four sets of eight leaf discs was placed in a 100-mL
flask containing filtered stream water (Sartorius cellulose nitrate
0.45 µm filters) and one of the following treatments: (1) antibacterial (50 mL/L penicillin-streptomycin solution; Sigma N0906),
(2) antifungal (50 mL/L nystatin suspension; Sigma N1638),
(3) antibacterial + antifungal (50 mL/L penicillin-streptomycin
solution + 50 mL/L nystatin suspension), and (4) control (no antibiotics added). The flasks were incubated for 36 h in an orbital
shaker (70 rpm) at stream temperature (22◦ C) and then the leaf
discs were used to determine microbial respiration and ATP concentration associated with the leaves (see above).
DATA ANALYSIS.—Leaf mass loss was expressed as a percentage of
initial dry mass remaining. A negative exponential model was fitted
by linear regression on logarithmically (ln) transformed data with
the initial leaf mass (intercept) fixed at 100 percent, to determine
breakdown rate k. Temperature-specific breakdown rate (k d ) was
Decomposition of Hura crepitans Leaves in a Tropical Stream
399
calculated by using cumulative degree-days as the independent variable. The degree-days elapsed were determined by multiplying the
temperature measured on a sampling date by the days elapsed since
the previous reading. Respiration rates and ATP concentrations in
the four treatments over the experimental period were tested for
normality (those not normally distributed were log transformed)
and compared using two-way ANOVA and Tukey’s HSD test
(Zar 1996). Statistical analyses were conducted using the software
STATISTICA 6.0.
RESULTS
BREAKDOWN RATE, MICROBIAL BIOMASS, AND ACTIVITY.—Leaves lost
19 percent of initial dry mass during the first 24 h in the stream
(Fig. 1). Mass loss data fitted well to the breakdown model (F >
1141, df = 41, P < 0.0001). Breakdown rate of Hura crepitans leaves
was rapid (k = −0.0672/d ± 0.0020 SE, k d = −0.0031/degreed ± 0.0001 SE); the bags lost 81 percent of their initial dry mass
within 24 days. Because the litterbags were vandalized, no material
was available for collection on day 31. The leaf material remaining
on day 24 was composed of very small fragments, insufficient to
determine ATP concentrations and respiration rates.
At the beginning of the study, the leaves contained low amounts
of ATP (5.8 ± 1.7 nmol ATP/g AFDM), but ATP content increased
rapidly thereafter, with peak values of 725.1±117.5 nmol ATP/g
AFDM at 9 days, when the remaining dry mass was 52 percent
(Fig. 2). Respiration rates increased rapidly and continuously
throughout the experiment (Fig. 2), attaining maximum values on
day 16 (1.07 ± 0.09 mg O 2 /h/g AFDM).
FIGURE 2. Changes in respiration rates and ATP concentrations associated with decomposing leaves of Hura crepitans in the tropical stream Camurı́
(mean ± 1 SE, N = 7).
the treatment containing both antibacterial and antifungal agents
(Fig. 3), although the values were generally significantly lower
than in the other treatments (Table 1). ATP concentrations were
higher in the antibacterial treatment than in antifungal treatment
(Fig. 3), suggesting that the fungal community dominated microbial biomass associated with leaf litter. Respiration rates were higher
in the antibacterial than in the antifungal treatment during the first
9 days of decomposition; after a maximum at day 5, respiration
rates steadily decreased in the antibacterial treatment, whereas these
rates increased in the antifungal treatment until the end of the
experiment (Fig. 3).
RELATIVE IMPORTANCE OF FUNGI AND BACTERIA.—Both microbial
respiration plus measurable concentrations of ATP were found in
DISCUSSION
LEAF
DECOMPOSITION,
ATP CONCENTRATIONS, AND RESPIRATION
leaves of Hura crepitans decomposed very rapidly in
stream Camurı́ (k = −0.0672/d) showing one of the highest rates
reported in the literature (e.g., Abelho 2001), although most of
the studies allowed invertebrates to feed on the leaves (Padgett
1976, Verghese & Furtado 1987, Benstead 1996, Mathuriau &
Chauvet 2002, Pamrong et al. 2002). Our results were consistent
with other observations of fast breakdown in tropical streams (Irons
et al. 1994, Rosemond et al. 1998).
The high and stable water temperature (22◦ C), together with
the hardwater characteristics of our stream, probably played a major role in controlling microbial activity associated with the leaves.
When calculated as a temperature-specific processing rate, the breakdown rate (k d = −0.0031/degree-day) was still high (Cummins
et al. 1989) and similar or higher than that reported for other leaf
species in mid-latitude or even tropical streams (Irons et al. 1994,
Mathuriau & Chauvet 2002).
Microbial biomass and activity have rarely been assessed in
leaves decomposing in tropical streams. In our study, the leaf litter
was rapidly colonized by microorganisms, and attained higher ATP
RATES.—The
FIGURE 1. Dry mass remaining of Hura crepitans leaves decomposing in the
tropical stream Camurı́ (mean ± 1 SE, N = 7).
400
Abelho, Cressa, and Graça
TABLE 1. Results of multiple comparisons (Tukey test HSD) after two-way
ANOVA (time vs. treatment). Time had a significant effect ( F > 20.405, df = 4, P < 0.0001), and there was a significant interaction between time and treatment in all tests
( F > 3.481, df = 12, P < 0.001). Treatments with the same letter are significantly different (P < 0.05). B = antibacterial treatment,
F = antifungal treatment, BF = antibacterial and antifungal treatment, C = control.
FIGURE 3. Changes in (a) respiration rates and (b) ATP concentrations associated with decomposing leaves of Hura crepitans treated with both (BF) and
one of the antifungal or the antibacterial antibiotics (mean ± 1 SE, N = 7).
concentrations (725 nmol/g AFDM) than in temperate streams,
where ATP concentrations reached a maximum of 330–496 nmol/g
AFDM in 15–115 days (Meyer & Johnson 1983, Suberkropp &
Chauvet 1995). This result suggests that microbial processing is
an important component of litter decomposition in this tropical
stream.
Fungal biomass has been reported to account for 88–100 percent of total microbial biomass associated with several leaf species
decomposing in temperate streams (e.g., Baldy et al. 1995, Weyers
& Suberkropp 1996, Baldy & Gessner 1997). To allow comparisons with other studies, we assumed that this was also the case
in this tropical stream and converted ATP concentrations to microbial dry mass using the conversion value 1.75 mg (3.18 nmol)
ATP/g fungal dry mass (Suberkropp et al. 1993). Fungal biomass
estimated in this way accounted for a maximum of 23 percent
2-way ANOVA
Tukey test
Respiration rates
(mg O 2 /L/g/AFDM)
F = 17.858, df = 3,
P < 0.0001
Ca > Fb > Bac > BFabc
ATP concentrations
(nmol ATP/g/AFDM)
F = 10.857, df = 3,
P < 0.0001
Ba > Cab > Fa > BFab
of total detrital dry mass on day 9. The values were higher than
those reported in the literature for temperate (5–18%; Gessner &
Chauvet 1994, Suberkropp 1995, Paul & Meyer 1996) or even
tropical streams (9.6%; Mathuriau & Chauvet 2002). Therefore,
either fungal biomass was extremely high in the studied stream,
or other microorganisms besides aquatic hyphomycetes were also
important during decomposition. The maximum respiration rates
associated with the decomposing leaves (1.07 mg O 2 /h/g AFDM)
were in the range of those reported by Suberkropp (1991) for softwater (0.4 mg O 2 /h/g) and hardwater (1.3 mg O 2 /h/g) streams
of North America. Since respiration is an indicator of carbon use
by decomposers, we suggest that a difference between temperate
and tropical streams is the velocity at which microbes colonize and
decompose leaf material.
The chemical characteristics of the leaves could have played a
major role in controlling microbial colonization and the observed
high breakdown rates. Leaching seems to be enhanced in tropical
streams (Covich 1988). In our study the initial mass loss, generally
attributed to leaching of soluble compounds, was high (19% in
the first day) and in the range of values obtained in other studies
(Mathuriau & Chauvet 2002). Leaching, together with the fast colonization by microorganisms, probably a result of a relatively high
initial nutrient content and a low content of condensed tannins,
could have interacted, resulting in the high mass loss observed in
the experiment. According to Stout (1989), most of the tropical
leaves with low condensed tannins have rapid (k = −0.0178/d ±
0.0045 SD) or very fast (k = −0.1182/d ± 0.0050 SD) breakdown
rates. Our values are intermediate between these two, suggesting
that Hura crepitans has a low condensed tannin content. Mathuriau
and Chauvet (2002) obtained breakdown rates similar to ours using
tropical leaf species with low tannin contents (1.13%).
RELATIVE IMPORTANC OF FUNGI AND BACTERIA.—The temporal dynamics of ATP concentrations and respiration rates were similar until day 9. From that point on, ATP concentrations decreased while
respiration rates continued to increase suggesting that a change had
occurred in the microbial colonization of leaf litter. This change
could be due to a replacement of the pioneer fungi, which are
Decomposition of Hura crepitans Leaves in a Tropical Stream
generally the first leaf-colonizers, by bacteria, which would account
for lower biomass but higher activity (Baldy et al. 2002), as suggested
by the continued increase in respiration rates.
This pattern is also consistent with the results obtained with the
antibiotics. The residual activity and biomass associated with leaves
treated with both antifungal and antibacterial agents showed that
antibiotics were not efficient enough to eliminate biotic activity.
However, despite the residual activity, samples treated with the
antifungal or antibacterial antibiotics differed, either in the amounts
or in the temporal dynamics: antifungal agents were more effective
in reducing microbial biomass and respiration until day 9, whereas
antibacterial agents were more efficient from day 9 onward. These
results suggest that fungi were the main microorganisms colonizing
leaf litter in the early stages, and, as in temperate streams, they tend
to be replaced by bacteria in later stages (Baldy & Gessner 1997).
However, bacterial biomass associated with decomposing leaves may
be relatively more abundant in tropical than in temperate streams.
In conclusion, our results suggest that microbial-mediated leaf
breakdown in our tropical stream was high in comparison with results from temperate streams. Microorganisms, as shown by the high
ATP concentrations associated with the leaves, developed abundantly and rapidly, supporting previous findings regarding the dominance of microorganisms on leaf decomposition in tropical streams
(Mathuriau & Chauvet 2002). The relative importance of bacteria
and fungi during leaf decomposition seems to follow the patterns
observed in temperate streams, with fungi dominating the early
stages of decomposition and bacteria dominating when leaf litter is
already fragmented and softened.
ACKNOWLEDGMENTS
This work was financed by the European Union (ISC-937084VE)
and by Fundação para a Ciência e a Tecnologia (FCT) through a
program grant (PBIC/C/BIA/2056/95) and through a scholarship
to Manuela Abelho (PRAXIS XXI/BD/2952/94). We thank Centro
de Neurociências (CNC) of Universidade de Coimbra (Portugal),
through Dr. Martinho do Rosário, and Laboratório de Biologı́a
Experimental of Universidad Central de Venezuela through Dr.
Alexis Mendonza and Dr. Blas Dorta, for laboratory facilities. We
especially acknowledge the precious help of Ângela Ribeiro in the
work with the luminometer and Dr. Keller Suberkropp for valuable
comments on an earlier version of the manuscript.
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