Tropical Forest Litter Decomposition under Seasonal Drought: Nutrient Release, Fungi and Bacteria

Nordic Society Oikos

Tropical Forest Litter Decomposition under Seasonal Drought: Nutrient Release, Fungi andBacteriaAuthor(s): Fernando H. Cornejo, Amanda Varela and S. Joseph WrightSource: Oikos, Vol. 70, Fasc. 2 (Jun., 1994), pp. 183-190Published by: Wiley on behalf of Nordic Society OikosStable URL: http://www.jstor.org/stable/3545629 .

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OIKOS 70: 183-190. Copenhagen 1994

Tropical forest litter decomposition under seasonal drought: nutrient release, fungi and bacteria

Fernando H. Cornejo, Amanda Varela and S. Joseph Wright

Cornejo, F. H., Varela, A. and Wright, S. J. 1994. Tropical forest litter decomposition under seasonal drought: nutrient release, fungi and bacteria. - Oikos 70: 183-190.

Irrigation was used to study the consequences of seasonal drought for nutrient release and bacterial and fungal numbers during dry season litter decomposition in tropical forest on Barro Colorado Island, Panama. Litter bags containing a single species of leaves were placed beneath nonspecific trees at the onset of the dry season in December 1987 and collected at one-month intervals until the onset of the wet season in May 1988. Serial dilutions were used to quantify densities of fungi and bacteria. Nutrient concentrations in recalcitrant litter fractions showed rapid declines in the first month of exposure (K, P) followed by bioaccumulation (N) or no significant changes over the next four months (P. K, Mg and most Ca). Irrigation depressed K concentrations and enhanced N and Mg concentrations possibly as a consequence of leaching and bioaccumulation, respectively. Irrigation also depressed fungal densities at the community level and for three of eight species that were analysed separately. Densities of three of the remaining species of fungi varied significantly among litter substrate species. Bacterial densities were enhanced by irrigation after one month of exposure but were depressed after five months which may reflect reduced litter substrate quality.

F H. Cornejo, Casilla 11, Lima 8, Peru. -A. Varela, Transversan 29 #101 A-26, Santa Fe de Bogota, Colombia. - S. J. Wright, Smithsonian Tropical Research Inst., Apdo 2072, Balboa, Panama.

Each year 7 to 14 Mg ha-' of litter falls to the ground in tropical forests (Vitousek 1984). The decomposition of this litter is critical to nutrient cycles (Cuevas and Medina 1988, Jordan 1989). Decomposition rates are rapid in tropical forests characterized by high, constant temper- atures and high annual rainfall (Olson 1963). However, seasonal drought limits decomposition rates in many tropical forests (Richards 1952). We explore the consequences of seasonal changes in moisture availability for litter decomposition in tropical moist forest on Barro Colorado Island (BCI), Panama.

Water affects decomposition directly through leaching and indirectly through effects on microbial decomposers. Alternate wet and dry cycles may stimulate microbial activity (Alexander 1977, Valencia 1983), and drought

may change the composition of the microbial community with fungi being more tolerant of dry conditions than bacteria (Griffin 1972, Hendrix et al. 1986). In addition, microbial activity varies with the quality and quantity of organic matter (Alexander 1977, Cuevas and Medina 1988).

We manipulated soil water during the dry season with irrigation to examine effects on decomposition rates, nutrient release, fungi and bacteria. Specific predictions were that irrigation would stimulate decomposition rates, nutrient release and bacterial numbers during the dry season.

Accepted 14 December 1993

Copyright (C) OIKOS 1994 ISSN 0030-1299 Printed in Denmark - all rights reserved

OIKOS 70:2 (1994) 183



Study site The vegetation of Barro Colorado Island (909'N, 79051'W) is classified as Tropical Moist Forest in the Holdridge System (Holdridge and Budowski 1956). Mean temperature is 260C and mean monthly temper- atures vary by just 1VC through the year. Annual rainfall averages 2600 mm with two strong seasons. The dry season usually begins in December and ends in April, and median rainfall between 1 January and 31 March is just 84 mm (Windsor 1990). Leaf litter fall peaks early in the dry season in December and January, remains high through April and falls by 50% to low wet season levels from May to November (Haines and Foster 1977, Leigh and Smythe 1978, Wright and Comejo 1990a). Litter decomposition is slow in the dry season, and standing litter on the forest floor builds to its annual peak in April (Swift et al. 1979). In the wet season decomposition is more rapid than accumulation, and the mineral soil is largely exposed by October and November.

Methods Decomposition was studied in irrigated and control plots. Two 2.25-ha plots received irrigation during the dry season, while two adjacent 2.25-ha plots served as controls. Irrigation maintained mean soil water potentials at 25- and 45-cm depths above -0.04 MPa while mean soil water potentials in control plots fell below -1.0 MPa each dry season (Wright 1991). About 675 Mg of water was added to each irrigated plot each week during the dry season. Water was drawn from Gatun Lake. BCI rain and Gatun Lake water have similar pH. Gatun Lake is oli- gotrophic, and nutrient concentrations are exceptionally low (Gonzalez et al. 1975; R. Stallard, unpubl.). Irriga- tion added just 0.67 and 0.13 kg ha-' yr-l of Kjeldahl N and total P, respectively (estimates based on mean nutrient concentrations for lake water from the Barro Col- orado region [Gonzalez et al. 1975] which were similar to concentrations measured in 1988 [R. Stallard, unpubl.]). Other nutrient concentrations were below detection limits. Wright and Cornejo (1990a, b) describe further details of the irrigation treatment.

Freshly fallen litter was collected from beneath trees of five species, weighed without drying and returned imme- diately to the forest in litter bags between 21 and 31 December 1987. Each litter bag received the equivalent of 10-20 g of dried litter of a single species (dry mass was estimated from fresh mass and the moisture content of fresh litter). Litter bags were made of 1.2 mm mesh fiberglass screen and measured 45 by 22 cm. Freshly fallen leaves were used because many of the primary decomposers of dead leaf tissue colonize the leaf before abscission (Fell and Newell 1981, Macauley and Waid 1981). Freshly fallen leaves were recognized by turgent and watery abscission zones.

A total of 300 litter bags was used. Five bags were located randomly on the soil surface beneath the crowns of three individuals of each of the five tree species in each plot. The species of litter and tree were always the same because the area beneath a tree's crown is invariably dominated by its own litter on BCI (SJW, unpubl.). The five tree species were: Anacardium excelsum Bertero & Balb. (Anacardiaceae), Hyeronima laxiflora Tul. Mull (Euphorbiaceae), Prioria copaifera Griseb (Legumino- sae), Quararibea asterolepis Pitt. (Bombacaceae) and Tetragastris panamensis Engler (Burseraceae). Tree species will be referred to by genus only.

A randomly chosen litter bag was collected from each tree in the final week of January, February, March, April and May (giving six replicate litter bags for each combination of tree species, treatment and month). The litter bags were washed with sterile distilled water to remove soil particles and air dried for 2 h. Litter bags were then opened and all foreign material (mostly fine roots) was removed. A fresh sample of 1.5 to 3.0 g was set aside for microbial analyses. The remaining leaves were weighed and oven dried at 60'C for 48 h.

Microbiology The serial dilution technique was used to study litter bacteria and fungi (Wollum 1982). Each month litter samples were pooled by species and plot. Samples were processed under sterile conditions using flamed instru- ments in a disinfected ultraviolet box. Leaves were first rinsed for one min with a stream of sterile distilled water to eliminate surface contaminants (e.g., spores). Fresh litter equivalent to 1 g dry mass was then macerated with a sterilized pestel and mortar. The macerate was mixed by hand for 30 s with 99 ml of sterile distilled water (dilution -2). Nine ml of sterile distilled water was added to 1 ml of the previous dilution for three additional serial dilutions (dilutions -3 through -5).

A 1-ml aliquot of the appropriate dilution was then added to 18 ml of molten medium and swirled. Each liter of bacterial medium included 5 g of Priptona, 2.5 g of yeast extract, 1 g of dextrose, 15 g of agar and 0.5 g of Nystatin. Each liter of fungal medium included 5 g of hydrolyzed soya, 10 g of dextrose, 1 g of KH2PO4, 0.5 g of MgSO4, 0.05 g of Rose Bengal, 1 g of ampicillin and 15 g of agar. Each month two replicate Petri dishes were prepared for dilutions -4 and -5 for each medium and for each combination of tree species and plot (for a total of 160 Petri dishes each month). Incubations took 3 d (at 370C) for bacteria and 7 d (at 250C) for fungi, after which numbers of colony-forming units (CFUs) were counted. Since we used only one nutrient medium and one set of incubation conditions each for bacteria and fungi, we do not expect to have found all microorganisms.

Fungal colonies were identified in two steps. First, colony morphology was used to identify each fungal CFU to morphospecies for each month except May. The

184 OIKOS 70:2 (1994)



150

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Dec 1987 and 31 May 1988. Data are grouped by week.

morphospecies were then isolated on potato dextrose agar, and microscopic characters were used for further identification. It was possible to identify most morphospecies to genus and a few to species.

Chemical analyses Chemical analyses were performed in the Soil Laboratory of the Universidad Nacional Agraria "'La Molinla" in Lima, Peru. Nitrogen was determined by the Micro-Kjel- dahl method. Phosphorus, potassium, calcium and magnesium were extracted in HCl. Phosphorus concentra-

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Fig. 2. Proportion of leaf mass remaining and nitrogen eoncen- tration (mg ga dry mass) for each litter species. Solid lines represent irrigated plots and dashed lines control plots. Error bars represent one standard error and are presented for one treatment for clarity unless one standard error was smaller than the plotting symbol. Sample size is six for leaf mass and three for nitrogen concentration for each combination of treatment month and litter species.

tions were determined by the ammonium molybdate method, using 1-2-4 amino-naphtol sulphonic for reduc- tion. Potassium determinations were made by flame pho- tometry. Calcium and magnesium were determined by the EDTA (Versenat) method.

Statistics Three-way analyses of variance were performed where the fixed main effects were litter species, month and treatment (irrigated and control). Analyses were performed for concentrations of N, P, K, Ca and Mg (mg g-' dry litter), the arcsine square root transformation of the proportion of leaf mass remaining, and the logarithm of bacterial and fungal CFUs g'l dry litter. Transformations stabilized variances. Eight analyses were performed and each analysis involved seven tests (3 main effects and 4 interactions). The Bonferonni procedure was used to in- sure against Type I statistical error and the adjusted 0.05 significance level was 0.0009 [= 0.05/(8 x 7)]. Identical ANOVAs were performed for the eight most frequent fungal species using the same adjusted significance level.

An analysis of covariance was performed to examine effects of treatment, litter species and remaining litter mass for community-level bacterial and fungal numbers (CFUs g-' dry litter). For this analysis, treatment and litter species were again fixed main effects, and the proportion of litter mass remaining was a covariate. Two analyses were performed, each analysis involved seven tests, and the adjusted Bonferonni significance level was 0.0036 [= 0.051(2 x 7)]. The transformations used for the three-way ANOVA again stabilized variances.

Results The 1987-88 dry season was relatively mild. A heavy rain in the final week of February and heavy rains begin- ning in the second week of May wet forest floor litter (Fig. 1).

Rates of decomposition and nutrient concentrations Litter mass disappeared much more quickly in irrigated plots than in control plots, and despite significant interactions, there were also clear differences among litter species (Fig. 2, Table 1). Decomposition rates varied with specific leaf area (SLA) and initial N concentrations in freshly fallen litter. The ranges of SLA and initial nutrient concentrations of the five species (Table 2) were similar to ranges reported for several tropical forests (Brassell et al. 1980, Cuevas and Medina 1988, Jordan 1989). Hyero- nima and Quararibea with high values of SLA and N had the highest mass loss, while Prioria and Tetragastris with

OIKOS 70:2 (1994) 185



Table 1. Analyses of variance for litter mass, nutrient concentrations and colony-forming units (CFUs) g-l dry litter for bacteria and fungi.-F-ratios and error mean squares (final row) are presented. Arcsine square root and logarithmic transformations stabilized variances for the proportion of leaf mass remaining and CFUs g' dry litter for bacteria and fungi, respectively. Nutrient concentrations (mg g'l) were not transformed.

Source DF Mass N P K Ca Mg Bact. Fungi

Species 4 124.7* 129.9* 3.6 1.1 45.0* 14.2* 25.7* 32.6* Treatment 1 790.1 * 75.7* 6.8 30.7* 0.1 25.2* 27.3* 246.4* Month 4 256.4* 10.6* 1.1 0.8 0.6 1.3 35.8* 37.4* SP x TMT 4 9.9k 4.3 1.1 0.7 13.7* 4.1 26.4* 18.2* SP x MO 16 5.2* 1.4 0.4 0.4 2.1 1.2 20.0* 2.3 MO x TMT 4 21.5* 3.3 2.6 4.6 1.1 0.1 34.3* 7.2* SP x TMT x MO 16 2.9* 0.8 1.1 0.7 1.0 0.9 2.6 3.9* Error** 0.02 1.12 0.06 1.24 7.34 2.80 0.12 0.19

* P < 0.0009. ** Error degrees of freedom equal: 298 for mass; 99 for N; 100 for P, K, Ca and Mg; 141 for bacteria and 196 for fungi.

low values of SLA and N had the lowest (Fig. 2, Table 2). Anacardium had the highest value for SLA, the lowest N concentration, and an intermediate rate of mass loss.

Nutrient concentrations in the remaining litter either increased or remained constant between January and May with few exceptions. Nitrogen concentrations were enhanced by irrigation, increased significantly over the five months litter bags were in the field, and differed among litter species (Fig. 2, Table 1). Phosphorus concentrations were highly variable and no significant effects were found (Fig. 3, Table 1). Irrigation depressed K concentrations (Fig. 3, Table 1). Calcium concentrations showed the only significant interaction observed for nutrients. The species x treatment interaction arose because Ca concentrations declined rapidly for irrigated Quararibea, but increased or remained roughly constant under irrigation for the other species (Fig. 4). Mg concentrations were enhanced by irrigation and also differed significantly among litter species (Fig. 4, Table 1).

The net effect of irrigation on dry-season nutrient release is summarized in Table 3, which presents the treatment ratio (irrigated/control) of the proportion of nutrient mass in fresh litter that remained in April. There are two consistent effects of irrigation. Irrigation increased K release from all litter species and the release of all nutrients from Quararibea litter. Irrigation had inconsistent effects on dry-season nutrient release for the remaining nutrients and litter species.

Table 2. Specific Leaf Area (SLA; cm2 g-1) and nutrient concentrations (mg g1) for fresh leaves of the five litter species.

Species SLA N P K Ca Mg

Anacardium 122.3 7.0 0.6 7.8 16.8 7.2 Hyeronima 120.7 11.2 0.5 2.9 8.8 2.4 Prioria 106.7 9.8 0.5 6.8 18.8 5.8 Quararibea 111.2 9.8 1.0 8.8 17.6 7.4 Tetragastris 69.2 9.0 0.4 4.9 6.0 3.4

Microorganisms

Bacterial CFUs were often too dense to count for dilution -4, and results are presented for dilution -5. Analyses gave qualitatively similar results for fungi for dilutions -4 and -5, and results are presented for dilution -4.

The three-way ANOVA demonstrated that irrigation affected both fungal and bacterial CFUs. Interpretation of the three-way ANOVA is difficult, however, due to a complex of significant interactions involving treatment, litter species and month (Fig. 5, Table 1).

Interpretation was easier for the ANCOVA. For bacteria, the homogeneity of slopes assumption of ANCOVA was rejected (Table 4). Control bacterial counts increased and irrigated bacterial counts decreased as litter mass decreased (Fig. 6). Litter species and interactions involving litter species did not influence bacterial counts (Table 4). For fungi, the homogeneity of slopes assump-

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Fig. 3. Phosphorus and potassium concentrations (mg g-' dry mass) for each litter species. Solid lines represent irrigated plots and dashed lines control plots. Error bars represent one standard error and are presented for one treatment for clarity unless one standard error was smaller than the plotting symbol. Sample size is three for each combination of treatment, month and litter species.

186 OIKOS 70:2 (1994)



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Fig. 4. Calcium and magnesium concentrations (mg g-' dry mass) for each litter species. Solid lines represent irrigated plots and dashed lines control plots. Error bars represent one standard error and are presented for one treatment for clarity unless one standard error was smaller than the plotting symbol. Sample size is three for each combination of treatment, month and litter species.

tion of ANCOVA was accepted (Table 4). Covariate interactions were therefore omitted, and the reduced AN- COVA model demonstrated that irrigation reduced fungal counts (Fig. 5) and that fungal counts differed significantly among litter species (Table 4).

We isolated about 500 morphospecies of fungi based on colony morphology and identified 48 genera. The genera with the most morphospecies were Aspergillus (16 species), Curvularia (8) and Verticillium (4). Species level identification was rarely possible for this diverse and little studied community. The number of morphospecies varied with time being 48 for fresh leaves in Decem- ber, 163 in January, 177 in February, 163 in March and 121 in April. Irrigation reduced counts of Penicillium sp., Acremonium sp. and a sterile mycelium (Fig. 7, Table 5), while Pestalotiopsis sp., Westerdykella sp. and Gliocla- dium sp. were influenced by the species of litter substrate (Fig. 8, Table 5). No significant effects were found for Fusarium sp. and Verticillium sp. (Table 5, data not shown).

Table 3. Irrigated: control ratios of the proportion of nutrient mass in fresh litter that remained in the litter in April.

N P K Ca Mg

Anacardium 0.96 0.78 0.50 0.80 1.54 Hyeronima 0.76 1.49 0.55 0.94 0.80 Prioria 1.04 0.79 0.72 1.11 1.27 Quararibea 0.78 0.43 0.37 0.37 0.43 Tetragastris 0.97 1.05 0.63 1.14 0.93

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Fig. 5. Numbers of colonies (CFUs g-' dry litter) for bacteria (dilution -5) and for fungi (dilution -4) for each litter species. Solid lines represent irrigated plots and dashed lines control plots. Error bars represent one standard error and are presented for one treatment for clarity unless one standard error was smaller than the plotting symbol. Sample size is four for each combination of treatment, month and litter species.

Discussion Litter bags have several limitations despite being the most frequently used method to study litter decomposition (Gilbert and Bocock 1962, Edwards 1977, Tanner 1981, Melillo et al. 1982, Anderson and Swift 1983). Litter bags may alter decomposition rates by altering litter microclimate, hindering soil contact and excluding litter macrofauna such as arthropods, millipedes, termites and earthworms (Ewel 1976, Edwards 1977, Hanlon and Anderson 1979, St. John 1980; but see Tanner 1981 and

Table 4. Analyses of covariance for colony-forming units (CFUs) g-' dry litter for bacteria and fungi. The covariate (Mass) is the proportion of litter dry mass remaining. F-ratios and error mean squares (final row) are presented. For fungi, the full model tests the assumption of homogeneity of slopes and validates the reduced ANCOVA model. Analyses were performed for the arcsine square root of the proportion of leaf mass remaining and the logarithm of CFUs g-' dry litter. These transformations stabilized variances.

Source DF Bacteria Fungi

Full Reduced model model

Treatment 1 11.0* 4.4 34.8* Species 4 3.9 0.7 6.7* Mass 1 0.1 1.6 0.02 SP x TMT 4 0.9 1.5 3.5 MassxTMT 1 11.7* 7.6 Mass x SP 4 3.4 1.2 Mass x TMT x SP 4 0.5 1.7 Error ** 0.47 0.36 0.40

* P < 0.0036. ** Error degrees of freedom equal: 78 for bacteria, 80 for the full model for fungi, and 89 for the reduced model for fungi.

OIKOS 70:2 (1994) 187



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Fig. 6. The relation between number of bacterial colonies (CFUs g'l dry litter) and the proportion of litter dry mass remaining for control (open symbols) and irrigated (closed symbols) litter. Each symbol represents a combination of plot, litter species and month.

Swift et al. 1979). Nevertheless, litter bags allow compar- isons among species and experimental manipulations and were appropiate for our purposes (Wieder and Lang 1982).

We predicted that irrigation would enhance mass loss, nutrient release and bacterial counts. The first prediction was upheld. Litter mass loss was much more rapid under

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Fig. 7. Numbers of colonies (CFUs g-1 dry litter) for fungi species depressed by irrigation. Solid lines represent irrigated plots and dashed lines control plots. Sample size is two for each combination of treatment, month and litter species.

irrigation (Fig. 2). This reflects increased leaching and biological activity with irrigation.

Significant variation in litter mass loss among litter species (Table 1) was correlated with differences in initial leaf N concentrations and specific leaf area (SLA; cm2 g-' dry mass). Hyeronima and Quararibea had rapid mass loss, high leaf N and high SLA. In contrast, Prioria and Tetragastris had slow mass loss, low leaf N and low SLA (Table 2, Fig. 2). This correlation may reflect dependence of decomposition rates on substrate quality, however, other factors such as microbial inhibitors may be important (Macauley and Waid 1981).

Litter nutrient concentrations go through the following three phases during decomposition: leaching, bioaccumulation and release. Leaching and/or accumulation may precede final release depending on the initial physical and chemical properties of the litter, the physical environment and decomposed activity (Swift et al. 1979, Berg and Staaf 1981). With the exception of Ca loss from irrigated Quararibea litter, the decline in nutrient concentrations that accompanies final release was not observed (Figs 2-4). K and P concentrations declined rapidly in the first month of exposure suggesting strong leaching (compare December values in Table 2 and January values in Fig. 3). Irrigation further depressed K concentrations further suggesting an important role for leaching (Table 3, Fig. 3). This is consistent with earlier reports that K is the most mobile element during decomposition (Brinson 1977, Swift et al. 1979, Anderson et al. 1983).

In contrast, irrigation enhanced N concentrations, and N concentrations increased steadily over the five months of exposure (Table 1, Fig. 2). This is consistent with enhanced bioaccumulation under irrigation and with earlier reports that N is accumulated by microorganisms (Anderson et al. 1983, Holland and Coleman 1987, Cue- vas and Medina 1988).

Irrigation also enhanced Mg concentrations for all litter species and Ca concentrations for all litter species except Quararibea (Table 1, Fig. 4). These increases may be an indirect consequence of enhanced leaching under irrigation. Divalent Mg and Ca ions would quickly bind to cation exchange sites freed by leaching of more mobile monovalent cations. Thus, irrigation increases in Mg and Ca concentrations need not involve bioaccumulation.

Microbial numbers Microbial activity depends on substrate quality as well as moisture (Witkamp 1966). Important substrate attributes include concentrations of carbon, other nutrients, microbial inhibitors and their ratios. These substrate attributes are likely to vary in a complex and dependent manner during decomposition. For this reason, further experi- mentation involving greater control of substrate quality would be necessary to identify substrate attributes most critical to microbes. Our analyses were designed to deter- mine whether moisture had consistent effects on micro-

188 OIKOS 70:2 (1994)



Table 5. Analyses of variance for numbers of colony-forming units g-' dry litter for eight species of fungi. F-ratios and error mean squares (final row) are presented. Logarithmic transformations stabilized variances. (1) Penicillium sp. (2) Acremonium sp. (3) sterile hyphae. (4) Pestalotia sp. (5) Westerdykella sp. (6) Gliocladium sp. (7) Fusarium sp. (8) Verticillium sp.

Source DF (1) (2) (3) (4) (5) (6) (7) (8)

Species 4 2.3 3.2 0.6 7.1* 9.6* 9.4* 1.5 2.3 Treatment 1 156.9* 29.5* 38.1* 0.5 1.3 3.2 0.8 1.2 Month 3 1.2 17.6* 4.1 1.1 1.8 4.3 2.1 0.5 SP x TMT 4 1.3 2.2 0.3 0.8 2.8 5.5* 3.5 0.6 SP x MO 12 1.4 2.7 1.3 0.5 1.1 0.9 1.8 1.1 MO x TMT 3 2.5 5.5 3.9 0.2 2.2 0.8 1.4 0.5 SP x TMT x MO 12 2.0 1.1 0.9 2.3 0.7 0.6 1.4 0.2 Error 40 0.4 0.3 0.2 0.3 0.5 0.3 0.1 0.3

* P < 0.001.

bial numbers over five months of decomposition and a range of substrate types (litter species).

The answer was clearly no for bacteria (Fig. 6, Table 4). Irrigation enhanced bacterial CFUs g'l dry litter during the first phases of decomposition (proportion of litter mass remaining > 0.9) and reduced them during intermediate phases (0.9 > proportion of litter mass remaining > 0.7; Fig. 6). Month and litter mass loss covary, and it is not surprising that post hoc tests based on the full three- way ANOVA model confirm that irrigation first enhanced and subsequently reduced bacterial counts. Bacte- rial counts were greater for irrigated litter in the first month of decomposition (January, F, 141 = 13.2, P < 0.001) and for control litter in the fifth month (May, F1,141 = 41.4, P < 0.001). For irrigated litter, bacterial counts tended to decline from higher values in January, February and March to lower values in April and May (Fig. 5).

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Fig. 8. Numbers of colonies (CFUs g-' dry litter) for fungi species affected by the species of litter substrate. Solid lines represent irrigated plots and dashed lines control plots. Sample size is two for each combination of treatment, month and litter species.

This decline was correlated with litter mass loss (Fig. 6) and probably reflects a variety of changes in substrate quality during decomposition.

In contrast, irrigation depressed community-level fungal CFUs g-' dry litter throughout the experiment (Table 4, Fig. 5). This result was also confirmed by post hoc tests based on the full three-way ANOVA model (F1 196 =

111.2 for January and F1,196 = 11.9 for May) and by species-level analyses (Fig. 7, Table 5). In control plots, community-level fungal counts were greatest when conditions were driest during February and March, and declined after light rains in April and heavier rains in May (Figs 1 and 5). These observations confirm that dry conditions enhance fungal activity (Edwards 1977, Holland and Coleman 1987).

Implications

Seasonal pulses of nutrient availability associated with seasonal decomposition have been identified in tropical grasslands (Birch 1958, 1964). Seasonal tropical forest, where high rates of litter fall and low rates of decomposition cause litter accumulation during the drier season, are also likely candidates for seasonal nutrient pulses (Swift et al. 1979). Our data substantiate this possibility.

The two mechanisms identified by Swift et al. (1979) that might contribute to seasonal pulses of nutrient availability were both considered as part of the irrigation experiment. The seasonality of litter inputs was unaf- fected by irrigation (Wright and Comejo 1990a, b); however, the advanced state of decay of irrigated litter (Fig. 2) suggests that final nutrient release will occur earlier when decomposition is not limited by seasonal drought. This may have a profound impact on the timing of forest nutrient inputs. Where drought does not occur, rapid forest floor decomposition will begin with leaf fall, and nutrient inputs from decomposing litter will reflect leaf fall seasonality. In contrast, where dry-season drought arrests decomposition, the first wet-season rains will ini- tiate the synchronous decomposition of all litter accumulated over the dry season. As a consequence, a strong pulse of nutrient inputs from decomposing litter should

OIKOS 70:2 (1994) 189



occur early in the wet season in seasonally dry tropical forests.

Acknowledgements - G. Gilbert and K. Arnebrant provided comments on the manuscript. Financial support came from the Exxon Foundation (AV) and the Short-term Visitor (FHC) and Environmental Sciences Programs (SJW) of the Smithsonian Inst.

References Alexander, M. 1977. Introduction to soil microbiology - 2nd

Edition. - Wiley, New York. Anderson, J. M. and Swift, M. J. 1983. Decomposition in trop-

ical forest. - In: Sutton, S. L., Chadwick, A. C. and Whit- more, T. C. (eds), The Tropical rain forest: ecology and management. Blackwell, Oxford, pp. 287-309.

-, Proctor, J. and Vallack, H.W. 1983. Ecological studies in four contrasting lowland rain forests in Gunung Mulu Na- tional Park, Sarawak. III. Decomposition processes and nutrient losses from leaf litter. - J. Ecol. 71: 503-527.

Berg, B. and Staaf, H. 1981. Leaching, accumulation and release of nitrogen in decomposing forest litter. - In: Clark, F. E. and Rosswall, T. (eds), Terrestrial nitrogen cycles, processes, ecosystem strategies and management impacts. Ecol. Bull. (Stockholm) 33: 163-178.

Birch, H. F. 1958. The effect of soil drying on humus decomposition and nitrogen availability. - Plant Soil 10: 9-31.

- 1964. Mineralization of plant nitrogen following alternate wet and dry conditions. - Plant Soil. 20: 43-49.

Brassell, H., Unwin, G. and Stocker, G. 1980. The quality, temporal distribution and mineral element content of litter fall in two forest types at two sites in tropical Australia. - J. Ecol. 68: 123-139.

Brinson, M. 1977. Decomposition and nutrient exchange of litter in an alluvial swamp forest. - Ecology 58: 601-609.

Cuevas, E. and Medina, E. 1988. Nutrient dynamics within amazonian forest. II. Fine root growth, nutrient availability and leaf litter decomposition. - Oecologia 76: 222-235.

Edwards, P. J. 1977. Studies of mineral cycling in a montane rain forest in New Guinea. II. The production and disappearance of litter. - J. Ecol. 65: 971-992.

Ewel, J. J. 1976. Litterfall and leaf decomposition in a tropical rain forest sucession in eastern Guatemala. - J. Ecol. 64: 293-308.

Fell, J. W. and Newell, S. Y. 1981. Role of fungi in carbon flow and nitrogen inmobilization in coastal marine plant litter systems. - In: Wicklow, D. and Carrol, G. (eds), The fungal community: its organization and role in the ecosystem. Mar- cel Dekker, New York, pp. 665-678.

Gilbert, 0. J. and Bocock, K. L. 1962. Some methods of study- ing disappearance and decomposition of leaf litter. - In: Murphy, P. W. (ed.), Progress in soil biology, pp. 348-352.

Gonzalez, A., Alvarado-Dufree, G. and Diaz, C. T. 1975. Canal Zone water quality study, final report. - Water and Labor- aratories Branch, Panama Canal Company, Canal Zone, Panama.

Griffin, D. M. 1972. Ecology of soil fungi. - Chapman and Hall, London.

Haines, B. and Foster, R. B. 1977. Energy flow through litter in a Panamanian forest. - J. Ecol. 65: 147-155.

Hanlon, R. D. and Anderson, J. M. 1979. The effects of Collem- bola grazing on microbial activity in decomposing leaf litter. - Oecologia 38: 93-99.

Hendrix, P. J., Parmelee, R. W., Crossley, D. A., Coleman, D. C., Odum, E. P. and Goffman, P. M. 1986. Detritus food webs in conventional and no-tillage agrosystems. - Bio- science 36: 374-380.

Holdridge, L. R. and Budowski, G. 1956. Report of an ecological survey of the Republic of Panama. - Caribbean Forester 17: 92-110.

Holland, E. A. and Coleman, D. C. 1987. Litter placement effects on microbial and organic matter dynamics in an agrosystem. - Ecology 68: 425-433.

Jordan, C. F 1989. An amazonian rain forest: the structure and function of a nutrient stressed ecosystem and the impact of slash-and-burn agriculture. - Man and Biosphere Series. UNESCO Paris, France and Parthenon, Carnforth.

Leigh, E. G. Jr and Smythe, N. 1978. Leaf production, leaf consumption and the regulation of folivory on Barro Col- orado Island. - In: Montgomery, G. G. (ed.), The ecology of arboreal folivores. Smithsonian Inst. Press, Washington, DC, pp. 33-50.

Macauley, B. and Waid, J. 1981. Fungal production on leaf surfaces. - In: Wicklow, D. and Carrol, G. (eds), The fungal community: its organization and role in the ecosystem. Mar- cel Dekker, New York, pp. 501-531.

Melillo, J. M., Aber, J. D. and Muratore, J. F 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics - Ecology 63: 621-626.

Olson, J. S. 1963. Energy storage and the balance of producers and decomposers in ecological systems. - Ecology 44: 322- 331.

Richards, P. W. 1952. The tropical rain forest. - Cambridge Univ. Press, London.

St. John, T. V. 1980. Influence of litter bags on growth of fungal vegetative structures. - Oecologia 46: 130-132.

Swift, M. J., Heal, 0. W. and Anderson, J. M. 1979. Decomposi- tion in Terrestrial Ecosystems. - Blackwell, Oxford.

Tanner, E. V. J. 1981. The decomposition of leaf litter in Jamai- can montane rain forest. - J. Ecol. 69: 263-275.

Valencia, H. A. 1983. Estimaciones de la respiracion microbial del suelo en vertientes humeda y seca de la Cordillera Central de Colombia. - In: Estudio de ecosistemas tropo- andinos Vol. 1. van der Hammen.

Vitousek, P. 1984. Litterfall, nutrient cycling and nutrient limita- tion in tropical forest. - Ecology 65: 285-298.

Wieder, R. K. and Lang, G. E. 1982. A critique of the analytical methods used in examining decomposition data obtained from litter bags. - Ecology 63: 1636-1642.

Windsor, D. M. 1990. Climate and moisture variability in a tropical forest, long-term records for Barro Colorado Island, Panama. - Smithsonian Contrib. Earth Sci. 29: 1-145.

Witkamp, M. 1966. Decomposition of leaf litter in relation to environment, microflora and microbial respiration. - Ecol- ogy 47: 194-201.

Wollum, A. G. 1982. Cultural methods for soil microorganisms. - In: Pace, A. L., Miller, R. H. and Keeney, D. R. (eds), Methods of soil analyses, part II. Chemical and microbiolog- ical properties. American Soc. of Agronomy and Soil Sci- ence Society of America, Madison, WI, pp. 781-802.

Wright, S. J. 1991. Seasonal drought and the phenology of understory shrubs in a tropical moist forest. - Ecology 72: 1643-1657.

- and Cornejo, F H. 1990a. Seasonal drought and the timing of flowering and leaf fall in a Neotropical forest. - In: Bawa, K. S. and Hadley, M. (eds), Reproductive ecology of tropical forest plants. Man and Biosphere Series. UNESCO, Paris, France and Partenon, Carnforth.

- and Cornejo, F H. 1990b. Seasonal drought and leaf fall in a tropical forest. - Ecology 71: 1165-1175.

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Documents

Tropical Forest Litter Decomposition under Seasonal Drought: Nutrient Release, Fungi and Bacteria