Nitrogen dynamics in decomposing chestnut oak (
Quercus prinus
L.)
in mesic temperate and tropical forest
Liam Heneghan
a,*, David C. Coleman
b, D.A. Crossley Jr.
b, Zou Xiaoming
c aEnvironmental Science Program, DePaul University, 2325 North Clifton Avenue, Chicago, IL 60614, USAbInstitute of Ecology, Ecology Annex, University of Georgia, Athens, GA 30602, USA
cInstitute for Tropical Ecosystems Studies, P.O. 363682, University of Puerto Rico, San Juan, 00936, Puerto Rico Received 15 August 1998; received in revised form 11 December 1998; accepted 25 March 1999
Abstract
This study examined nitrogen dynamics in decomposingQuercus prinusL. litter, con®ned in litterbags, in two tropical forests (La Selva Biological Station, Costa Rica and Luquillo Experimental Forest, Puerto Rico) and one temperate forest site (Coweeta Hydrologic Laboratory, NC). Using regressions of %N in the decomposing litter against litter mass remaining. we demonstrated similar concentrations of N at all sites when the amount of litter lost was 50%. By using naphthalene, an arthropod repellent, we examined the effect of microarthropods on the N ¯uxes in the litterbags. Microarthropods had little effect on the %N remaining. At La Selva, the presence of fauna resulted in a marginally signi®cant increase in litter nitrogen concentrations (p<0.06). At both tropical sites, there was a signi®cant net immobilization of N followed by N mineralization after four months. Although there was a net immobilization of N at Coweeta, this lasted for a longer period and the litterbags had not begun to mineralize N after 10 months. We suggest that the rapid accumulation of N in decomposing litter at the tropical sites during the ®rst few months after leaf fall can result in the retention of mobile nitrogen ions in soils. The subsequent mineralization, in later decomposition stages, can make N available to trees during leaf ¯ush.#1999 Elsevier Science B.V. All rights reserved.
Keywords:Nitrogen; Microarthropods; Decomposition; Tropical soils; Vernal dam; Tropical±temperate contrasts
1. Introduction
Comparisons of nitrogen cycling in lowland tropi-cal rainforests and temperate forests reveal that both produce litter with comparable dry mass/N ratios and have similarly inef®cient within-stand N use at mod-erate and high nitrogen levels (Vitousek, 1984). Decomposition, in contrast, proceeds relatively rapidly in lowland tropical rainforest compared with
temperate forest (Melillo and Gosz, 1983; Heneghan et al., in press). Since the rapid mineralization of carbon and nitrogen from decomposing rainforest litter is coupled with characteristically high levels of annual precipitation, the potential for leaching losses of mobile nitrogen ions is high (Jordan, 1985). Jordan (1985) regarded many of the structural characteristics of tropical rainforest: e.g. high root biomass, super®cial root position in soil, aerial roots, as adaptations for rapid capturing of available nutri-ents. Rainforest soils also support a highly diverse microbial community (Lodge et al., 1996) and the
*Corresponding author.
E-mail address:lhenegha@wppost.depaul.edu (L. Heneghan)
microbial production also contributes to retention of nitrogen. However, because of this potential for high N immobilization by microbes, in N-limiting conditions microbes may compete with plants for nutrients (Zak et al., 1990).
We have previously demonstrated that microarthro-pods can have a signi®cant impact on the decomposi-tion of both, local litters (Heneghan et al., in press) and on a single substrate examined in two different tro-pical sites (Heneghan et al., 1998). An in¯uence of microarthropods on N dynamics can also be expected. This is because, through its in¯uence on microbes, grazing by microarthropods can stimulate or inhibit microbial production (Lussenhop, 1992). Zheng et al. (1997) showed, using general models of both below-ground food webs and ecosystem processes, that the faunal effect on decomposition is determined by pro-perties of the microbial populations. Whether micro-bial production increases or decreases in response to grazing appears, however, to depend on the grazing intensity of the fauna (Hanlon and Anderson, 1979). A microarthropod in¯uence on microbial N accumula-tion would, therefore, result in greater or lower N concentration for a given mass of litter remaining, depending on the abundance of grazers in the system. In this paper, we examine C and N dynamics in decomposingQuercus prinuslitter con®ned in litter-bags in one temperate and two tropical forests. The temperate site is at Coweeta Hydrologic Laboratory, NC (CWT) and the tropical sites include Luquillo Forest, Puerto Rico (LUQ) and La Selva Biological Station, Costa Rica (LAS). Each site has distinctive microarthropod assemblages in terms of abundance and diversity (Heneghan et al., in press). The objec-tives of the study were (a) to compare N dynamics in decomposing litter in tropical and temperate forests, (b) to contrast N dynamics in two tropical sites which were similar in climate but which differed in the level of abundance and diversity of their microarthropods, and (c) to examine the role of microarthropods in determining the ¯uxes of N in the litter.
2. Materials and methods
2.1. Site descriptions
Three sites were chosen for this experiment, one temperate site at Coweeta Hydrologic Laboratory
(CWT), and two tropical sites: Luquillo Experimental Forest in Puerto Rico (LUQ) and La Selva Biological Station (LAS) in Costa Rica. Descriptions of the sites are given in Heneghan et al., 1998). A brief summary of their characteristics is given here.
Coweeta Hydrologic Laboratory (U.S. Forest Ser-vice), located in the Southern Appalachians of western North Carolina (358000
N; 838300
W), is a 2185-ha forested basin containing numerous small watersheds. The native hardwood forest is dominated byQuercus,
Carya and Acer spp. Mean annual rainfall is
1700 mm at lower elevations and this rainfall is
somewhat variably distributed throughout the year.
The mean annual temperature is 138C. Watershed
18, where this experiment was carried out, is a lower elevation (720 m) mixed hardwood growing on an ultisol, in the Cowee-Evard gravelly loam series.
The El Verde ®eld station at Luquillo Experimental Forest (U.S. Forest Service) (188200
N, 658490 W) is classi®ed as lower montane rainforest (Odum and Pidgeon, 1970). Elevation ranges between 300 and
600 m. Mean monthly temperature varies from 20.88
to 24.48C with a mean annual precipitation of
3456 mm (Brown et al., 1983). Soils are dominated by Zarzal series that are deep Oxisols of volcanic origin (Huffaker, 1995).
La Selva Biological Station (Organisation of Tro-pical Studies) (108260
N, 838590
W) is located in the Atlantic lowland rainforest (McDade and Hartshorn, 1994). The plot which we used was in a small patch of secondary forest where the mean monthly temperature is 25.88C and the average annual rainfall is 4000 mm (OTS, personal communication). The soils are alluvial and the plots are adjacent to the Puerto Viejo river.
2.2. Experimental design
Recently senesced leaves of Quercus prinus were
collected at CWT. The original N content of the litter was 0.72% and the original carbon concentration was 49.5% (C : N ratio of 68.75). Three grams of air-dried litter were placed in individually marked ®berglass litterbags measuring 1010 cm2. Three sets of bags
or biweekly (LAS and LUQ) with naphthalene, a biocide which repels microarthropods. The rate of application was 100 g mÿ2
month (all sites) and the naphthalene was distributed around the litterbags so that fauna would be repelled from the portion of the plots containing these bags. This is because there is evidence from microcosm studies that naphthalene can affect microbial activity (Seastedt and Crossley, 1983; Blair et al., 1989). Although there is no evidence that application at the rates used in this study affect microbial activity, this caveat must be borne in mind when the results are being assessed.
Each month, six litterbags (3 from naphthalene treated subplots and 3 from subplots where the ani-mals had unrestricted access) from each of the three replicated plots were collected at random at all sites (54 bags in total per month). Litter was oven-dried and weighed. Subsequently, the litter was ground and subsamples ignited at 5008C to determine the ash-free dry weight (AFDW). %N of the litter was analyzed by combustion using a Carlo Erba C/N analyzer (Carlo Erba, Milan).
The relationship between %N remaining and AFDW of litter remaining was examined using simple linear regression. When the concentration of N remaining in decomposing litter is plotted as a func-tion of remaining litter mass, the results give an inverse linear regression (Aber and Melillo, 1980). This relationship is thought to hold true for a very broad range of substrate types, and from both, aquatic and terrestrial systems (Aber and Melillo, 1980). Difference in the %N remaining in the litter was contrasted using analysis of variance. Differences in N remaining in litter with, and without, animals were compared using T-tests. For all statistical analyses using the SAS package (SAS Institute, 1988), differ-ences at thep <0.05 level are reported as signi®cant.
3. Results
3.1. Temperate-tropical contrasts of litterbag N dynamics
The concentration of N remaining in litterbags, as decomposition proceeded, was greater in the tropical sites than in the temperate forest (Fig. 1). After one month, the mean concentration of N in untreated
litterbags was 29.2% higher at LUQ and 77.9% higher at LAS when compared to CWT, the temperate site. This effect continued throughout the course of the study and was strongly signi®cant for the ®rst ®ve months of the experiment. The %N in litterbags at 50% original mass, using regressions equations cal-culated on data from untreated litterbags, was similar for all sites: CWT, 1.29%N; LUQ, 1.28%N; and LAS, 1.27%N (Fig. 1). The biomass loss was more rapid at both these tropical sites. These latter results are pre-sented in Heneghan et al. (in press).
Strong initial N immobilization at the tropical sites resulted in a rise in the concentration of N in these
Fig. 1. Litter mass remaining (%) as a function of N concentration in
Quercus prinuslitter placed in forests during a 10-month experiment at (a) Coweeta Hydrologic Laboratory, NC, (b) Luquillo Experimental Forest, Puerto Rico, and (c) La Selva Biological Field Station, Costa Rica. The regression equations accompanying each panel include the original point (litter N 0.72% and % original litter 100%) and are given for untreated litter and for litter treated with naphthalene to reduce microarthropod numbers. When the regressions are performed without the original point the relationship still holds for all treatments and sites with the exception of untreated litterbags at La Selva. Each symbol represents a mean of three samples for each sampling occasion. (a) Naphthalene:y ÿ63.09x143.26,r20.90; Micro-arthropods:y ÿ86.94x162.55,r20.80; (b) Naphthalene:y ÿ56.90x122.83, r20.54; Microarthropods: y ÿ77.78x
140.85,r20.62; and (c) Naphthalene;y ÿ91.39x168.53,
litterbags for the ®rst three months of the experiment (Fig. 2). This was greatest at LAS, where the amount of N increased to 135% of the original amount in litterbags with animals. A similar net N immobilisa-tion was found at LUQ. However, here the greatest amount was in treated litterbags.
3.2. Effects of fauna on %N remaining
The concentration of N remaining in litterbags at the end of the experiment increased marginally when faunal activity had been curtailed by applications of naphthalene at LUQ. This was indicated by a signi®-cantly steeper slope when %N was plotted against
%mass remaining (T-test, p0.03). The trend was
similar at CWT though there were no signi®cant differences in slopes (T-test, p0.18). Although the %N changes during the experiment in naphtha-lene-treated litterbags at LAS showed a relationship with %mass remaining, the relationship of these fac-tors in litterbags with microarthropods were quite distinctive (Fig. 1(c)). Here, there was an immediate increase in N concentration relative to the control (%N was elevated by 31.6% in the faunated bags compared with the control when the data on the ®rst collection date was compared). This elevation is marginally signi®cant (T-test,p0.06).
4. Discussion
We have shown that N concentrations, in decom-posing litter as a function of litter mass remaining, are similar in tropical and temperate forests. At 50% mass loss all three sites had the same predicted %N. How-ever, the total mass loss at the tropical sites was greater than at the temperate sites and much of this decom-position occurred in the ®rst months of the experiment (Heneghan et al., in press). Because of rapid microbial colonization of the relatively low-quality litter used in this study, decomposition proceeded in the tropical sites accompanied by a net immobilization of N (Fig. 2). After this initial phase, N is mobilized at both tropical sites. At the temperate site there was some net immobilization of N but after 10 months no mobilization of this nutrient occurred.
On the basis of a range of ecosystem parameters Jordan (1985) has classi®ed La Selva as being one of
the more eutrophic of the seven intensively studied rainforests. Luquillo is more nutrient-poor and in a PCA analysis was revealed to be similar to highly infertile Amazonia soils (Jordan, 1985). The nitrogen import into litterbags appears to re¯ect the relative nutrient status at the tropical sites. We have shown that there can be an effect of fauna on the accumulation of N in the litterbags. The presence of a low-abundance, high-diversity fauna at La Selva resulted in an initial immobilization of nitrogen compared with litterbags without fauna. The effect was only marginally sig-ni®cant however. Although there was also a net immobilization of N at Luquillo in faunated litterbags, this was not greater than the control levels. The fauna at Luquillo, in contrast to La Selva, was higher in abundance but lower in diversity (Heneghan et al., in press). Tian et al. (1992) examined the decomposition and nutrient dynamics of ®ve agroforestry and crop residues in humid tropical conditions (Nigeria) and found immobilization of N for substrates with a C : N ratios >30. They also found a small effect of fauna on
the mobilization ofLeucaenaprunings.
4.1. Microbial immobilisation of N in tropical soils: a possible `vernal' dam
In view of the nitrogen limitation of most terrestrial ecosystems (Vitousek and Howarth, 1991), it is pos-sible that in nutrient-poor conditions high demand by microbes for N could lead to competition between microbial populations and plants. Diaz et al. (1993) suggested that in response to elevated CO2, microbial
immobilization of nitrogen may act as a negative feedback on plant growth. In a northern temperate hardwood forest, Zak et al. (1990) found that
micro-bial populations immobilized added 15N in amounts
10±20 times greater than ephemeral spring ¯ora. They considered these results in the context of the `vernal dam' hypothesis of Muller and Bormann (1976), which speculates that spring plants reduce losses of N from the forest ¯oor before canopy closure. In this way, the results of the Zak et al. (1990) study indicate that, though microbes compete successfully with spring ¯ora for N, their use may complement the N demands of forest trees.
We offer the following hypothesis of the system-level signi®cance of the results from this study. In tropical forests, both leaf fall and leaf ¯ush show some
regular patterns which can be related to rainfall (Leigh and Windsor, 1996; Parker, 1994). When litterfall is synchronized, the potential for loss of N from the soil is elevated since the plant demand will be lowered at this time. As a consequence of the rapid growth of decomposer fungi, N is immobilized in the litter. As the litter is rapidly decomposed, N is subsequently mineralized at a time when leaf ¯ush creates a demand for nutrients. The net effect of this is that N is retained in the soil. The signi®cance of this putative sequence will be accentuated in forests when leaf fall is synchronized with periods of drought as is the case in Barro Colorado Island (Leigh and Windsor, 1996).
Acknowledgements
Funding for this research came from the National Science Foundation grants DEB-9416819 to the Uni-versity of Georgia. We would like to thank the Orga-nization of Tropical Studies (OTS) and the members of the Huertos project, particularly Dr. J.J. Ewel, Ankila Hiremath, Seth Bigelow and Silvino Villegas for their practical assistance and encouragement.
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