Download On the nature and ecological functions of soil soluble organic

Editorials
Soil Soluble Organic Nitrogen
Editorials
On the Nature and Ecological Functions of Soil Soluble Organic Nitrogen (SON)
in Forest Ecosystems
Chengrong Chen and Zhihong Xu*
Centre for Forestry and Horticultural Research and School of Science, Faculty of Science, Griffith University, Nathan, Brisbane,
Queensland, Australia
* Corresponding author ([email protected])
As Editor-in-Chief of the area SOILS and as Subject Editor of the sub-areas Soil Chemistry and Biochemistry as well as Soil Microbiology, it is
our pleasure to inform the JSS community about the new Australian research project soil SON (soluble organic nitrogen) and, subsequently,
to present a short overview on SON.
DOI: http://dx.doi.org/10.1065/jss2006.06.159
An international collaborative research project on the nature
and ecological functions of soil SON in forest ecosystems
A new Australian Research Council (ARC) Discovery project
– 'The nature and ecological functions of soil soluble organic
nitrogen in contrasting forest ecosystems' – is currently being
undertaken by Professor Zhihong Xu and Dr Chengrong Chen
(Griffith University, Brisbane, Australia) for the period 2006–
2008, in close collaboration with Professor Torgny Näsholm
(Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, Sweden) and
Dr Heike Knicker (Lehrstuhl für Bodenkunde, Technische
Universität München, Freising-Weihenstephan, Germany).
The aims of the ARC Discovery project are:
• To determine the chemical nature of soil SON in contrasting forest ecosystems by developing and applying advanced
14N and 15N nuclear magnetic resonance, high performance liquid chromatography, pyrolysis-field ionization/mass
spectrometry and pyrolysis-gas chromatography/mass spectrometry.
• To determine the fate and biological nature of soil SON in
contrasting forest ecosystems by developing and applying
advanced 15N isotopic tracing techniques (including use of
15NH , 15NO , 13C- and 15N-labelled amino acids and other
4
3
organic materials).
• To test and verify hypotheses that
a) the amount and nature of soil SON in forest ecosystems are largely controlled by tree-soil-microbe-environment interactions;
b) soil SON acts as both a source and a sink for available
mineral N (e.g. NH4+-N, NO3–-N) to be taken up by
trees and microbes; and
c) soil SON plays a vital ecological role and the formation of SON from soil organic matter regulates the overall N cycling in N-limiting forest ecosystems.
Overview Soil SON
Introduction
Nitrogen (N) availability and fluxes are closely related to both
biomass production and species composition in terrestrial
ecosystems (e.g. Xu et al. 1993a, b, Bobbink et al. 1998, White
et al. 2004). Over 80% of N in soil is present in organic form
(e.g. Schulten & Schnitzer 1998). However, the current research on plant N uptake in terrestrial ecosystems has focused mainly on ammonium and nitrate while soluble organic
N (SON) has received little attention due to the uncertainty
in its availability for direct uptake by plants, its ecological
significance, and the technical difficulty in its measurement
(e.g. Lipson & Näsholm 2001, Jones et al. 2004, Chen et al.
2005a, b). In recent years, there is increasing evidence that
some plants are able to directly utilize and generally prefer
amino acids over inorganic N (e.g. Schimel & Chapin 1996,
Lipson & Monson 1998, Näsholm et al. 1998, Henry &
Jefferies 2003, Weigelt et al. 2005). This challenges the traditional views of the terrestrial N cycle that plants are not able
to access the organic N directly without depending on microbial mineralization to produce inorganic N and that plants
cannot compete efficiently with soil microbes for uptake of
nutrients from the soil. On the other hand, due to its mobility, soil SON represents major inputs of N to surface water in
many forested watersheds and thereby affects water quality
(e.g. Perakls & Hedin 2002, Qualls & Richardson 2003).
However, little is known about the sources and dynamics,
chemical nature and ecological functions of soil SON in forest ecosystems, particularly under subtropical and tropical
conditions (e.g. Zhong & Makeschin 2003, Zhu & Carreiro
2004). An improved understanding of the dynamic nature
and ecological significance of soil SON is required for reducing ecosystem N losses, sustaining managed forest ecosystems, maintaining biodiversity of natural forest ecosystems,
and minimizing potential N pollution in forested watersheds.
1
The Pool Size and Nature of Soil SON in Forest Ecosystems
Soil SON is operationally defined as organic forms of N dissolved in water or extracted by salt solutions (e.g. CaCl2, KCl,
K2SO4). Soil SON pools measured by different methods may
vary either in size or in chemical composition (e.g. Hannam
& Prescott 2003, Zhu & Carreiro 2004, Chen et al. 2005a,
b). The information about pool sizes and fluxes of SON in
forest soils is scant, particularly for tropical and subtropical
environments, although the amounts and fluxes of organic N
dissolved in solution have been investigated in some temperate forest ecosystems (e.g. Qualls & Haines 1991, Zhong &
Makeschin 2003). The amounts of SON in soils may vary
JSS – J Soils & Sediments 6 (2) 63 – 66 (2006)
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Soil Soluble Organic Nitrogen
greatly with soil type, vegetation cover, management practice
(N fertilization, burning, residue retention etc.), environmental conditions (e.g. rainfall, air temperature) and analytical
methods used (e.g. Chapman et al. 2001, Hannam & Prescott
2003, Zhu & Carreiro 2004, Chen et al. 2005a, b). In temperate forest ecosystems, concentrations of SON extracted
by various methods from surface soils (0–15 cm) generally
ranged from 6.5 to 16.3 mg kg–1 (Hannam & Prescott 2003,
Zhong & Makeschin 2003, Zhu & Carreiro 2004). Our recent studies have also found that concentrations of SON in
forest soils (0–10 cm) collected from subtropical Australia
ranged from as low as 1 mg N kg–1 to 124 mg N kg–1, accounting for 12–67% of total soluble N (Chen et al. 2005a,
b). According to the classic views of the terrestrial N cycle,
these SON pools would not be considered for studying the N
dynamics within the ecosystems. However, the presence of
substantial amounts of SON found in forest soils makes it
difficult to justify the sole focus on inorganic N (NH4+-N and
NO3–-N) in studying the ecological functions of N.
Despite the importance of SON, there is a paucity of information concerning its composition, particularly in forest soils.
Chemical nature of soil SON greatly depends on the sources
of SON and varies with soil type and land use. In agricultural
soils, free amino acids and amino sugars only account for
<5% of SON, heterocyclic-N for up to 15% and amino-N
(peptides and proteins) for 35–57% (e.g. Murphy et al. 2000,
Jones et al. 2004, Paul & Williams 2005). In forest soils, free
amino acids comprise a small proportion of SON, ranging
from 1.5% to 25% of SON (e.g. Schmidt & Stewart 1999,
Hannam & Prescott 2003). The remaining components of
SON may include polypeptides, amino-sugars, proteins,
polyphenols, tannin and amino acid-humic acid complexes
(e.g. Smolander & Kitunen 2002). In general, soils contain
larger amounts (10–20% of SON) of free amino acids in arctic and boreal forest ecosystems, than in temperate and subtropical ecosystems (<10% of SON) (e.g. Schmidt & Stewart
1999, Hannam & Prescott 2003). Little is known about the
composition of amino acids in SON pools. Yu et al. (2002)
suggested that the amino acids with microbial origins, such
as alanine, aspartic acids and glutamic acid, might be predominant in temperate forest ecosystems. Biodegradability
of soluble organic matter has been used as a measure of its
biological nature (e.g. Cleveland et al. 2004). About 10–40%
of soluble organic C (SOC) may be easily decomposed (Kalbitz
et al. 2000). But there is very limited information about biodegradability of SON (Kalbitz et al. 2000, Neff et al. 2003).
2
The SON Cycle and its Potential Ecological Role in Forest
Ecosystems
SON can enter into ecosystems through precipitation, be generated during the contact of water with vegetation and soils,
and ultimately leave the ecosystems through leaching or runoff into stream or groundwater (e.g. Qualls & Haines 1991,
Neff et al. 2002, 2003). A number of biological, physical,
chemical and hydrological processes are involved in the production, decomposition and movement of SON in forest ecosystems. Compared with SOC, much less is known about the
dynamic transformation and ecological significance of SON
in soil (e.g. Kalbitz et al. 2000). The SON can be directly
produced by microbial turnover and indirectly through microbial generation of extracellular enzymes (Neff et al. 2003).
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Editorials
Fig. 1: A hypothetical model for the SON cycle in forest ecosystems. a: Decompostion; b: Cell uptake; c: Microbial exucation; d: Microbial autolysis; e:
Root direct uptake; f: Root exucation; g: Humification; h: Nutrient leakage;
i: Tropic interaction (micro/meso-fauna grazing)
A hypothetical model for the SON cycle in forest ecosystems is
presented in Fig. 1. The potential sources of SON in forest mineral soils, as shown in Fig. 1, may include: a) leaching of soluble organic matter and microbial biomass from forest floors
(leaf litter, woody debris etc.) and from tree canopy; b) microbial dissolution and decomposition of soil organic matter (e.g.
cellulose, lignin); c) microbial debris and metabolites; d) root
exudation and turnover; and e) atmospheric organic N deposition (e.g. Qualls et al. 2000, Neff et al. 2003). It has been suggested that the majority of SON may be derived from the dissolution and decomposition of litter materials and soil organic
matter in forest ecosystems because of their abundance in the
soil (e.g. Kalbitz 2000, Qualls et al. 2002). However, the contribution from these, along with other sources as described above,
to the production of SON in forest soils, is poorly quantified.
The amount of SON retained in mineral soil and the flux of
SON are mainly controlled by geochemical and hydrological
mechanisms (e.g. Kalbitz et al. 2000, Qualls & Richardson 2003).
2.1
The fate of soil SON
In the hypothetical model (see Fig. 1), the fate of soil SON in
forest ecosystems may include: a) microbial cell uptake; b)
decomposition into inorganic N; c) root direct uptake; d)
humification into soil organic matter; and e) leaching loss.
On one hand, soil SON could be mineralised by endocellular
enzymes, produced by microbes, plants and macro/mesofauna, releasing NH4+ and by microbial immobilization-mineralization (‘microbial loop’) and micro/meso-fauna grazing
(trophic interaction) to release NH4+ (e.g. Elliott et al. 1980,
Coleman 1994, Jones et al. 2004). On the other hand, soil
inorganic N (e.g. NH4+) can be immobilized by microbes and
the microbial N may thus enter SON pools as amino acids
and other forms of organic N by microbial death or damage
due to stress (e.g. drying & rewetting, freeze-thaw; e.g. Deluca
et al. 1992, Chen et al. 2003). Therefore, soil SON may act
as both sink and source for inorganic N (e.g. NH4+).
2.2
Microbial mineralization
Microbial mineralization of insoluble organic N is an essential intermediate step for the conversion of organic N into
inorganic N for plant growth, which is described as a rate-
JSS – J Soils & Sediments 6 (2) 2006
Editorials
Soil Soluble Organic Nitrogen
Fig. 2: Classical model of microbial mineralization of organic N in forest ecosystems (a) and the proposed model of microbial mineralization of organic N
in forest ecosystems (b)
limiting step for N supply in traditional ecological models
(e.g. Aber & Melillo 2001) (Fig. 2a). Microbial mineralization is classically considered as the centre of terrestrial N cycle and regulates the overall N availability due to the assumptions that plants can only utilize inorganic N and are less
competitive for available N compared with soil microbes (e.g.
Schimel & Bennett 2004). However, a number of studies have
shown that available inorganic N (as traditionally measured by
net N mineralization) is not sufficient to account for annual
tree N uptake in alpine, arctic and boreal forest ecosystems
(e.g. Chapin et al. 1988, Fisk & Schmidt 1995, Kaye & Hart
1997). This leads to a re-examination of the above assumption
on the terrestrial N cycles. The growing evidence in the past
decade has indicated the widespread direct uptake of simple
organic N (e.g. amino acids) by plants with or without
mycorrhiza across many ecosystems (including arctic, alpine,
boreal and subtropical ecosystems; e.g. Chapin et al. 1993,
Lipson & Monson 1998, Näsholm et al. 1998, Henry & Jefferies
2003, Weigelt et al. 2005). The capability of adsorbing intact
amino acids by plants varies with plant species, type of amino
acids, soil N status and degree of competition from microbes
(e.g. Schmidt & Stewart 1999, Lipson & Näsholm 2001,
Öhlund & Näsholm 2004). The extent of contribution of SON
pools to plant N nutrition is still unclear (e.g. Näsholm &
Persson 2001, Cookson & Murphy 2004, Jones et al. 2005). In
addition, direct evidence for uptake of native soil SON by plants
is still lacking. Microbes are assumed to outcompete plants for
uptake of nutrients due to their ubiquitous distribution throughout the soil, their higher surface to volume ratio, substrate affinities, and specific growth rate compared with plant roots
(e.g. Lipson & Näsholm 2001). It has been suggested that relatively low concentrations of amino acids, rapid turnover (with
half-lives of 1.7–28.7 hours in the soil), and relatively slow
movement of amino acids compared with NH4+ and NO3– make
it difficult for plant roots to capture substantial amounts of
amino acids in soil (e.g. Lipson & Näsholm 2001). However,
some strategies have been suggested for plants to efficiently
compete for organic N with microbes, including longer life
span of plants, temporal partition of N between plants and
microbes, association with mycorrhiza and microsite processes (e.g. Lipson & Näsholm 2001, Näsholm & Persson
2001, Schimel & Bennett 2004). As discussed above, direct
utilization of organic N may be a potentially important new
pathway for plant N uptake (Fig. 2b), leading to a 'shortcircuiting' of the N cycle bypassing the mineralization path-
JSS – J Soils & Sediments 6 (2) 2006
way (see Fig. 2a). If this 'short circuit' is proved to be significant in the terrestrial N cycle, the conversion from soil organic matter into SON rather than the conversion of SON
into NH4+ would be the rate-limiting step and regulate the
overall N availability in the ecosystem (see Fig. 2b). This is
supported by preliminary results from some laboratory experiments (e.g. Jones & Kielland 2002, Jones et al. 2004).
3
Conclusions and Perspectives
The ecological significance of SOC has been discussed and
many questions remain unanswered. The ecological role of
SON is even less known compared with SOC due to the uncertainties concerning its composition, sinks, sources and
bioavailability. As described in Fig. 1, SON may act as both
source and sink for inorganic N, and production of SON may
provide for long-term N storage in terrestrial ecosystems if SON
is significantly adsorbed to mineral soil (e.g. Hättenschwiler &
Vitousek 2000). The low molecular weight SON fraction may
directly regulate the rate of ammonification and nitrification
in soil by providing the substrate for these transformations,
contribute greatly to plant N nutrition, and play a vital ecological role in N cycling in forest ecosystems. The SON, along
with soluble inorganic N, has the potential to be leached out
of the ecosystems in the hydrological events (e.g. rainfall; e.g.
Perakls & Hedin 2002, Neff et al. 2003). Leaching loss of SON
from forest ecosystems, due to its mobility in soil solution, may
have some ecological consequences. Leaching of SON can constrain the accumulation and availability of N and reduce N
stock in terrestrial ecosystems. Moreover, it can enhance N
bioavailability in aquatic ecosystems. The SON may represent
the major form of N in stream water and contribute to pollution of surface water and forested watersheds (e.g. Qualls et al.
2000, Perakls & Hedin 2002). Mobility of SON appears to
be regulated by the sorption to mineral soil components and
to a lesser degree, by the biodegradation and uptake of biota.
Neff et al. (2003) implied that the recalcitrant fraction of SON
might contribute significantly to SON loss before its decomposition or uptake could occur, even during periods of substantial ecosystem demand for N. In addition to its potential
ecological roles described as above, SON may, by the association with SOC, potentially be a major controlling factor in
soil formation, mineral weathering and pollutant transport
(e.g. Kalbitz et al. 2000). However, all these potential ecological roles of SON have yet to be quantified.
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Soil Soluble Organic Nitrogen
Acknowledgement. We acknowledge the funding support and in-kind
contributions from the ARC and Forestry Plantations Queensland. Professor Torgny Näsholm (Swedish University of Agricultural Sciences,
Umeå, Sweden) and Dr Heike Knicker (Technische Universität München, Freising-Weihenstephan, Germany) are our project collaborators, and made valuable comments on the ARC project development.
We wish to thank our Publisher Editor Ms Almut Heinrich for her valuable comments and editorial inputs.
References
Aber JD, Melillo JM (2001): Terrestrial Ecosystems, 2nd ed. Harcourt-Academic Press San Diego, CA
Bobbink R, Hornung M, Roelofs JGM (1998): The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. Journal of Ecology 86, 717–738
Chapin FS, Fetcher N, Kielland K, Everett KR, Linkins AE (1988): Productivity and nutrient cycling of Alaskan tundra: Enhancement by flowing
soil water. Ecology 69, 693–702
Chapin FS, Moilanen L, Kielland K (1993): Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150–153
Chapman PJ, Williams BL, Hawkins A (2001): Influence of temperature
and vegetation cover on soluble inorganic and organic nitrogen in a spodosol. Soil Biology and Biochemistry 33, 1113–1121
Chen CR, Xu ZH, Blumfield TJ, Hughes JM (2003): Soil microbial biomass
during the early establishment of hoop pine plantation: Seasonal variation and impacts of site preparation. Forest Ecology and Management
186, 213–225
Chen CR, Xu ZH, Keay P, Zhang SL (2005a): Total soluble nitrogen in
forest soils as determined by persulfate oxidation and by high temperature catalytic oxidation. Australian Journal Soil Research 43, 515–523
Chen CR, Xu ZH, Zhang SL, Keay P (2005b): Soluble organic nitrogen pools
in forest soils of subtropical Australia. Plant and Soil 277, 285–297
Cleveland CC, Neff J C, Townsend AR, Hood E (2004): Composition, dynamics, and fate of leached dissolved organic matter in terrestrial ecosystems: Results from a decomposition experiment. Ecosystems 7, 175–285
Coleman DC (1994): The microbial loop concept as used in terrestrial soil
ecology studies. Microbial Ecology 28, 245–250
Cookson WR, Murphy DV (2004): Quantifying the contribution of dissolved organic matter to soil nitrogen cycling using 15N isotopic pool
dilution. Soil Biology and Biochemistry 36, 2097–2100
DeLuca TH, Keeney DR, McCarty GW (1992): Effect of freeze-thaw events
on mineralization of soil nitrogen. Biology and Fertility of Soils 14,
116–120
Elliott ET, Anderson RV, Coleman DC, Cole CV (1980): Habitable pore
space and microbial trophic interactions. Oikos 35, 327–335
Fisk MC, Schmidt S (1995): Nitrogen mineralization and microbial biomass
nitrogen dynamics in three alpine tundra communities. Soil Science Society of America Journal 59, 1036–1043
Hannam KD, Prescott CE (2003): Soluble organic nitrogen in forests and
adjacent clearcuts in British Columbia, Canada. Canadian Journal of
Forest Research 33, 1709–1718
Hattenschwiler S, Vitousek PM (2000): The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends in Ecology and Evolution 15,
238–243
Henry HAL, Jefferies RL (2003): Interactions in the uptake of amino acids,
ammonium and nitrate ions in the Arctic salt-marsh grass, Puccinellia
phryganodes. Plant Cell and Environment 26, 419–428
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005): Dissolved
organic nitrogen uptake by plants – An important N uptake pathway?
Soil Biology and Biochemistry 37, 413–423
Jones DL, Kielland K (2002): Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biology and
Biochemistry 34, 209–219
Jones DL, Shannon D, Murphy DV, Farrar J (2004): Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biology
and Biochemistry 36, 749–756
Kalbitz K, Solinger S, Park J-H, Michalzik B, Matzner E (2000): Controls
on the dynamics of dissolved organic matter in soils: A review. Soil Science 165, 277–304
Kaye JP, Hart SC (1997): Competition for nitrogen between plants and soil
microorganisms. Trends in Ecology and Evolution 12, 139–143
66
Editorials
Lipson DA, Monson RK (1998): Plant-microbe competition for soil amino
acids in the alpine tundra: effects of freeze-thaw and dry-rewet events.
Oecologia 113, 406–414
Lipson DA, Näsholm T (2001): The unexpected versatility of plants: Organic nitrogen use and availability in terrestrial ecosystems. Oecologia
128, 305–316
Murphy DV, Macdonald AJ, Stockdale EA, Goulding KWT, Fortune S, Gaunt
JL, Poulton PR, Wakefield JA, Webster CP, Wilmer WS (2000): Soluble
organic nitrogen in agricultural soil. Biology and Fertility of Soils 30,
374–387
Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998):
Boreal forest plants take up organic nitrogen. Nature 392, 914–916
Näsholm T, Persson J (2001): Plant acquisition of organic nitrogen in boreal
forests. Physiologia Plantarum 111, 419–426
Neff JC, Chapin III FS, Vitousek PM (2003): Breaks in the cycle: Dissolved
organic nitrogen in terrestrial ecosystems. Frontiers in Ecology and the
Environment 1, 205–211
Neff JC, Holland EA, Dentener FJ, McDowell WH, Russell KM (2002):
The origin, composition and rates of organic nitrogen deposition: A missing piece of the nitrogen cycle? Biogeochemistry 57/58, 99–136
Öhlund J, Näsholm T (2004): Regulation of organic and inorganic nitrogen
uptake in Scots pine (Pinus sylvestris) seedlings. Tree Physiology 24,
1397–1402
Paul J-P, Williams BL (2005): Contribution of [alpha]-amino N to extractable organic nitrogen (DON) in three soil types from the Scottish uplands. Soil Biology and Biochemistry 37, 801–803
Perakls SS, Hedin LO (2002): Nitrogen loss from unpolluted South American
forests mainly via dissolved organic compounds. Nature 415, 416–419
Qualls RG, Haines BL (1991): Geochemistry of dissolved organic nutrients
in water percolating through a forest ecosystem. Soil Science Society
America Journal 55, 1112–1123
Qualls RG, Haines BL, Swank WT, Tyler SW (2000): Soluble Organic and
Inorganic Nutrient Fluxes in Clearcut and Mature Deciduous Forests.
Soil Science Society America Journal 64, 1068–1077
Qualls RG, Haines BL, Swank WT, Tyler SW (2002): Retention of soluble
organic nutrients by a forested ecosystem. Biogeochemistry 61, 135–171
Qualls RG, Richardson CJ (2003): Factors controlling concentration, export, and decomposition of dissolved organic nutrients in the Everglades
of Florida. Biogeochemistry 62, 197–229
Schimel JP, Bennett J (2004): Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85, 591–602
Schimel JP, Chapin FS III (1996): Tundra plant uptake of amino acid and
NH4+ nitrogen in situ: Plants compete well for amino acid N. Ecology
77, 2142–2147
Schmidt S, Stewart GR (1999): Glycine metabolism by plant roots and its
occurrence in Australian plant communities. Australian Journal of Plant
Physiolology 26, 253–264
Schulten H-R, Schnitzer M (1998): The chemistry of soil organic nitrogen:
A review. Biolology and Fertility of Soils 26, 1–15
Smolander A, Kitunen V (2002): Soil microbial activities and characteristics
of dissolved organic C and N in relation to tree species. Soil Biology and
Biochemistry 34, 651–660
Weigelt A, Bol R, Bardgett RD (2005): Preferential uptake of soil nitrogen
forms by grassland plant species. Oecologia 142, 627–635
White LL, Zak DR, Barnes BV (2004): Biomass accumulation and soil nitrogen availability in an 87-year-old Populus grandidentata chronosequence. Forest Ecology and Management 191, 121–127
Xu ZH, Saffigna PG, Myers RJK, Chapman AL (1993a): Nitrogen cycling
in leucaena (Leucaena leucocephala) alley cropping in semi-arid tropics. I. Mineralization of nitrogen from leucaena residues. Plant and
Soil 148, 63–72
Xu ZH, Myers RJK, Saffigna PG, Chapman AL (1993b): Nitrogen cycling
in leucaena (Leucaena leucocephala) alley cropping in semi-arid tropics.
II. Response of maize growth to addition of nitrogen fertilizer and plant
residues. Plant and Soil 148, 73–82
Yu Z, Zhang Q, Kraus TEC, Dahlgren RA, Anastasio C, Zasoski RJ (2002):
Contribution of amino compounds to dissolved organic nitrogen in forest soils. Biogeochemistry 61, 173–198
Zhong Z, Makeschin F (2003): Soluble organic nitrogen in temperate forest
soils. Soil Biology and Biochemistry 35, 333–338
Zhu W-X, Carreiro MM (2004): Temporal and spatial variations in nitrogen transformations in deciduous forest ecosystems along an urban-rural gradient. Soil Biology and Biochemistry 36, 279–288
JSS – J Soils & Sediments 6 (2) 2006