N-fixing trees in restoration plantings: Effects on nitrogen supply and soil microbial communities
Introduction
Afforestation of agricultural land may contribute to carbon sequestration, potentially mitigating climate change, and restoring of native ecosystems (Guo and Gifford, 2002, Hoogmoed et al., 2012, Paul et al., 2002). Single-species tree plantations for wood production are among the most common afforestation systems (Chazdon, 2008, Paul et al., 2002), although restoration plantings, which contain a mixture of native tree species that are not harvested, are becoming more widely planted (Cunningham et al., 2012). This is because in addition to their potential capacity to store carbon, both above- and below-ground, they provide a range of additional ecological benefits (Harrison et al., 2000), including increased habitat for native flora and fauna (Munro et al., 2009) and ecological stability (e.g. higher resilience to insect pests, Knoke et al., 2008), and nutrient interception when planted as buffer strips adjacent to waterways (Burger et al., 2010, Fennessy and Cronk, 1997).
A fundamental question in establishing mixed-species restoration plantings is which species to plant. One consideration in selecting tree species is whether individual species possess desirable traits. For example, nitrogen-fixing trees can directly fix atmospheric nitrogen (N) to support partly or totally their own growth, giving them an advantage over non-N-fixing tree species, especially in N limited systems (Galiana et al., 1998). Consequently, higher levels of soil C under N-fixing trees have been attributed to higher growth rates of N-fixing trees and subsequent higher C inputs into the soil via litter and root exudates (e.g. Resh et al., 2002, Wang et al., 2010). Including N-fixing tree species in mixed-species restoration plantings may increase and accelerate the carbon sequestration potential of the ecosystem (Kaye et al., 2000). In addition to increasing soil N (Kaye et al., 2000), heightened N levels may reduce lignin decomposition (e.g. Berg and Matzner, 1997, Carreiro et al., 2000), further slowing organic matter decomposition and increasing C sequestration (Prescott, 2010).
In mixed-species plantings, N-fixing trees can also facilitate the growth of non-N-fixers. The non-N-fixers may benefit from lowered competition for the available soil N, or they may be able to access the fixed atmospheric N pool (Forrester et al., 2006) after decomposition of the N-fixers litter (van Kessel et al., 1994), through root exudates, or via interconnected mycorrhizal networks between the trees (He et al., 2003). This facilitative effect of N-fixers on non-N-fixers is important for net primary production, as well as community development (Siddique et al., 2008) and successional processes (Chapin et al., 1994, Vitousek and Walker, 1989). Consequently, the inclusion of N-fixers in mixed species woody plants may have an important impact upon N dynamics in these systems.
The stand-scale consequences of N2-fixation on soil C sequestration are ultimately driven by the effects of N on soil processes. This may include impacts on soil microbial communities, which play a key role in organic matter decomposition (Wardle, 2002). This process is governed by complex interactions among factors such as litter quantity and quality (nutrient content and chemical structure), soil microbial community composition and several biotic and abiotic factors (e.g. Prescott, 2010). Soil microbial communities are often found to differ among tree species (Priha et al., 2001), presumably, due to differences in litter quality and quantity (Bauhus et al., 1998, Hobbie, 1992, Schweiter et al., 2012). Higher amounts of N in litter and soil under N-fixing trees are likely to have a major effect on the soil microbial community beneath these trees (Allison et al., 2006). For example, higher available nitrogen or a lower C:N ratio under N-fixers may favour bacterial over fungal decomposers (Fierer et al., 2009, Harrison and Bardgett, 2010). Bacteria are generally less adapted to decompose recalcitrant litter as fungi (Henriksen and Breland, 1999, van der Heiden et al., 2008). Therefore, increased N levels under N-fixing trees may shift the microbial community towards bacterial dominance, slowing the rate of decomposition of organic matter and increasing the rate of soil C sequestration. In contrast, fungal biomass is more recalcitrant and fungi have a higher C assimilation efficiency compared with bacteria, therefore a shift towards more bacteria could also result in a reduction of soil C sequestration (Bailey et al., 2002b).
If the potential for N-fixers to increase soil C sequestration in mixed-species afforestation plantings is to be maximized, we need to better understand the role of N-fixers in these plantings. An extensive literature exists on interactions between N-fixing and non-N-fixing trees (e.g., Bouillet et al., 2013, Forrester, 2014), albeit predominantly in relation to tree growth and wood production (e.g. Binkley et al., 2003, Parrotta, 1999) but also soil C sequestration (e.g. Kaye et al., 2000) or nutrient cycling (e.g. Khanna, 1997). However, there is a lack of consensus about how N-fixers and non-N-fixers interact and what drives differences among studies. Further, little is known about the impact of N-fixers on soil microbial communities in mixed-species plantings. Here, we present the results of a field-based study in which we investigated two important aspects of restoration plantings including both N-fixing and non-N-fixing tree species: 1) the pathways that fixed atmospheric N takes within the stand and 2) the effect of N-fixers on the soil microbial community. We asked two specific questions:
- 1.
Do non-N-fixing trees have access to N derived from the fixation of atmospheric N2 by neighbouring N-fixing trees, in the early development of a tree planting?
- 2.
Do changes in the N dynamics associated with N-fixing trees, result in changes in soil microbial communities in a mixed-species restoration planting?
To address these questions, we focused on a young (14 yr) mixed-species planting in southeastern Australia.
Section snippets
Site description
A field study was conducted in November 2011, in a mixed-species restoration planting along Castle Creek near Euroa (36′86°S, 145′58°E) in northern Victoria, south-eastern Australia. The region has a temperate climate with an mean annual rainfall of 650 mm, ranging from 30 to 80 mm month−1, monthly maximum temperatures between 12.3 and 29.7 °C and monthly minimum temperatures between 4.1 and 15.3 °C (1981–2010, Australian Bureau of Meteorology, 2011). The site was previously a pasture that was
Nitrogen cycling
There were no significant differences (P < 0.05) in the δ15N values between tree types (N-fixers and non-N-fixers) for any of the sample types (leaves, species-specific litter, litter, 0–10 cm soil layer and 10–20 cm soil layer, Table 1). However, there were significant differences in δ15N value of the soil (both 0–10 and 10–20 cm soil layers) among tree species within tree type (P < 0.01, Table 1). Soil underneath A. dealbata had a significantly higher δ15N value compared with the other tree
Discussion
There were indications that the N fixed by the N-fixing trees was redistributed and utilized by the non-N-fixing trees. Overall, there was a strong species effect within the N-fixing tree types, whereas the non-N-fixing species were more similar to each other. Characterization of the soil microbial community showed no differences among the N-fixers and the non-N-fixers, but some differences in communities under different tree species.
Conclusion
The results presented here suggest that even in a young planting in a dry environment (<800 mm yr−1) where litter decomposition is slow, N-fixers may play an important role in facilitation of non-N-fixing trees. Possible pathways by which non-N-fixing trees could take up newly fixed N include direct below-ground exchange of fixed atmospheric N from N-fixing trees to the non-N-fixing trees, or via the uptake of organic forms of N from the litter layer, instead of via the slower process of
Acknowledgements
This research was funded by the Australian Research Council Linkage Program (LP0990038), Goulburn Broken Catchment Management Authority (CMA), North Central CMA, Victorian Department of Sustainability and Environment, EPA Victoria and Kilter Pty. Ltd. T.R.C. acknowledges the Australian Research Council for financial support. T.R.C. (FT120100463) and P.J.B. were supported by Australian Research Council Future Fellowships. M.H. thanks the Holsworth Wildlife Research Endowment for additional
References (79)
- et al.
Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana
Soil Biol. Biochem.
(2006) - et al.
Relationships between soil microbial biomass determined by chloroform fumigation–extraction, substrate induced respiration, and phospolipid fatty acid analysis
Soil Biol. Biochem.
(2002) - et al.
Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration
Soil Biol. Biochem.
(2002) - et al.
Effects of tree species, stand age and soil type on soil microbial biomass and its activity in a southern boreal forest
Soil Biol. Biochem.
(1998) - et al.
Eucalyptus grandis and Acacia mangium in monoculture and intercropped plantations: evolution of soil and litter microbial and chemical attributes during early stages of plant development
Appl. Soil Ecol.
(2013) - et al.
Twenty years of stand development in pure and mixed stands of Eucalyptus saligna and nitrogen-fixing Facaltaria moluccana
For. Ecol. Manag.
(2003) - et al.
Eucalyptus and Acacia tree growth over entire rotation in single- and mixed-species plantations across five sites in Brazil and Congo
For. Ecol. Manag.
(2013) - et al.
Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon
Soil Biol. Biochem.
(2008) - et al.
Changes in soil carbon of pastures after afforestation with mixed species: sampling, heterogeneity and surrogates
Agric. Ecosyst. Environ.
(2012) - et al.
Ectomycorrhizal diversity enhances growth and nitrogen fixation of Acacia mangium seedlings
Soil Biol. Biochem.
(2013)
Variations in microbial community composition through two soil depth profiles
Soil Biol. Biochem.
The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process
For. Ecol. Manag.
Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review
For. Ecol. Manag.
15N natural abundance as a tool for assessing N2-fixation of herbaceous shrub and tree legumes in improved fallows
Soil Biol. Biochem.
Nitrogen availability effects on carbon mineralization, fungal and bacterial growth, and enzyme activities during decomposition of wheat straw in soil
Soil Biol. Biochem.
Effects of plant species on nutrient cycling
Trends Ecol. Evol.
Is there more soil carbon under nitrogen-fixing trees than under non-nitrogen-fixing trees in mixed-species restoration plantings?
Agric. Ecosyst. Environ.
Does afforestation of pastures increase sequestration of soil carbon in Mediterranean climates?
Agric. Ecosyst. Environ.
Comparison of growth and nutrition of young monocultures and mixed stands of Eucalyptus globulus and Acacia mearnsii
For. Ecol. Manag.
Effect of invasive Acacia dealbata link on soil microorganisms as determined by PCR-DGGE
Appl. Soil Ecol.
Nitrogen-fixation by Acacia dealbata and changes in soil properties 5 years after mechanical disturbance or slash-burning following timber harvest
For. Ecol. Manag.
Physicochemical and microbiological effects of long- and short-term winery wastewater application to soils
J. Hazard. Mater.
Productivity, nutrient cycling, and succession in single- and mixed-species plantations of Casuarina equisetifolia, Eucalyptus robusta, and Leucaena leucocephala in Puerto Rico
For. Ecol. Manag.
Change in soil carbon following afforestation
For. Ecol. Manag.
Soil microbial community composition as affected by restoration practices in California grassland
Soil Biol. Biochem.
Mixed plantations can promote microbial integration and soil nitrate increases with changes in the N cycling genes
Soil Biol. Biochem.
δ15N as an integrator of the nitrogen cycle
Trends Ecol. Evol.
Natural 15N abundance of plants and soils under different management practices in a montane grassland
Soil Biol. Biochem.
Occurrence of arbuscular mycorrhizaon aged Eucalyptus
Mycorrhiza
Australian Government, Bureau of Meteorology
Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δ15N
Ecology
Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata
J. Ecol.
Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems
Environ. Rev.
Arbuscular mycorrhizal impacts on competitive interactions between Acacia etbaica and Boswellia papyrifera seedlings under drought stress
J. Plant Ecol.
Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospolipid fatty acid profiles
Microb. Ecol.
An ordination of upland forest communities of southern Wisconsin
Ecol. Monogr.
Trajectories of change: riparian vegetation and soil conditions following livestock removal and replanting
Aust. Ecol.
Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition
Ecology
Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska
Ecol. Monogr.
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