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Gross nitrogen transformations in adjacent native and plantation forests of subtropical Australia
ARTICLE IN PRESS
Soil Biology & Biochemistry 39 (2007) 426–433 www.elsevier.com/locate/soilbio
Gross nitrogen transformations in adjacent native and plantation forests of subtropical Australia Joanne Burtona,b,c,, Chengrong Chenb, Zhihong Xub, Hossein Ghadiria,c a
Faculty of Environmental Sciences, Griffith University, Nathan 4111, Australia Centre for Forestry and Horticultural Research, Faculty of Science, Griffith University, Nathan 4111, Australia c Centre for Riverine Landscapes, Faculty of Environmental Science, Griffith University, Nathan 4111, Australia
b
Received 22 June 2006; received in revised form 3 August 2006; accepted 11 August 2006 Available online 18 September 2006
Abstract The impact of land-use change on soil nitrogen (N) transformations was investigated in adjacent native forest (NF), 53 y-old first rotation (1R) and 5 y-old second rotation (2R) hoop pine (Araucaia cunninghamii) plantations. The 15N isotope dilution method was used to quantify gross rates of N transformations in aerobic and anaerobic laboratory incubations. Results showed that the land-use change had a significant impact on the soil N transformations. Gross ammonification rates in the aerobic incubation ranged between 0.62 and 1.78 mg N kg1 d1, while gross nitrification rates ranged between 2.1 and 6.6 mg N kg1 d1. Gross ammonification rates were significantly lower in the NF and the 1R soils than in the 2R soils, however gross nitrification rates were significantly higher in the NF soils than in the plantation soils. The greater rates of gross nitrification found in the NF soil compared to the plantation soils, were related to lower soil C:N ratios (i.e. more labile soil N under NF). Nitrification was found to be the dominant soil N transformation process in the contrasting forest ecosystems. This might be attributed to certain site conditions which may favour the nitrifying community, such as the dry climate and tree species. There was some evidence to suggest that heterotrophic nitrifiers may undertake a significant portion of nitrification. r 2006 Elsevier Ltd. All rights reserved. Keywords: Gross N mineralisation; Gross nitrification; Anaerobic and aerobic incubation; C:N ratio; Land-use change
1. Introduction As a result of growing demands for forest products and a reduced forest land base, the Australian forestry industry is becoming increasingly reliant on single tree species plantations to meet its timber needs. At present in Queensland, Australia, about 216,500 ha are devoted to both exotic pine and native species plantations which supply a large proportion of the timber inputs for the Queensland forestry industry (QDPI and F, 2006). In order to maintain the long-term productivity of these forest soils, and hence a sustainable forestry industry, it is essential to understand
Corresponding author. Faculty of Environmental Sciences, Griffith University, Nathan Campus, Kessels Road Nathan, Brisbane, Qld. 4111, Australia. Tel.: +61 7 3735 3638; fax: +61 7 3735 7459. E-mail address: J.Burton@griffith.edu.au (J. Burton).
0038-0717/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2006.08.011
the impact of land-use change from native forest (NF) to forest plantations on soil nutrient cycling. Nitrogen (N) is an essential element for plant growth and N deficiency frequently limits forest productivity (Binkley and Hart, 1989; Paul and Clark, 1989; Reich et al., 1997). Soil N transformations are microbially mediated processes, which are influenced by a number of factors, including composition and diversity of the soil microbial community, substrate quality and quantity, and environmental conditions (Stevenson and Cole, 1999; Compton and Boone, 2002; Templer et al., 2003; Grenon et al., 2004). These factors are likely to be influenced by land-use change. For instance, land-use change from NF to plantation forest results in a shift in plant species, which directly influences the quality and quantity of organic matter input from both plant residues and root exudates. This in turn may lead to changes in soil microbial communities, which subsequently influence soil N transformations (Van Miegroet and Cole,
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1988; Verchot et al., 2001; Ross et al., 2004; Patra et al., 2006; Ste-Marie and Houle, 2006). Land-use change also causes disturbance to the soil ecosystem through harvesting and site preparation, which may have an impact on soil microbial communities and subsequently N availability and long-term site productivity (Cole, 1995; McMurtrie and Dewar, 1997; O’Connell et al., 2004; Tan et al., 2005). Finally, environmental conditions such as temperature and moisture also influence soil N transformations, particularly losses of N from the soil through leaching or denitrification. To date, a large proportion of research into soil N dynamics has been conducted in the northern hemisphere, where N deposition is an issue affecting soil N transformations and the climate is quite different from that in south east Queensland, Australia (Ross et al., 2004; Ste-Marie and Houle, 2006). Hence, there is a paucity of information relating to gross N transformations in subtropical forest soils. Furthermore, the effect of land-use change from NF to plantation forest and subsequent rotations on soil N transformations in subtropical zones has not been well studied. Hoop pine (Araucaia cunninghamii) is an N demanding native rainforest species of south east Queensland. At present, hoop pine plantations account for approximately one quarter of Queensland’s plantation area (50,000 ha) and most of the current plantations were established on land which was previously NF. The objective of this study was to examine the impact of land-use change from NF to first rotation (1R) hoop pine plantation and subsequent second rotation (2R) hoop pine plantation on soil N transformations in subtropical Australia. 2. Materials and methods 2.1. Site description and sample collection This study was conducted in Yarraman State Forest, south east Queensland, Australia (261520 S, 1511510 E). Details of the study area were provided by Chen et al. (2004). In brief, annual rainfall at this site ranges between 433 and 1110 mm, with an average of 816 mm. The soil was a Typic Durustalf (Soil Survey Staff, 1999), with a clayey texture (Chen et al., 2004). The NF site is classified as a mixed rainforest/scrub and is dominated by bunya pine (Araucaria bidwilli Hook.), yellowwood (Terminalia oblongata F. Muell. Suubsp. Oblongata), crows ash (Pentaceras australis R.B) and lignum-vitae (Premna lignum-vitae), with emergent hoop pine (Araucaria cunninghamii Aiton ex A. Cunn.). Experimental sites measuring 0.2 ha in area were located in adjacent NF, 1R hoop pine plantation (53 y-old) and 2R hoop pine plantation (5 y-old). Both the 1R and 2R hoop pine plantation sites were converted from NF in 1952. The first rotation of hoop pine at the 2R site was clearfall harvested in 1999, and post harvest residues from the first rotation plantation were formed into windrows approximately 6 m apart,
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using a D6 bulldozer with shear blade. The areas between windrows were then used as tree-planting rows for the 2R hoop pine plantation. Hence, the 2R plantation experimental area was divided into two treatments based on the residue management practices. These were: (1) tree planting row (2R-T) and (2) windrow of harvest residues (2R-W). A buffer area of at least 100 m was left between experimental areas to avoid edge effects. Each of the four treatments had five 24 m2 replicate plots. Fifteen soil cores (0–10 cm) were randomly collected from each plot using a 7.5 cm diameter auger and bulked. Litter (L) layer and fermentation (F) layer samples were collected from the plots at the NF and 1R sites using a 0.25 m2 steel quadrat. Five samples were taken from each plot and bulked together. Humus layer was not clearly distinguished in either the NF or plantation forests. All samples were transported to the laboratory where field moist soils were well mixed and passed through a o2 mm sieve and stored at 4 1C until the 15N isotope dilution study could be conducted. Roots, separated from soil during sieving, and litter samples were dried at 50 1C. A subsample of each soil was air-dried for chemical analysis. 2.2. Aerobic and anaerobic incubations Gross and net ammonification, nitrification and ammonium and nitrate consumption rates were determined in a 3-d aerobic incubation using the 15N pool dilution method (Hart et al., 1994b). Traditionally, anaerobic incubations have been used as an index of N mineralisation and availability (Keeney, 1982). They are also useful in terms of understanding N transformation processes which may occur in soils that are subjected to anaerobic conditions during periods of rainfall, as well as predicting N transformations which may occur in anaerobic microsites within the soil. As such, anaerobic incubations were also conducted using the 15N pool dilution method to determine gross and net mineralisation and ammonium consumption rates. Prior to the aerobic incubation, six portions of the field moist soils (5 g dry weight equivalent) were weighed into 50 ml propylene falcon tubes. The soil moisture was then adjusted to 45% of the water holding capacity and samples were conditioned at 25 1C for 24 h in a humid environment to ensure that they would not dry out. After conditioning, two soil samples were labelled with 600 ml of either (15NH4)2SO4 solution (4.76 mg N; ca. 98 at% 15N excess), or K15NO3 solution (15 mg N; ca. 99 at% 15N excess), which were applied evenly to the samples. An equivalent volume of distilled water was applied to another two soil samples, to be used as the control. Average soil moisture content of all samples after this addition was approximately 65% of the water holding capacity. Tubes were then capped and placed into the incubator at 25 1C. After 3 h, as suggested in Murphy et al. (2003), the time zero (T0) samples were removed from the incubator and extracted with 50 ml of 2 M KCl.
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Samples were shaken for 1 h, centrifuged at 2000 rpm for 10 min and then filtered through Whatman No. 42 filter paper and frozen until analysis. The remaining samples (T1) were removed from the incubator after 72 h and extracted as above. For the anaerobic incubation, four portions of field moist soils were prepared and conditioned as above. After conditioning, two soil samples were labelled with 25 ml of (15NH4)2SO4 solution (4.76 mg N; ca. 98 at% 15N excess). The equivalent volume of distilled water was added to another two samples of fresh soil, to be used as the control. Tubes were shaken gently for 3 min and then placed into the incubator at 25 1C. After 3 h, the T0 samples were removed from the incubator and extracted with 25 ml of 4 M KCl, so that the final ratio of soil:extract as well as the concentration of the KCl extract was equivalent to that used for the aerobic incubation. Samples were shaken for 1 h, centrifuged at 2000 rpm for 10 min and then filtered through Whatman No. 42 filter paper and frozen until further analysis could take place. The T1 samples were removed from the incubator after 72 h and extracted as above. 2.3. Steam distillation and chemical analysis Mineral N (NH+ 4 –N and NO3 –N) concentrations in the extracts were determined using a LACHAT Quickchem Automated Ion Analyser (QuikChem Method 10-107-0604-D for NH+ 4 –N and QuikChem Method 12-107-04-1-B 15 for NO N analysis using 3 –N). Samples were prepared for steam distillation (Keeney and Nelson, 1982). In brief, each extract was spiked with a known NH+ 4 and NO3 standard to provide sufficient total N for analysis. We then added 10 ml of 3.5% NaOH to convert the NH+ 4 to NH3 gas, and steam distilled the sample. The NH3 gas was collected in 10 ml of 2% HCl. Subsequently, 0.2 mg of Devarda’s alloy + was added to reduce the NO 3 to NH4 and the sample was redistilled with the NO3 collected in the form of NH3 in 10 ml of 2% HCl. Distillates were dried down at 50 1C, and isotope ratio analyses were performed using an isotope ratio mass spectrometer with a Eurovector elemental analyser (Isoprime-EuroEA 3000). Soil, root and litter total carbon (C) and N as well as carbon isotope composition (d13C) and 15N natural abundance (d15N) were also measured using the mass spectrometer.
2.4. Calculations and statistical analysis Rates of N mineralisation and ammonium consumption (for anaerobic incubation data), and ammonification, nitrification and ammonium consumption (for aerobic incubation data) were calculated using the equations developed by Kirkham and Bartholomew (1954), and presented in Hart et al. (1994b). One-way analysis of variance (ANOVA) was carried out for all data in Statistix for Window version 2.2 (Analytical Software, Tallahassee, FL). We acknowledge that a limitation of this study, as with many other paired-site studies, was the pseudoreplication used for ANOVA. Least significant difference (LSD, Po0.05) was used to separate treatment means when differences were significant. Paired t-tests and Pearson linear correlations were also conducted in Statistix for Windows version 2.2. 3. Results 3.1. Soil chemical properties Basic chemical properties of the soils under the adjacent NF, 1R, 2R-T and 2R-W are shown in Table 1. Soil total C and N were significantly higher in the NF soils than in the plantation soils. Total C was higher in the 1R soils than in the 2R soils. Concentrations of NH+ 4 were higher in the NF soils than in the plantation soils, while the concentration of NO 3 was approximately two times higher in the NF soils than in the plantation soils (Table 1). However, there was no significant difference in NH+ 4 and NO3 concentrations between the 1R and the 2R soils, or between the 2R-T and the 2R-W soils. The same pattern was found for the d15N results, whilst d13C was higher in the 2R-T soils than in the NF soils. The C:N ratios ranged between 11.8 in the NF soils and 13.7 in the 1R soils. The NF soils had significantly lower C:N ratios than the plantation soils, while the 1R soils had significantly higher C:N ratios than the 2R soils. Both pH and cation exchange capacity (CEC) differed among the different treatments. 3.2. Characteristics of forest litter material and tree roots Total C and total N contents and d13C and d15N values were measured on L- and F-layer, and root samples from
Table 1 Soil properties for adjacent native forest (NF), 53 y-old first rotation hoop pine plantation (1R), 5 y-old second rotation tree row (2R-T) and second rotation windrow (2R-W) at the Yarraman site, subtropical Australia Forest type
pH (1:2.5 H2O)
CEC (C mol kg1)
Total C (%)
Total N (%)
C:N ratio
d13C (%)
d15N (%)
NH+ 4 (mg N kg1)
NO 3 (mg N kg1)
NF 1R 2R-T 2R-W
6.2b 6.6a 6.0c 6.2b
56.9a 50.9a 38.0b 36.5b
8.9a 7.1b 5.8c 6.1c
0.75a 0.52b 0.46b 0.47b
11.8c 13.7a 12.6b 12.9b
25.8b 25.7ab 25.5a 25.7ab
9.8a 8.9b 8.3b 8.6b
2.5a 2.1b 2.1b 2.2b
98.6a 43.8b 43.1b 58.5b
Values are means (n ¼ 5) and if followed by the same letter are not significant at the 5% level of significance.
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Table 2 Basic chemical properties of litter (L) and fermentation (F) layer of adjacent native forest (NF) and 53 y-old first rotation hoop pine plantation (1R) at the Yarraman site, subtropical Australia Fermentation layer 13
15
Litter layer 13
15
Roots (0–10 cm)
Forest type
d C (%)
d N (%)
Total C (%)
Total N (%)
C:N ratio
d C (%)
d N (%)
Total C (%)
Total N (%)
C:N ratio
d13C (%)
d15N (%)
Total C (%)
Total N (%)
C:N ratio
NF 1R
27.4a 27.2a
6.4a 4.9b
37.6a 38.6a
1.7a 1.2b
23.0b 32.1a
27.5b 26.9a
5.5a 3.2b
37.9b 42.3a
1.4a 0.64b
27.8b 69.1a
26.3a 26.5a
1.3b 2.9a
38.7b 46.0a
1.4a 0.7b
11.8b 13.7a
Values are means (n ¼ 5) and if followed by the same letter are not significant at the 5% level of significance.
Table 3 Gross and net N mineralisation, ammonification and NH+ 4 consumption rates from adjacent native forest (NF), 53 y-old first rotation hoop pine plantation (1R), 5 y-old second rotation tree row (2R-T) and second rotation windrow (2R-W) at the Yarraman site, subtropical Australia Forest type
NF 1R 2R-T 2R-W
Anaerobic incubation
Aerobic incubation
Gross mineralisation (mg N kg1 d1)
NH+ 4 consumption (mg N kg1 d1)
Net mineralisation (mg N kg1 d1)
Gross ammonification (mg N kg1 d1)
NH+ 4 consumption (mg N kg1 d1)
Net ammonification (mg N kg1 d1)
9.1a 3.5c 7.2ab 6.7b
3.68a 0.23c 4.01a 2.32b
5.9a 3.3bc 2.6c 4.0b
0.74b 0.62b 1.78a 1.50a
0.97b 0.82b 2.12a 1.80a
0.27a 0.21a 0.20a 0.20a
Values are means (n ¼ 5) and if followed by the same letter are not significant at the 5% level of significance.
the NF and 1R sites (Table 2). Total C and d13C values in the L-layer were lower at the NF site compared to the 1R site. Both the F- and L-layers at the NF site had significantly higher total N and d15N values than those of the 1R site. Roots at the NF site were also found to have lower total C and d15N but higher total N. The C:N ratios of both the F- and L-layers were significantly lower at the NF site than in the 1R site. Roots at the NF site also had significantly lower C:N ratio. Soil C:N ratios were positively correlated to the C:N ratios of the L-layer (r ¼ 0.76, Po0.01), F-layer (r ¼ 0.66, Po0.01) and roots (r ¼ 0.83, Po0.01). 3.3. Aerobic incubation Gross ammonification rates in the aerobic incubation ranged between 0.62 in the 1R soils and 1.78 mg N kg1 d1 in the 2R-T soils, whilst the rate of NH+ 4 consumption ranged between 0.82 in the 1R soils and 2.12 mg N kg1 d1 in the 2R-T soils (Table 3). Both gross ammonification and NH+ 4 consumption were significantly lower in the NF and the 1R soils compared to the 2R-T and the 2R-W soils. Net ammonification rates were all negative and no significant difference was found among the treatments (Table 3). Gross nitrification rates ranged between 2.1 mg N kg1 d1 (equivalent to 120 mg N m2 d1) in the 1R soil and 6.6 mg N kg1 d1 (equivalent to 345 mg N m2 d1) in the NF soil (Fig. 1). A paired t-test showed that the rate of gross nitrification was significantly higher than the rate of gross ammonification in all soils
(P ¼ 0.002) (Table 3, Fig. 1). Both net and gross nitrification rates were significantly higher in the NF soils than in the plantation soils. However, no significant differences in the nitrification rates were found between the 1R and the 2R plantations soils. Gross and net nitrification rates were negatively correlated to soil C:N ratio (r ¼ –0.66 and –0.59, respectively, Po0.01). 3.4. Anaerobic incubations The rate of gross N mineralisation in the anaerobic incubation ranged between 3.5 mg N kg1 d1 in the 1R soils and 9.1 mg N kg1 d1 in the NF soils (Table 3). The NF soils generally had higher rates of gross and net N mineralisation and NH+ 4 consumption than the plantation soils (Table 3). The 1R soils had significantly lower gross N mineralisation and NH+ 4 consumption rates than the 2R soils. Significant differences between the 2R-T soils and the 2R-W soils were found in the rates of NH+ 4 consumption and net N mineralisation. Gross and net N mineralisation were negatively correlated to soil C:N ratio (r ¼ 0.66 and –0.60, respectively, Po0.01). 4. Discussion The three adjacent sites used for this study were located on the same position of the slope, had the same vegetative cover prior to the establishment of hoop pine plantations, and the soils were developed from the same basaltic parent material. As such, differences in soil N transformations
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10
Gross nitrification Net nitrification Nitrate consumption
Nitrification (mg N kg-1 d-1)
8 6 4 2 0 NF
2R-T
1R
-2
2R-W
Forest type
-4 Fig. 1. Gross and net nitrification and NO 3 consumption rates in soils under adjacent native forest (NF), 53 y-old first rotation hoop pine plantation (1R), 5 y-old second rotation tree row (2R-T) and second rotation windrow (2R-W) at the Yarraman site, subtropical Australia.
among the sites are assumed to be the result of the land-use change and site management practices. Differences between the NF and the 1R soils may reflect the impact of the change in tree species, the ensuing difference in the quality of organic matter input, the effect of disturbance during 1R establishment and subsequent silvicultural practices, and changes in microclimate. While the difference between 1R and 2R hoop pine plantations may reflect the short-term impact of harvesting and site preparation on soil N transformations, as well as the effect of closed and open canopy on soil temperature. Any differences between 2R-T and 2R-W may reflect the impact of residue management practices. It is acknowledged that pseudo-replication is a limitation of this study and as such the experiment may be viewed as a case study. 4.1. Impacts of land-use change on soil N mineralisation and immobilisation Gross ammonification rates in the aerobic incubation were some of the lowest reported and were accompanied by relatively low concentrations of NH+ 4 . Similar rates have been reported in a mature forest soil in Alberta, Canada (Carmosini et al., 2002). However, gross ammonification rates one to two orders of magnitude higher have been reported by Grenon et al. (2004). Rates of gross ammonification and NH+ 4 consumption were similar in the NF and 1R soils, whilst rates of both processes were significantly higher in the 2R soils. Carmosini et al. (2002) also found that gross ammonification and immobilisation of NH+ 4 were higher in harvested soils compared to mature aspen-conifer mixed forest soils. Ammonification is sensitive to disturbance and has been found to increase as temperature increases (Carlyle, 1986; Frazer et al. 1990; Grenon et al. 2004). Therefore, it is not surprising to find similar rates of ammonification in the NF and 1R soils, as both ecosystems have been undisturbed for a substantial period of time. Also both ecosystems have closed canopies and as such, soil temperature is likely to be similar. The 2R forest, however, does not have a closed canopy and
disturbance in the form of harvesting and site preparation was relatively recent. As such, it is hypothesised that the stronger rate of ammonification in the 2R soils compared to the 1R soils may be the result of a pulse of increased mineralisation of native organic N caused by soil disturbance, as well as higher soil temperature due to the lack of a closed canopy. In the anaerobic incubation, gross and net N mineralisation, as well as NH+ consumption rates, were 4 comparable to rates measured by Wang et al. (2001) in 20 different soil types under waterlogged conditions. The NF soils had higher rates of gross N mineralisation and NH+ 4 consumption than the plantation soils, whilst the 1R soils had lower rates than the 2R soils. Research has shown that aerobic microbial biomass has the tendency to be lysed under anaerobic conditions, which subsequently increases the amount of labile C and N (Bundy and Meisinger, 1994; Wu and Brookes, 2005). Also, previous work at this site found that a larger microbial biomass was present in the NF soils as compared to the plantation soils (Chen et al., 2004). Hence, it is hypothesised that the differences in soil N transformations under waterlogged conditions partly reflect differences in microbial biomass among the treatments. The significant difference in the rates of NH+ 4 consumption and net N mineralisation under anaerobic conditions between the 2R-T and the 2R-W soil may also indicate differences in microbial biomass and available C and N as a result of residue management. Further investigations of microbial biomass under both tree rows and windrows would be necessary to substantiate this conclusion. 4.2. Impacts of land-use change on soil nitrification The change in land use from NF to forest plantations had an impact on net and gross nitrification, as well as the NO 3 pool, with rates and concentrations measured in the NF soil more than double those in the plantation soils (Fig. 1). However, no significant differences in rates of nitrification and the NO 3 pool were found among 1R,
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2R-T and 2R-W soils. Nitrification is a microbially mediated process and it is well established that the quality of organic matter input, a factor associated with land-use change, can affect the microbial community, and ultimately soil N transformations (Cote et al., 2000; Chen et al., 2004; Grenon et al., 2004). In this study, C:N ratios were significantly lower in NF litter (both F- and L- layer) and root material than in the 1R litter and root material (Table 2). Generally, it is accepted that lower C:N ratios are indicative of higher quality organic matter (Attiwill and Adams, 1993). Soil C:N ratios were positively correlated to L-layer, F-layer and root C:N ratios, whilst gross nitrification was negatively correlated to soil C:N ratio. Similar results were also found by Breuer et al. (2002) and Ross et al. (2004). In addition to the differences in organic matter quality, previous research at this study site found that microbial biomass was greater in the NF soils and that both bacterial and fungal group diversity was higher in the NF soil as compared with the plantation soils (Chen et al., 2004; He, 2004; He et al., 2005). Hence, it is possible that the conversion from a mixed species forest to a single species forest has changed the quality of organic matter input and subsequently microbial population and diversity, which has ultimately resulted in higher nitrification rates in the NF soils compared to the plantation soils. In general, gross nitrification rates, particularly for the NF soils, were amongst the highest reported and are comparable to rates found by Stark and Hart (1997), Neill et al. (1999) and Compton and Boone (2002). Such results indicate that nitrification is a strong and important process in these soils. While other researchers have found small NO 3 pools coinciding with high nitrification rates and attributed this to microbial assimilation, NO 3 concentrations in this study were high and consumption negative (Davidson et al., 1992; Stark and Hart, 1997) (Table 1 and Fig. 1). High concentrations of NO 3 at this particular site have been found by other workers (C.R. Chen, personal communication). Such results suggest that NO 3 is accumulating in these soils. There are a number of explanations, which may individually or collectively result in the high rates of nitrification as well as the accumulation of NO 3 in these soils. Research has established that root exudates can influence soil microbial activity and that exudates from different tree species can affect the composition of microbial populations (Grayston et al., 1997; Landi et al., 2006). It is therefore possible that root exudates in these forest systems favour nitrifying communities, leading to high rates of nitrification and large NO 3 pools. Also, it is likely that the dry conditions prevalent at this site may favour nitrification and prevent the loss of substantial quantities of NO 3 through leaching or denitrification. It is interesting to note that gross nitrification was stronger than gross ammonification in this study, particularly as many researchers have found the opposite to be true (Davidson et al., 1992; Silva et al., 2005). In the soil environment, nitrification can be carried out by both
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autotrophs and heterotrophs. Autotrophic nitrification is the process through which autotrophs convert inorganic NH+ 4 to NO3 , whereas heterotrophic nitrification is the conversion of organic N to NO by heterotrophs 3 (Stevenson and Cole, 1999). Although traditionally autotrophic nitrification is believed to be the dominant nitrification process, several studies have found heterotrophic nitrification in soils. For example, Schimel et al. (1984) found that the potential for heterotrophic nitrification in a Sierran forest soil was greater than the potential for autotrophic nitrification, whilst Grenon et al. (2004) found that heterotrophic nitrification accounted for 20–100% of total nitrification. Also, gross nitrification rates in excess of gross ammonification were reported by Accoe et al. (2005) for grassland soils. The higher rates of gross nitrification than gross ammonification measured under aerobic conditions in this study may indirectly indicate a significant role of heterotrophic nitrification in the N transformations of these soils. A high rate of heterotrophic nitrification would explain the high rate of nitrification that exists in these soils despite the relatively low ammonification rates and concentrations of NH+ 4 . If, as the data suggest, heterotrophic nitrification is dominant in these soils and the change in land-use has had a detrimental impact on this particular community, this may explain why nitrification is much stronger in the NF soils compared to the plantation soils despite having lower ammonification rates. 4.3. Comparison of aerobic and anaerobic results Wang et al. (2001) found that gross N mineralisation rates in aerobic and anaerobic incubations were well correlated and that gross N mineralisation in anaerobic incubations were not always higher. To the contrary, in this study, rates measured in the anaerobic incubation were consistently higher (with the exception of NH+ 4 consumption in the 1R soils) and not correlated to rates measured in the aerobic incubation (Table 3). The incubations in the study by Wang et al. (2001) were performed on air dried soil and hence results may be somewhat artificial as microbial population and activity are affected by air drying and rewetting processes (Fierer and Schimel, 2002; De Nobili et al., 2006). In this study, the higher rates of N mineralisation in the anaerobic incubation are likely attributed to increased labile organic N and C as a result of lysis of aerobic microbial biomass under waterlogged conditions (Bundy and Meisinger, 1994; Wu and Brookes, 2005). Also, it is expected that microbes at this site are suited to the prevailing dry conditions and therefore may consist largely of aerobes, which would undergo lysis in anaerobic conditions. In a particularly dry site such as this, the anaerobic results may not be as useful as aerobic results for predicting actual N transformations. However, the results of the anaerobic incubation provide a useful index of the impact of land-use change on soil N transformations and availability.
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4.4. Comparison of net and gross transformation rates In both aerobic and anaerobic incubations, soil net N transformations were underestimated compared with the gross rates. Similar results have been found by other researchers who have also concluded that soil net N transformation rates are only useful as an index of N availability (Hart et al., 1994a; Schimel and Bennett, 2004). In the aerobic incubation, rates of net ammonification were negative for all the soils and no significant difference was found among the forest sites. Silva et al. (2005) also found no differences in net N transformation rates between forest ecosystems, but differences in gross N transformation rates were detected between the ecosystems. This suggests that gross N transformation measurements may be a more sensitive indicator of land-use change than the net N transformation rates and also that factors controlling N consumption and production do not equally affect these processes (Hart et al., 1994a). 5. Conclusion Results of the aerobic incubation suggest that the change in land-use from NF to 1R hoop pine plantation had no effect on ammonification and NH+ 4 consumption rates. However, it did result in a significant decline in the rate of nitrification. In contrast, the land-use change from 1R hoop pine plantation to 2R hoop pine plantation increased the rate of ammonification, but had little effect on rates of nitrification. Differences in N transformations between the NF and 1R soils may be caused by the shift in tree species and quality of organic matter input, which has subsequently caused changes in the size and diversity of the soil microbial community. Whilst differences in N transformations between the 1R and 2R soils may be a reflection of time since disturbance and differences in soil temperature. Results of the aerobic incubation also found that in the fifth year of the 2R hoop pine plantation, residue management practices did not affect soil N transformations. Nitrification was found to be the dominant N transformation process in these soils, despite relatively low NH+ 4 concentrations and rates of ammonification. The significantly higher rates of nitrification compared to ammonification suggests that heterotrophic nitrification may be significant. Future studies focusing on characterisation of litter and microbial communities as well as root exudates would enhance our understanding of the factors controlling soil N transformations in these ecosystems. Acknowledgements For allowing us access to the experimental site, we acknowledge Forestry Plantations Queensland and in particular Mr. Richard Jackson. We would like to thank Dr. Rui Yin, Mr. Yu Huang, Ms. Elizabeth Bridon and Mr. Stephen Faggotter for their assistance in soil sampling and processing. We also thank Mr. Rene Diocares for
technical assistance, Associate Professor Janet Chaseling for statistical advice and Dr. Weijin Wang for discussion of the data.
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Reich, P., Grigal, D., Aber, J., Gower, S., 1997. Nitrogen mineralisation and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78, 335–347. Ross, D.S., Lawrence, G.B., Fredriksen, G., 2004. Mineralization and nitrification patterns at eight northeastern USA forested research sites. Forest Ecology and Management 188, 317–335. Schimel, J., Bennett, J., 2004. Nitrogen mineralisation: challenges of a changing paradigm. Ecology 85, 591–602. Schimel, J., Firestone, M., Killham, K., 1984. Identification of heterotrophic nitrification in a Sierran forest soil. Applied and Environmental Microbiology 48, 802–806. Silva, R., Jorgensen, E., Holub, S., Gonsoulin, M., 2005. Relationships between culturable soil microbial populations and gross nitrogen transformation processes in a clay loam soil across ecosystems. Nutrient Cycling in Agroecosystems 71, 259–270. Soil Survey Staff, 1999. Soil Taxonomy a Basic System of Soil Classification for Making and Interpreting Soil Surveys. USDA Soil Conservation Service, Washington, DC, 600pp. Stark, J.M., Hart, S.C., 1997. High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385, 61–64. Ste-Marie, C., Houle, D., 2006. Forest floor gross and net nitrogen mineralization in three forest types in Quebec, Canada. Soil Biology & Biochemistry 38, 2135–2143. Stevenson, F., Cole, M., 1999. Cycles of Soil:Carbon, Nitrogen, Phosphorus, Sulfur, and Micronutrients. Wiley, New York, 427pp. Tan, X., Chang, S.X., Kabzems, R., 2005. Effects of soil compaction and forest floor removal on soil microbial properties and N transformations in a boreal forest long-term soil productivity study. Forest Ecology and Management 217, 158–170. Templer, P., Findlay, S., Lovett, G., 2003. Soil microbial biomass and nitrogen transformations among five tree species of the Catskill Mountains, New York, USA. Soil Biology & Biochemistry 35, 607–613. Van Miegroet, H., Cole, D., 1988. The influence of N—fixing alder on acidification and cation leaching from a forest soil. In: Cole, D., Gessel, S. (Eds.), Forest Site Evaluation and Long-term Productivity. University of Washington Press, pp. 113–125. Verchot, L.V., Holmes, Z., Mulon, L., Groffman, P.M., Lovett, G.M., 2001. Gross vs. net rates of N mineralization and nitrification as indicators of functional differences between forest types. Soil Biology & Biochemistry 33, 1889–1901. Wang, W.J., Chalk, P.M., Chen, D., Smith, C.J., 2001. Nitrogen mineralisation, immobilisation and loss, and their role in determining differences in net nitrogen production during waterlogged and aerobic incubation of soils. Soil Biology & Biochemistry 33, 1305–1315. Wu, J., Brookes, P.C., 2005. The proportional mineralisation of microbial biomass and organic matter caused by air-drying and rewetting of a grassland soil. Soil Biology & Biochemistry 37, 507–515.
Soil Biology & Biochemistry 39 (2007) 426–433 www.elsevier.com/locate/soilbio
Gross nitrogen transformations in adjacent native and plantation forests of subtropical Australia Joanne Burtona,b,c,, Chengrong Chenb, Zhihong Xub, Hossein Ghadiria,c a
Faculty of Environmental Sciences, Griffith University, Nathan 4111, Australia Centre for Forestry and Horticultural Research, Faculty of Science, Griffith University, Nathan 4111, Australia c Centre for Riverine Landscapes, Faculty of Environmental Science, Griffith University, Nathan 4111, Australia
b
Received 22 June 2006; received in revised form 3 August 2006; accepted 11 August 2006 Available online 18 September 2006
Abstract The impact of land-use change on soil nitrogen (N) transformations was investigated in adjacent native forest (NF), 53 y-old first rotation (1R) and 5 y-old second rotation (2R) hoop pine (Araucaia cunninghamii) plantations. The 15N isotope dilution method was used to quantify gross rates of N transformations in aerobic and anaerobic laboratory incubations. Results showed that the land-use change had a significant impact on the soil N transformations. Gross ammonification rates in the aerobic incubation ranged between 0.62 and 1.78 mg N kg1 d1, while gross nitrification rates ranged between 2.1 and 6.6 mg N kg1 d1. Gross ammonification rates were significantly lower in the NF and the 1R soils than in the 2R soils, however gross nitrification rates were significantly higher in the NF soils than in the plantation soils. The greater rates of gross nitrification found in the NF soil compared to the plantation soils, were related to lower soil C:N ratios (i.e. more labile soil N under NF). Nitrification was found to be the dominant soil N transformation process in the contrasting forest ecosystems. This might be attributed to certain site conditions which may favour the nitrifying community, such as the dry climate and tree species. There was some evidence to suggest that heterotrophic nitrifiers may undertake a significant portion of nitrification. r 2006 Elsevier Ltd. All rights reserved. Keywords: Gross N mineralisation; Gross nitrification; Anaerobic and aerobic incubation; C:N ratio; Land-use change
1. Introduction As a result of growing demands for forest products and a reduced forest land base, the Australian forestry industry is becoming increasingly reliant on single tree species plantations to meet its timber needs. At present in Queensland, Australia, about 216,500 ha are devoted to both exotic pine and native species plantations which supply a large proportion of the timber inputs for the Queensland forestry industry (QDPI and F, 2006). In order to maintain the long-term productivity of these forest soils, and hence a sustainable forestry industry, it is essential to understand
Corresponding author. Faculty of Environmental Sciences, Griffith University, Nathan Campus, Kessels Road Nathan, Brisbane, Qld. 4111, Australia. Tel.: +61 7 3735 3638; fax: +61 7 3735 7459. E-mail address: J.Burton@griffith.edu.au (J. Burton).
0038-0717/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2006.08.011
the impact of land-use change from native forest (NF) to forest plantations on soil nutrient cycling. Nitrogen (N) is an essential element for plant growth and N deficiency frequently limits forest productivity (Binkley and Hart, 1989; Paul and Clark, 1989; Reich et al., 1997). Soil N transformations are microbially mediated processes, which are influenced by a number of factors, including composition and diversity of the soil microbial community, substrate quality and quantity, and environmental conditions (Stevenson and Cole, 1999; Compton and Boone, 2002; Templer et al., 2003; Grenon et al., 2004). These factors are likely to be influenced by land-use change. For instance, land-use change from NF to plantation forest results in a shift in plant species, which directly influences the quality and quantity of organic matter input from both plant residues and root exudates. This in turn may lead to changes in soil microbial communities, which subsequently influence soil N transformations (Van Miegroet and Cole,
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1988; Verchot et al., 2001; Ross et al., 2004; Patra et al., 2006; Ste-Marie and Houle, 2006). Land-use change also causes disturbance to the soil ecosystem through harvesting and site preparation, which may have an impact on soil microbial communities and subsequently N availability and long-term site productivity (Cole, 1995; McMurtrie and Dewar, 1997; O’Connell et al., 2004; Tan et al., 2005). Finally, environmental conditions such as temperature and moisture also influence soil N transformations, particularly losses of N from the soil through leaching or denitrification. To date, a large proportion of research into soil N dynamics has been conducted in the northern hemisphere, where N deposition is an issue affecting soil N transformations and the climate is quite different from that in south east Queensland, Australia (Ross et al., 2004; Ste-Marie and Houle, 2006). Hence, there is a paucity of information relating to gross N transformations in subtropical forest soils. Furthermore, the effect of land-use change from NF to plantation forest and subsequent rotations on soil N transformations in subtropical zones has not been well studied. Hoop pine (Araucaia cunninghamii) is an N demanding native rainforest species of south east Queensland. At present, hoop pine plantations account for approximately one quarter of Queensland’s plantation area (50,000 ha) and most of the current plantations were established on land which was previously NF. The objective of this study was to examine the impact of land-use change from NF to first rotation (1R) hoop pine plantation and subsequent second rotation (2R) hoop pine plantation on soil N transformations in subtropical Australia. 2. Materials and methods 2.1. Site description and sample collection This study was conducted in Yarraman State Forest, south east Queensland, Australia (261520 S, 1511510 E). Details of the study area were provided by Chen et al. (2004). In brief, annual rainfall at this site ranges between 433 and 1110 mm, with an average of 816 mm. The soil was a Typic Durustalf (Soil Survey Staff, 1999), with a clayey texture (Chen et al., 2004). The NF site is classified as a mixed rainforest/scrub and is dominated by bunya pine (Araucaria bidwilli Hook.), yellowwood (Terminalia oblongata F. Muell. Suubsp. Oblongata), crows ash (Pentaceras australis R.B) and lignum-vitae (Premna lignum-vitae), with emergent hoop pine (Araucaria cunninghamii Aiton ex A. Cunn.). Experimental sites measuring 0.2 ha in area were located in adjacent NF, 1R hoop pine plantation (53 y-old) and 2R hoop pine plantation (5 y-old). Both the 1R and 2R hoop pine plantation sites were converted from NF in 1952. The first rotation of hoop pine at the 2R site was clearfall harvested in 1999, and post harvest residues from the first rotation plantation were formed into windrows approximately 6 m apart,
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using a D6 bulldozer with shear blade. The areas between windrows were then used as tree-planting rows for the 2R hoop pine plantation. Hence, the 2R plantation experimental area was divided into two treatments based on the residue management practices. These were: (1) tree planting row (2R-T) and (2) windrow of harvest residues (2R-W). A buffer area of at least 100 m was left between experimental areas to avoid edge effects. Each of the four treatments had five 24 m2 replicate plots. Fifteen soil cores (0–10 cm) were randomly collected from each plot using a 7.5 cm diameter auger and bulked. Litter (L) layer and fermentation (F) layer samples were collected from the plots at the NF and 1R sites using a 0.25 m2 steel quadrat. Five samples were taken from each plot and bulked together. Humus layer was not clearly distinguished in either the NF or plantation forests. All samples were transported to the laboratory where field moist soils were well mixed and passed through a o2 mm sieve and stored at 4 1C until the 15N isotope dilution study could be conducted. Roots, separated from soil during sieving, and litter samples were dried at 50 1C. A subsample of each soil was air-dried for chemical analysis. 2.2. Aerobic and anaerobic incubations Gross and net ammonification, nitrification and ammonium and nitrate consumption rates were determined in a 3-d aerobic incubation using the 15N pool dilution method (Hart et al., 1994b). Traditionally, anaerobic incubations have been used as an index of N mineralisation and availability (Keeney, 1982). They are also useful in terms of understanding N transformation processes which may occur in soils that are subjected to anaerobic conditions during periods of rainfall, as well as predicting N transformations which may occur in anaerobic microsites within the soil. As such, anaerobic incubations were also conducted using the 15N pool dilution method to determine gross and net mineralisation and ammonium consumption rates. Prior to the aerobic incubation, six portions of the field moist soils (5 g dry weight equivalent) were weighed into 50 ml propylene falcon tubes. The soil moisture was then adjusted to 45% of the water holding capacity and samples were conditioned at 25 1C for 24 h in a humid environment to ensure that they would not dry out. After conditioning, two soil samples were labelled with 600 ml of either (15NH4)2SO4 solution (4.76 mg N; ca. 98 at% 15N excess), or K15NO3 solution (15 mg N; ca. 99 at% 15N excess), which were applied evenly to the samples. An equivalent volume of distilled water was applied to another two soil samples, to be used as the control. Average soil moisture content of all samples after this addition was approximately 65% of the water holding capacity. Tubes were then capped and placed into the incubator at 25 1C. After 3 h, as suggested in Murphy et al. (2003), the time zero (T0) samples were removed from the incubator and extracted with 50 ml of 2 M KCl.
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Samples were shaken for 1 h, centrifuged at 2000 rpm for 10 min and then filtered through Whatman No. 42 filter paper and frozen until analysis. The remaining samples (T1) were removed from the incubator after 72 h and extracted as above. For the anaerobic incubation, four portions of field moist soils were prepared and conditioned as above. After conditioning, two soil samples were labelled with 25 ml of (15NH4)2SO4 solution (4.76 mg N; ca. 98 at% 15N excess). The equivalent volume of distilled water was added to another two samples of fresh soil, to be used as the control. Tubes were shaken gently for 3 min and then placed into the incubator at 25 1C. After 3 h, the T0 samples were removed from the incubator and extracted with 25 ml of 4 M KCl, so that the final ratio of soil:extract as well as the concentration of the KCl extract was equivalent to that used for the aerobic incubation. Samples were shaken for 1 h, centrifuged at 2000 rpm for 10 min and then filtered through Whatman No. 42 filter paper and frozen until further analysis could take place. The T1 samples were removed from the incubator after 72 h and extracted as above. 2.3. Steam distillation and chemical analysis Mineral N (NH+ 4 –N and NO3 –N) concentrations in the extracts were determined using a LACHAT Quickchem Automated Ion Analyser (QuikChem Method 10-107-0604-D for NH+ 4 –N and QuikChem Method 12-107-04-1-B 15 for NO N analysis using 3 –N). Samples were prepared for steam distillation (Keeney and Nelson, 1982). In brief, each extract was spiked with a known NH+ 4 and NO3 standard to provide sufficient total N for analysis. We then added 10 ml of 3.5% NaOH to convert the NH+ 4 to NH3 gas, and steam distilled the sample. The NH3 gas was collected in 10 ml of 2% HCl. Subsequently, 0.2 mg of Devarda’s alloy + was added to reduce the NO 3 to NH4 and the sample was redistilled with the NO3 collected in the form of NH3 in 10 ml of 2% HCl. Distillates were dried down at 50 1C, and isotope ratio analyses were performed using an isotope ratio mass spectrometer with a Eurovector elemental analyser (Isoprime-EuroEA 3000). Soil, root and litter total carbon (C) and N as well as carbon isotope composition (d13C) and 15N natural abundance (d15N) were also measured using the mass spectrometer.
2.4. Calculations and statistical analysis Rates of N mineralisation and ammonium consumption (for anaerobic incubation data), and ammonification, nitrification and ammonium consumption (for aerobic incubation data) were calculated using the equations developed by Kirkham and Bartholomew (1954), and presented in Hart et al. (1994b). One-way analysis of variance (ANOVA) was carried out for all data in Statistix for Window version 2.2 (Analytical Software, Tallahassee, FL). We acknowledge that a limitation of this study, as with many other paired-site studies, was the pseudoreplication used for ANOVA. Least significant difference (LSD, Po0.05) was used to separate treatment means when differences were significant. Paired t-tests and Pearson linear correlations were also conducted in Statistix for Windows version 2.2. 3. Results 3.1. Soil chemical properties Basic chemical properties of the soils under the adjacent NF, 1R, 2R-T and 2R-W are shown in Table 1. Soil total C and N were significantly higher in the NF soils than in the plantation soils. Total C was higher in the 1R soils than in the 2R soils. Concentrations of NH+ 4 were higher in the NF soils than in the plantation soils, while the concentration of NO 3 was approximately two times higher in the NF soils than in the plantation soils (Table 1). However, there was no significant difference in NH+ 4 and NO3 concentrations between the 1R and the 2R soils, or between the 2R-T and the 2R-W soils. The same pattern was found for the d15N results, whilst d13C was higher in the 2R-T soils than in the NF soils. The C:N ratios ranged between 11.8 in the NF soils and 13.7 in the 1R soils. The NF soils had significantly lower C:N ratios than the plantation soils, while the 1R soils had significantly higher C:N ratios than the 2R soils. Both pH and cation exchange capacity (CEC) differed among the different treatments. 3.2. Characteristics of forest litter material and tree roots Total C and total N contents and d13C and d15N values were measured on L- and F-layer, and root samples from
Table 1 Soil properties for adjacent native forest (NF), 53 y-old first rotation hoop pine plantation (1R), 5 y-old second rotation tree row (2R-T) and second rotation windrow (2R-W) at the Yarraman site, subtropical Australia Forest type
pH (1:2.5 H2O)
CEC (C mol kg1)
Total C (%)
Total N (%)
C:N ratio
d13C (%)
d15N (%)
NH+ 4 (mg N kg1)
NO 3 (mg N kg1)
NF 1R 2R-T 2R-W
6.2b 6.6a 6.0c 6.2b
56.9a 50.9a 38.0b 36.5b
8.9a 7.1b 5.8c 6.1c
0.75a 0.52b 0.46b 0.47b
11.8c 13.7a 12.6b 12.9b
25.8b 25.7ab 25.5a 25.7ab
9.8a 8.9b 8.3b 8.6b
2.5a 2.1b 2.1b 2.2b
98.6a 43.8b 43.1b 58.5b
Values are means (n ¼ 5) and if followed by the same letter are not significant at the 5% level of significance.
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Table 2 Basic chemical properties of litter (L) and fermentation (F) layer of adjacent native forest (NF) and 53 y-old first rotation hoop pine plantation (1R) at the Yarraman site, subtropical Australia Fermentation layer 13
15
Litter layer 13
15
Roots (0–10 cm)
Forest type
d C (%)
d N (%)
Total C (%)
Total N (%)
C:N ratio
d C (%)
d N (%)
Total C (%)
Total N (%)
C:N ratio
d13C (%)
d15N (%)
Total C (%)
Total N (%)
C:N ratio
NF 1R
27.4a 27.2a
6.4a 4.9b
37.6a 38.6a
1.7a 1.2b
23.0b 32.1a
27.5b 26.9a
5.5a 3.2b
37.9b 42.3a
1.4a 0.64b
27.8b 69.1a
26.3a 26.5a
1.3b 2.9a
38.7b 46.0a
1.4a 0.7b
11.8b 13.7a
Values are means (n ¼ 5) and if followed by the same letter are not significant at the 5% level of significance.
Table 3 Gross and net N mineralisation, ammonification and NH+ 4 consumption rates from adjacent native forest (NF), 53 y-old first rotation hoop pine plantation (1R), 5 y-old second rotation tree row (2R-T) and second rotation windrow (2R-W) at the Yarraman site, subtropical Australia Forest type
NF 1R 2R-T 2R-W
Anaerobic incubation
Aerobic incubation
Gross mineralisation (mg N kg1 d1)
NH+ 4 consumption (mg N kg1 d1)
Net mineralisation (mg N kg1 d1)
Gross ammonification (mg N kg1 d1)
NH+ 4 consumption (mg N kg1 d1)
Net ammonification (mg N kg1 d1)
9.1a 3.5c 7.2ab 6.7b
3.68a 0.23c 4.01a 2.32b
5.9a 3.3bc 2.6c 4.0b
0.74b 0.62b 1.78a 1.50a
0.97b 0.82b 2.12a 1.80a
0.27a 0.21a 0.20a 0.20a
Values are means (n ¼ 5) and if followed by the same letter are not significant at the 5% level of significance.
the NF and 1R sites (Table 2). Total C and d13C values in the L-layer were lower at the NF site compared to the 1R site. Both the F- and L-layers at the NF site had significantly higher total N and d15N values than those of the 1R site. Roots at the NF site were also found to have lower total C and d15N but higher total N. The C:N ratios of both the F- and L-layers were significantly lower at the NF site than in the 1R site. Roots at the NF site also had significantly lower C:N ratio. Soil C:N ratios were positively correlated to the C:N ratios of the L-layer (r ¼ 0.76, Po0.01), F-layer (r ¼ 0.66, Po0.01) and roots (r ¼ 0.83, Po0.01). 3.3. Aerobic incubation Gross ammonification rates in the aerobic incubation ranged between 0.62 in the 1R soils and 1.78 mg N kg1 d1 in the 2R-T soils, whilst the rate of NH+ 4 consumption ranged between 0.82 in the 1R soils and 2.12 mg N kg1 d1 in the 2R-T soils (Table 3). Both gross ammonification and NH+ 4 consumption were significantly lower in the NF and the 1R soils compared to the 2R-T and the 2R-W soils. Net ammonification rates were all negative and no significant difference was found among the treatments (Table 3). Gross nitrification rates ranged between 2.1 mg N kg1 d1 (equivalent to 120 mg N m2 d1) in the 1R soil and 6.6 mg N kg1 d1 (equivalent to 345 mg N m2 d1) in the NF soil (Fig. 1). A paired t-test showed that the rate of gross nitrification was significantly higher than the rate of gross ammonification in all soils
(P ¼ 0.002) (Table 3, Fig. 1). Both net and gross nitrification rates were significantly higher in the NF soils than in the plantation soils. However, no significant differences in the nitrification rates were found between the 1R and the 2R plantations soils. Gross and net nitrification rates were negatively correlated to soil C:N ratio (r ¼ –0.66 and –0.59, respectively, Po0.01). 3.4. Anaerobic incubations The rate of gross N mineralisation in the anaerobic incubation ranged between 3.5 mg N kg1 d1 in the 1R soils and 9.1 mg N kg1 d1 in the NF soils (Table 3). The NF soils generally had higher rates of gross and net N mineralisation and NH+ 4 consumption than the plantation soils (Table 3). The 1R soils had significantly lower gross N mineralisation and NH+ 4 consumption rates than the 2R soils. Significant differences between the 2R-T soils and the 2R-W soils were found in the rates of NH+ 4 consumption and net N mineralisation. Gross and net N mineralisation were negatively correlated to soil C:N ratio (r ¼ 0.66 and –0.60, respectively, Po0.01). 4. Discussion The three adjacent sites used for this study were located on the same position of the slope, had the same vegetative cover prior to the establishment of hoop pine plantations, and the soils were developed from the same basaltic parent material. As such, differences in soil N transformations
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10
Gross nitrification Net nitrification Nitrate consumption
Nitrification (mg N kg-1 d-1)
8 6 4 2 0 NF
2R-T
1R
-2
2R-W
Forest type
-4 Fig. 1. Gross and net nitrification and NO 3 consumption rates in soils under adjacent native forest (NF), 53 y-old first rotation hoop pine plantation (1R), 5 y-old second rotation tree row (2R-T) and second rotation windrow (2R-W) at the Yarraman site, subtropical Australia.
among the sites are assumed to be the result of the land-use change and site management practices. Differences between the NF and the 1R soils may reflect the impact of the change in tree species, the ensuing difference in the quality of organic matter input, the effect of disturbance during 1R establishment and subsequent silvicultural practices, and changes in microclimate. While the difference between 1R and 2R hoop pine plantations may reflect the short-term impact of harvesting and site preparation on soil N transformations, as well as the effect of closed and open canopy on soil temperature. Any differences between 2R-T and 2R-W may reflect the impact of residue management practices. It is acknowledged that pseudo-replication is a limitation of this study and as such the experiment may be viewed as a case study. 4.1. Impacts of land-use change on soil N mineralisation and immobilisation Gross ammonification rates in the aerobic incubation were some of the lowest reported and were accompanied by relatively low concentrations of NH+ 4 . Similar rates have been reported in a mature forest soil in Alberta, Canada (Carmosini et al., 2002). However, gross ammonification rates one to two orders of magnitude higher have been reported by Grenon et al. (2004). Rates of gross ammonification and NH+ 4 consumption were similar in the NF and 1R soils, whilst rates of both processes were significantly higher in the 2R soils. Carmosini et al. (2002) also found that gross ammonification and immobilisation of NH+ 4 were higher in harvested soils compared to mature aspen-conifer mixed forest soils. Ammonification is sensitive to disturbance and has been found to increase as temperature increases (Carlyle, 1986; Frazer et al. 1990; Grenon et al. 2004). Therefore, it is not surprising to find similar rates of ammonification in the NF and 1R soils, as both ecosystems have been undisturbed for a substantial period of time. Also both ecosystems have closed canopies and as such, soil temperature is likely to be similar. The 2R forest, however, does not have a closed canopy and
disturbance in the form of harvesting and site preparation was relatively recent. As such, it is hypothesised that the stronger rate of ammonification in the 2R soils compared to the 1R soils may be the result of a pulse of increased mineralisation of native organic N caused by soil disturbance, as well as higher soil temperature due to the lack of a closed canopy. In the anaerobic incubation, gross and net N mineralisation, as well as NH+ consumption rates, were 4 comparable to rates measured by Wang et al. (2001) in 20 different soil types under waterlogged conditions. The NF soils had higher rates of gross N mineralisation and NH+ 4 consumption than the plantation soils, whilst the 1R soils had lower rates than the 2R soils. Research has shown that aerobic microbial biomass has the tendency to be lysed under anaerobic conditions, which subsequently increases the amount of labile C and N (Bundy and Meisinger, 1994; Wu and Brookes, 2005). Also, previous work at this site found that a larger microbial biomass was present in the NF soils as compared to the plantation soils (Chen et al., 2004). Hence, it is hypothesised that the differences in soil N transformations under waterlogged conditions partly reflect differences in microbial biomass among the treatments. The significant difference in the rates of NH+ 4 consumption and net N mineralisation under anaerobic conditions between the 2R-T and the 2R-W soil may also indicate differences in microbial biomass and available C and N as a result of residue management. Further investigations of microbial biomass under both tree rows and windrows would be necessary to substantiate this conclusion. 4.2. Impacts of land-use change on soil nitrification The change in land use from NF to forest plantations had an impact on net and gross nitrification, as well as the NO 3 pool, with rates and concentrations measured in the NF soil more than double those in the plantation soils (Fig. 1). However, no significant differences in rates of nitrification and the NO 3 pool were found among 1R,
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2R-T and 2R-W soils. Nitrification is a microbially mediated process and it is well established that the quality of organic matter input, a factor associated with land-use change, can affect the microbial community, and ultimately soil N transformations (Cote et al., 2000; Chen et al., 2004; Grenon et al., 2004). In this study, C:N ratios were significantly lower in NF litter (both F- and L- layer) and root material than in the 1R litter and root material (Table 2). Generally, it is accepted that lower C:N ratios are indicative of higher quality organic matter (Attiwill and Adams, 1993). Soil C:N ratios were positively correlated to L-layer, F-layer and root C:N ratios, whilst gross nitrification was negatively correlated to soil C:N ratio. Similar results were also found by Breuer et al. (2002) and Ross et al. (2004). In addition to the differences in organic matter quality, previous research at this study site found that microbial biomass was greater in the NF soils and that both bacterial and fungal group diversity was higher in the NF soil as compared with the plantation soils (Chen et al., 2004; He, 2004; He et al., 2005). Hence, it is possible that the conversion from a mixed species forest to a single species forest has changed the quality of organic matter input and subsequently microbial population and diversity, which has ultimately resulted in higher nitrification rates in the NF soils compared to the plantation soils. In general, gross nitrification rates, particularly for the NF soils, were amongst the highest reported and are comparable to rates found by Stark and Hart (1997), Neill et al. (1999) and Compton and Boone (2002). Such results indicate that nitrification is a strong and important process in these soils. While other researchers have found small NO 3 pools coinciding with high nitrification rates and attributed this to microbial assimilation, NO 3 concentrations in this study were high and consumption negative (Davidson et al., 1992; Stark and Hart, 1997) (Table 1 and Fig. 1). High concentrations of NO 3 at this particular site have been found by other workers (C.R. Chen, personal communication). Such results suggest that NO 3 is accumulating in these soils. There are a number of explanations, which may individually or collectively result in the high rates of nitrification as well as the accumulation of NO 3 in these soils. Research has established that root exudates can influence soil microbial activity and that exudates from different tree species can affect the composition of microbial populations (Grayston et al., 1997; Landi et al., 2006). It is therefore possible that root exudates in these forest systems favour nitrifying communities, leading to high rates of nitrification and large NO 3 pools. Also, it is likely that the dry conditions prevalent at this site may favour nitrification and prevent the loss of substantial quantities of NO 3 through leaching or denitrification. It is interesting to note that gross nitrification was stronger than gross ammonification in this study, particularly as many researchers have found the opposite to be true (Davidson et al., 1992; Silva et al., 2005). In the soil environment, nitrification can be carried out by both
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autotrophs and heterotrophs. Autotrophic nitrification is the process through which autotrophs convert inorganic NH+ 4 to NO3 , whereas heterotrophic nitrification is the conversion of organic N to NO by heterotrophs 3 (Stevenson and Cole, 1999). Although traditionally autotrophic nitrification is believed to be the dominant nitrification process, several studies have found heterotrophic nitrification in soils. For example, Schimel et al. (1984) found that the potential for heterotrophic nitrification in a Sierran forest soil was greater than the potential for autotrophic nitrification, whilst Grenon et al. (2004) found that heterotrophic nitrification accounted for 20–100% of total nitrification. Also, gross nitrification rates in excess of gross ammonification were reported by Accoe et al. (2005) for grassland soils. The higher rates of gross nitrification than gross ammonification measured under aerobic conditions in this study may indirectly indicate a significant role of heterotrophic nitrification in the N transformations of these soils. A high rate of heterotrophic nitrification would explain the high rate of nitrification that exists in these soils despite the relatively low ammonification rates and concentrations of NH+ 4 . If, as the data suggest, heterotrophic nitrification is dominant in these soils and the change in land-use has had a detrimental impact on this particular community, this may explain why nitrification is much stronger in the NF soils compared to the plantation soils despite having lower ammonification rates. 4.3. Comparison of aerobic and anaerobic results Wang et al. (2001) found that gross N mineralisation rates in aerobic and anaerobic incubations were well correlated and that gross N mineralisation in anaerobic incubations were not always higher. To the contrary, in this study, rates measured in the anaerobic incubation were consistently higher (with the exception of NH+ 4 consumption in the 1R soils) and not correlated to rates measured in the aerobic incubation (Table 3). The incubations in the study by Wang et al. (2001) were performed on air dried soil and hence results may be somewhat artificial as microbial population and activity are affected by air drying and rewetting processes (Fierer and Schimel, 2002; De Nobili et al., 2006). In this study, the higher rates of N mineralisation in the anaerobic incubation are likely attributed to increased labile organic N and C as a result of lysis of aerobic microbial biomass under waterlogged conditions (Bundy and Meisinger, 1994; Wu and Brookes, 2005). Also, it is expected that microbes at this site are suited to the prevailing dry conditions and therefore may consist largely of aerobes, which would undergo lysis in anaerobic conditions. In a particularly dry site such as this, the anaerobic results may not be as useful as aerobic results for predicting actual N transformations. However, the results of the anaerobic incubation provide a useful index of the impact of land-use change on soil N transformations and availability.
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4.4. Comparison of net and gross transformation rates In both aerobic and anaerobic incubations, soil net N transformations were underestimated compared with the gross rates. Similar results have been found by other researchers who have also concluded that soil net N transformation rates are only useful as an index of N availability (Hart et al., 1994a; Schimel and Bennett, 2004). In the aerobic incubation, rates of net ammonification were negative for all the soils and no significant difference was found among the forest sites. Silva et al. (2005) also found no differences in net N transformation rates between forest ecosystems, but differences in gross N transformation rates were detected between the ecosystems. This suggests that gross N transformation measurements may be a more sensitive indicator of land-use change than the net N transformation rates and also that factors controlling N consumption and production do not equally affect these processes (Hart et al., 1994a). 5. Conclusion Results of the aerobic incubation suggest that the change in land-use from NF to 1R hoop pine plantation had no effect on ammonification and NH+ 4 consumption rates. However, it did result in a significant decline in the rate of nitrification. In contrast, the land-use change from 1R hoop pine plantation to 2R hoop pine plantation increased the rate of ammonification, but had little effect on rates of nitrification. Differences in N transformations between the NF and 1R soils may be caused by the shift in tree species and quality of organic matter input, which has subsequently caused changes in the size and diversity of the soil microbial community. Whilst differences in N transformations between the 1R and 2R soils may be a reflection of time since disturbance and differences in soil temperature. Results of the aerobic incubation also found that in the fifth year of the 2R hoop pine plantation, residue management practices did not affect soil N transformations. Nitrification was found to be the dominant N transformation process in these soils, despite relatively low NH+ 4 concentrations and rates of ammonification. The significantly higher rates of nitrification compared to ammonification suggests that heterotrophic nitrification may be significant. Future studies focusing on characterisation of litter and microbial communities as well as root exudates would enhance our understanding of the factors controlling soil N transformations in these ecosystems. Acknowledgements For allowing us access to the experimental site, we acknowledge Forestry Plantations Queensland and in particular Mr. Richard Jackson. We would like to thank Dr. Rui Yin, Mr. Yu Huang, Ms. Elizabeth Bridon and Mr. Stephen Faggotter for their assistance in soil sampling and processing. We also thank Mr. Rene Diocares for
technical assistance, Associate Professor Janet Chaseling for statistical advice and Dr. Weijin Wang for discussion of the data.
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