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Rhizosphere effects on soil nutrient dynamics and microbial activity in an Australian tropical lowland rainforest.


In recent decades, there has been a growing realisation of the critical roles of soil biological processes and their interactions with aboveground communities in global biogeochemical cycles that influence climate, hydrology, and nutrient budgets (Mosier 1998; Wardle et al. 2004). The rhizosphere--the soil zone that surrounds and is influenced by plant roots--is a highly biologically active region of the soil profile (Kuzyakov 2002). Root growth, nutrient uptake, secretion, and litter deposition influence environmental stability and resource availability both for plants and for soil fauna and microbiota (Bais et al. 2006; Richardson et al. 2009). The rhizosphere therefore plays a critical role in the cycling of nutrients in vascular plant dominated ecosystems, and in their interactions with global biogeochemical cycles.

The influence of the rhizosphere upon nutrient cycling is enacted via a suite of interactions between plants and soil organisms. Root secretion and dead root tissue deposition present a substantial source of soil carbon (C) (Kuzyakov and Domanski 2000), promoting soil microbial activity and stimulating decomposition (Kuzyakov 2010). Alongside nitrogen (N) release from soil organic matter, root nodule, endophytic, and free-living [N.sub.2]-fixing bacteria also contribute to rhizospheric N acquisition (Franche et al. 2009). Acidic secretions by plant roots and rhizospheric microorganisms may solubilise nutrient ions immobilised in soil particles (Landeweert et al. 2001). Rhizospheric secretions may also mobilise phosphorus (P) via ligand exchange and cation chelation (Jones 1998). The proliferation of roots and associated microorganisms through the soil influences soil physical and hydrological properties (Hinsinger et al. 2009), in turn influencing soil biological resource availability. Rhizospheric effects on pH may also influence soil microbial activity. The balance of competitive uptake of soluble nutrients by plants and microorganisms (Priha and Smolander 2003), versus their release by decomposition, solubilisation, and plant and microbial excretion, will influence ambient concentrations of soluble nutrients in the rhizosphere.

Tropical rainforests cover <10% of the Earth's land surface (FAO 1993), and yet they account for a substantial proportion of the Earth's terrestrial biomass (Soepadmo 1993), net primary productivity (Malhi and Grace 2000), and biodiversity (Myers 1988). Via vast exchanges of energy, water, C, and nutrients, the productivity of forests in the Earth's tropics presents a major driving force in the regulation of the Earth's biogeochemical (Detwiler and Hall 1988; Hedin et al. 2009), hydrological (Poschl et al. 2010), and climatic (Bonan 2008) cycles.

Given the recognition of the critical role of rhizosphere processes in nutrient cycling and ecosystem stability, it is likely that rhizosphere processes in tropical rainforest systems form a major component of the biome's interactions with global processes. Very little is known, however, about the specific ecosystem functions of rhizosphere processes in rainforest soils, with few studies on rainforest soil ecology having distinguished between bulk and rhizosphere soil processes. Furthermore, studies of rhizosphere processes have mainly been conducted on individual species, commonly under controlled conditions, with few studies on rhizosphere processes in mixed-species communities in natural settings. Our study therefore aimed to investigate the strength of the influence of rhizosphere processes upon soil nutrient cycling in mixed-species, lowland tropical rainforest by comparing the nutrient status and microbial activity of soil immediately surrounding plant roots to that of bulk soil not immediately associated with roots. We hypothesised that soil microbial biomass and activity, total C and N concentrations, soluble organic C concentration, and soluble N generation would be higher in the rhizosphere soil than the surrounding bulk soil due to root deposition of C and N and its stimulatory effect upon rhizosphere microbial populations. We also expected differences in the concentrations of other elemental nutrients between the rhizosphere soil and bulk soil due to their solubilisation by rhizospheric secretion.

We collected rhizosphere and adjacent bulk soil from Australian lowland tropical rainforest at the Australian Government managed, Australian Canopy Crane research facility at Cape Tribulation, Far North Queensland. The site has facilitated a range of ecological research from canopy to forest floor (Stork 2007). By contributing to the understanding of belowground processes at this site, our study assists in providing a more holistic picture of the ecosystem scale functioning of tropical rainforest. To test our hypotheses we compared the C and N pool size, N mineralisation rate, microbial biomass C and N content, microbial respiratory C[O.sub.2] release and C substrate utilisation, and elemental nutrient profile of the rhizosphere soil with that of the surrounding bulk soil. The ratios of different elements in the environment provide insight into the status and drivers of ecological processes (Elser et al. 2000). We were interested, therefore, to test whether the stoichiometry of nutrient pools differed between the rainforest rhizosphere and bulk soils, and what this may reveal regarding biological resource availability and the influence of biological resource utilisation upon environmental conditions. Several biochemical pathways of soil N transformation, including ammonification, nitrification, denitrification, and ammonia volatilisation, discriminate against [sup.15]N (Hogberg 1997), driving soil [sup.15]N enrichment and associated [sup.15]N depletion of plant tissue. We therefore also measured the [delta][sup.15]N of the rainforest rhizosphere and bulk soils as an indication of rclative pathways of N input, transformation, and loss.

Materials and methods

Research site

The study site was within the Australian Canopy Crane Facility, at Cape Tribulation, 140km north of Cairns, Queensland, Australia (16[degrees]06' S, 145[degrees]27' E). The site elevation ranges from 31 to 55m above sea level. It lies within a semi-enclosed coastal basin formed by ridges running east-west to an upland massif (Grove et al. 2000). Annual rainfall is ~3500mm, with ~550mm in March and 80mm in August. The average daily temperature ranges from 22[degrees]C (July) to 28[degrees]C (January). The soil is alluvial and classified as a red clay loam podzol (Australian Soil Classification, Isbell 2002) with a metamorphic origin and has good drainage characteristics. The lowland rainforest at this site is complex mesophyll vine forest, with the most abundant families being Meliaccae, Euphorbiaceae, Lauraceae, Myrtaceae, and Apocynaceae and the most abundant species being Cleistanthus myrianthus Kurz, Alstonia scholaris (L.) R.Br., Myristica insipida R.Br., Normanbya normanbyi (W.Hill) L.H. Bailey, and Roclanghamia angustifolia (Benth.) Airy Shaw (Laidlaw et al. 2007). The area has been affected by intermittent disturbance caused by cyclones, and this is considered to play a key role in shaping the ecology of these lowland rainforests in North Queensland.

Soil sampling

Soil samples (0-0.10m) were randomly collected from five areas (10 by 20 [m.sup.2]) of the study site. Fifteen cores (75 mm in diameter) were sampled from each area. Rhizosphere soil samples were obtained using a conventional hand-shaking method (Hendriks and Jungk 1981). The soil adhering to the root surface after the gentle shaking was regarded as rhizosphere soil, while the remaining soil was considered as the bulk soil. Once separated, the rhizosphere or bulk soils from the 15 cores were mixed well to form a composite rhizosphere or a composite bulk sample from each sampling area. Field-moist soil samples were passed through a 2-mm sieve and stored at 4[degrees]C before analysis. Analyses of soluble chemistry and microbial properties were carried out on the fresh soils and a subsample of each soil was air-dried and ground (<150 [micro]m) for total element determination. Results were expressed on an oven-dry soil basis.

Soil chemical and biological analysis

Soluble organic C and total soluble N in 2M KCl extracts were measured by the high temperature catalytic oxidation method using a Shimadzu TOC-VCPH/CPN analyser (fitted with a TN unit) as described by Chen et al. (2005). Concentrations of soil inorganic N (N[H.sub.4+]-N, N[O.sub.3]-N) and soluble organic N were determined in 2 M KC1 extracts using methods described by Chen et al. (2005). Total C, N, and [delta][sup.15]N were analysed using an isotope ratio mass spectrometer with a Eurovector Elemental Analyser (Isoprime-EuroEA 3000, Milan, Italy). Total amounts of soil P, S, Na, B, Cu, Zn, Mo, K, My, Fe, Al, Ca, and Mn were determined using HN[O.sub.3]-H[Cl.sub.4] digestion, followed by a Varian Vista Pro ICPOES.

Soil net N mineralisation was determined by a 7-day anaerobic incubation under laboratory conditions as described by Waring and Bremner (1964). Soil microbial biomass C and N were measured by the chloroform fumigation-extraction method using an EC factor of 2.64 (Vance et al. 1987) and an EN factor of 2.22 (Brookes et al. 1985). Soil respiration was measured by aerobic incubation of field-moist soils (20 g ovendry equivalent) at 22[degrees]C in a 1-L sealed glass jar, and trapping C[O.sub.2] evolved from the soil in 0.1 M NaOH after 1, 3, 7, and 14 days (see Chen et al. 2000). The residual NaOH was titrated with 0.05 M HC1 to the phenolphthalein endpoint and C[O.sub.2] evolved was calculated from the difference in normality between NaOH blanks and samples. The C substrate utilisation patterns of the microbial communities in the rainforest rhizosphere and bulk soil were determined by [Biolog.sup.TM] assay. Soil pH was measured at a soil to water ratio of 1 : 2.5, and soil moisture content determined graimetrically.

Statistical analyses

All data were subject to the normality test, and the paired t-test (rhizospbere and bulk soils paired by sampling area) was used to compare the differences between the rhizosphere and bulk soils. Principal component analysis (PCA) on all data was carried out using Statistica Version 6.1 (Statsoft, Inc.).


Soil C pools

The concentrations of total C (Fig. la) and microbial biomass C (Fig. 1c) of the rhizosphere soil were significantly greater than for the bulk soil (P=0.010 and t=3.71, P-0.003 and t=5.12, respectively). The concentration of soluble organic C (Fig. 1b) also tended to be greater in the rhizosphere soil, although not significantly so (P=0.059, t=1.89).

Soil N pools

The total N concentration of the rhizospherc soil was significantly greater than that of the bulk soil (P=0.008, t=4.0; Fig. 2a). The total soluble N concentration of the rhizosphere soil was also significantly greater than for the bulk soil (P=0.002, t=6.1; Fig. 2b), driven by significantly greater concentrations of both soluble organic N (P=0.034, t=2.5; Fig. 2b) and soluble inorganic N (P=0.007, t=4.2; Fig. 2b). The difference in soluble inorganic N between the rhizosphere soil and bulk soil was driven primarily by ammonium, ammonium concentrations in the rhizosphere soil being 20 times greater than for the bulk soil (P=0.034, t=2.5; Fig. 2b), whereas there was no significant difference for nitrate (P=0.314, t=0.5; Fig. 2b). Potentially minerallisable N in the rhizosphere soil was four times greater than in the bulk soil (P=0.034, t=2.1; Fig. 2c), in keeping with the findings for soluble organic N. The mean [delta][sup.15]N value of the rhizosphere soil was significantly lower than that of the bulk soil (P=0.028, t=-2.7; Fig. 2d). There was no significant difference in the concentration of microbial biomass N between the rhizosphere and bulk soils (P=0.235, t=0.80; Fig. 2e).


Soil concentrations of other elemental nutrients

The concentrations of P, S, Na, Cu, Zn, K, Mg, and Ca were all significantly higher in the rhizosphere soil than the bulk soil (Table 1 ). No significant difference was found between bulk and rhizosphere soil for concentrations of Fe, Al, Mn, B, and Me (Table 1).

Soil microbial metabolic activity

The cumulative release of C[O.sub.2] from microbial respiration over the 2-week laboratory incubation was substantially greater for the rhizosphere soil than the bulk soil at all sampling dates (Fig. 3a), with the mean respiration rate of the rhizosphere soil over the 2-week incubation being nearly three times that of the bulk soil (P=0.057, t=2.01; Fig. 3b). In the [Biolog.sup.TM] assay of microbial C substrate use, the rhizosphere soil showed significantly greater average well colour development, sum of activity, substrate richness, and Shannon's diversity index than the bulk soil (Table 2). There was no significant difference in pH (P=0.129, t=1.3) and moisture (P=0.110, t-1.5) conditions for microbial activity between the bulk and rhizosphere soil, the mean (n=5) pH of the bulk and rhizosphere soil being 4.57 ([+ or -]s.e. 0.17) and 4.80 ([+ or -]s.e. 0.08), respectively, and the mean (n = 5) moisture content 34% ([+ or -]s.e. 0.04) and 37% ([+ or -]s.e. 0.05), respectively.


Stoichiometry of total soil C N, P, and S

The ratios of total C to N, P, and S in the rhizosphere soil were all greater than those in the bulk soil (significant for C : N and C : P only; Table 3), a product of the greater elevation of total C in rhizosphere soil above that in the bulk soil than the elevation of total N, P, and S. The ratio of total N to P was also found to be significantly greater for the rhizosphere soil than the bulk soil (Table 3), driven by the greater elevation of rhizosphere soil total N than total P, whereas no significant difference was found for total N to S ratio between the rhizosphere soil and bulk soil. The ratio of total P to S was found to be significantly lower in the rhizosphere soil than the bulk soil (Table 3), the elevation of S concentrations in the rhizosphere soil being greater than that of P.

Stoichiometry of soil C and N pools

Similar to the overall C to N ratios, the ratio of C to N bound in soil microbial biomass was significantly greater for the rhizosphere soil than the bulk soil (P=0.028, t=2.67; Fig. 4), driven by the elevated concentration of microbial biomass C in the rhizosphere soil. An opposite trend in C to N ratios was found for the soluble soil pools (Fig. 4). The ratio of soluble organic C to soluble inorganic N in the rhizosphere soil was significantly lower than in the bulk soil (P=0.028, t=-2.6), driven largely by the substantially elevated concentration of ammonium in the rhizosphere soil. The ratio of soluble organic C to soluble organic N also tended to be lower in the rhizosphere soil than the bulk soil (not significant, P=0.126, t=-1.34)), reflecting the greater elevation of rhizosphere soil soluble organic N than soluble organic C.


PCA analysis on soil parameters

PCA analysis on the soil parameters measured for each rhizosphere soil and bulk soil sample (Fig. 5) shows clear joint separation of the rhizosphere and bulk soils by sampling area along PC axis 1 (explaining 51.3% of total variation). This spatial separation being driven by a suite of variables including total C and N (factor loading (FL) 0.97 and 0.99, respectively), moisture (FL 0.94), microbial biomass C and N (FL 0.90 and 0.95, respectively), and a range of elemental nutrients (S, FL 0.97; Mg, FL 0.95; Zn, FL 0.94; Mn, FL 0.88; P, FL 0.81). Within this spatial variation, the rhizosphem and bulk components at each soil locality are then distinctly separated along PC axis 2 (explaining 19.2% of total variation). This distinct separation of bulk and rhizosphere soil was driven by ammonium concentration (FL 0.90), microbial biomass C to N ratio (FL 0.89), and parameters of microbial activity, including cumulative C[O.sub.2] release (FL 0.77) and average well colour development (FL 0.89) and Shannon's diversity index (FL 0.94) in Biolog[TM] assay.


Root chemistry

The single root sample analysed had total C and N concentrations of 429.1 and 7.8mg/g, respectively, giving a total C to N ratio of 55.1. The [[delta].sup.15]N of the root sample was -1.47[pethousandr].


The findings clearly illustrate a marked difference in the biological and chemical nature of the rainforest rhizosphere soil compared with that of the surrounding bulk soil. The significantly greater total C and N concentrations in the rainforest rhizosphere soil than in the bulk soil are indicative of strong biological influence upon soil processes in the rainforest rhizospherc, as has been found across other vascular plant dominated ecosystems. That the total C to N ratio of the rainforest rhizosphere soil was significantly greater than that of the bulk soil may, in part, be due to large inputs of C-rich, root-derived organic matter into the rhizosphere soil. Nitrogen is a limiting resource for plants. Plants may, therefore, retain N in their tissues while yielding C, with the knock-on benefit that C-limited soil microbiota utilise this plant-derived C to acquire further nutrition via organic matter decomposition, which in turn generates soluble N products for plant uptake. In addition, given that root-derived organic matter is likely to dominate in the rhizosphere, and leaf and woody derived organic matter in the bulk soil, differences in the C to N ratios of these organic input sources (Jackson et al. 1997; Vivanco and Austin 2006) may also contribute to differences in rhizosphere soil and bulk soil total C to N ratios.


The greater microbial biomass C and microbial metabolic activity, both overall respiration and utilisation of a range of specific C substrates, in the rainfbrest rhizosphere soil compared with the bulk soil suggest that alongside root activity, high microbial activity is contributing to the strong biological influence upon rhizosphere soil processes. That the rhizosphere presents favourable conditions for microbial activity is in accordance with previous studies on temperate species that report greater soil microbial biomass (Priha et al. 1999; Joergensen 2000; Phillips and Fahey 2007) and microbial respiration (Jensen and Sorensen 1994; Priha et al. 1999; Steer and Harris 2000; Phillips and Fahey 2007) in the rhizosphere than in the surrounding bulk soil. It is well established that root-derived C presents a substantial C source for microbial activity in rhizosphere soils (Kuzyakov 2010). While we do not have direct evidence for the relative contribution of root inputs v. inputs from aboveground, the fact that the concentration of C in the rainforest rhizosphere soil was found to be significantly higher than that in the surrounding bulk soil suggests that root-derived C is a major factor promoting microbial activity in the rainforest rhizosphere. Additionally, the observation that the rainforest rhizosphere soil microbial community was capable of utilising a wider range of labile C substrates than that in the surrounding bulk soil suggests a more metabolically diverse microbial community in the rhizosphere, which may in part be a product of a wider diversity of available C substrates.

The combination of higher ambient soluble N concentration and greater microbial activity in the rainforest rhizosphere soil than the surrounding bulk soil suggests a greater rate of soluble N release via the microbial metabolism of organic matter in the rhizosphere. That the ammonium concentration of the rainforest rhizosphere soil was found to be so markedly higher than the surrounding bulk soil suggests substantial ammonium generation via mineralisation in the rainforest rhizosphere, in keeping with the findings of the N mineralisation assay. This is in agreement with previous studies reporting greater rates of ammonium mineralisation in rhizosphere soil than in the surrounding bulk soil for temperate species (Norton and Firestone 1996; Herman et al. 2006). Our findings cannot differentiate between the relative contributions of a larger pool of organic matter available for microbial metabolism and higher microbial activity in driving greater microbially mediated soluble N generation in the rhizosphere, but it is likely to be a combination of both. Root secretion of nitrogenous organic compounds (Lesuffieur et al. 2007) may also be a contributor to the heightened concentration of soluble organic N in the rhizosphere soil.

Despite greater soluble N generation, it is somewhat surprising that the ambient concentration of soluble N was also higher in the rainforest rhizosphere soil than the surrounding bulk soil, given likely high rhizospheric plant and microbial N demand. It may be that rhizospheric soluble N generation exceeds plant and microbial uptake requirements in the rainforest sampled, in keeping with global trends for high N richness and N export of lowland tropical forest (Hedin et al. 2009). Findings for the relative concentrations of soluble inorganic N in rhizosphere and adjacent bulk soils for temperate plant species have been varied, with no consistent trend for either ammonium or nitrate (Hojberg et al. 1996; Schrttelndreier and Falkengren-Grerup 1999; Yanai et al. 2003).

The observation that there was no difference between the microbial biomass N contents of the rainforest rhizosphere soil and bulk soil despite heightened rhizosphere soil microbial biomass C may reflect a greater microbial demand for C than for N from rhizospheric organic matter metabolism, and is in keeping with the lower soluble organic C to soluble N ratio of the rainforest rhizosphere soil. Fungal biomass has a higher C to N ratio than bacteria (Harris et al. 1997); a higher fungi to bacteria ratio in the rainforest rhizosphere soil than in the surrounding bulk soil, with mychorrhizal hyphae in the rhizosphere potentially contributing to this, may therefore be contributing to the heightened rhizosphere soil microbial biomass C to N ratio.

Given the general indication of greater N cycling activity in the rainforest rhizosphere soil than the surrounding bulk soil and that several biochemical soil N transformation pathways discriminate against [sup.15]N (Hogberg 1997), it is surprising that the [[delta].sup.15]N ([sup.15]N to [sup.14]N ratio relative to atmospheric [N.sub.2]) of the rainforest rhizosphere soil was lower than that of the surrounding bulk soil. Plant tissue [[delta].sup.15]N is generally lower than that of soil (Ledgard et al. 1984; Nadelhoffer and Fry 1994), and zones of high plant litter input into the soil can therefore be expected to have depleted [[delta].sup.15]N signatures (Nadelhoffer and Fry 1988; Kitayama and lwamoto 2001). The [[delta].sup.15]N of the root sample from the rainforest study site was lower than that of the rhizosphere and bulk soils, in keeping with the findings of fine root v. bulk topsoil [[delta].sup.15]N for other forest localities (Kitayama and Iwamoto 2001; Templer et al. 2007). High inputs of plant root litter may, therefore, have driven the depletion of [sup.15]N in the rainforest rhizosphere soil. In addition, leaching may be expected to be lower in the rhizosphere soil than the bulk soil due to rhizospheric effects on soil physical properties and cation exchange capacity. As biochemical soil N transformation pathways discriminate against [sup.15]N, and therefore soluble N products are likely to be enriched in [sup.15]N, lower leaching of [sup.15]N from the rhizosphere soil than the bulk soil may also have contributed to the lower [[delta].sup.15]N of the rhizosphere soil.

That total P, S, Na, Cu, Zn, K, Mg, and Ca concentrations were greater in the rainforest rhizosphere soil than in the bulk soil suggests that biological processes may be acting to concentrate these elemental nutrients in the rhizosphere. Acidic secretions by plant roots and rhizosphere-dwelling microorganisms have been shown to solubilise a range of elemental nutrients immobilised in soil particles (Landeweert et al. 2001). This would not, however, be expected to result in an increase in total rhizospheric concentrations of the given elements, as retention of mobilised ions in local soil solution and microbial biomass would result in no net change, and loss of mobilised nutrient ions from the rhizosphere soil to plant uptake and leaching would result in a net reduction. The depletion of a range of soluble nutrients in the rhizosphere has indeed been observed in several studies (Schrttelndreier and Falkengren-Grerup 1999; Chen et al. 2002; Wang et al. 2005). It may be that over time, rapid uptake and tight recycling of soluble nutrient ions by the rainforest rhizospheric soil microbial biomass acts to retain and concentrate elemental nutrients, competing effectively with plant nutrient uptake and reducing nutrient loss to leaching. Certain elemental nutrients may also be retained within recalcitrant root litter present in the rhizosphere.

Despite the greater concentration of P in the rainforest rhizosphere soil than the surrounding bulk soil, the ratios of C, N, and S to P are all greater in the rhizosphere soil than in the bulk soil. This suggests that P availability may be limiting the extent of biological activity in the rainforest rhizosphere, and that processes affecting the mobilisation of P and the efficacy of plant and microbial P uptake are of substantial importance in maintaining the high levels of biological activity observed in the rhizosphere soil.

The paucity of information regarding the differences between forest rhizosphere and bulk soil chemical and biological properties in natural, mixed-species field settings makes it difficult to draw comparisons between the rhizosphere v. bulk soil differentiation found for this tropical lowland rainforest and that of contrasting forest types. In keeping with our findings of favourable conditions for microbial activity in the rhizosphere of lowland tropical rainforest, soil respiration and microbial biomass C were found to be greater in the rhizosphere than the surrounding bulk soil of temperate, north American, broadleaved monospecific stands (Phillips and Fahey 2007) and temperate broadleaved and coniferous tree seedlings grown ex-situ (Priha et al. 1999). In contrast to our findings, microbial biomass N was also higher in the seedling rhizospheres than the surrounding bulk soil. This may reflect differences in rhizospheric microbial community composition between tropical and temperate trees, between saplings and mature trees, and/or between trees grown under natural and controlled conditions, such as possible greater investment in mycorrhizae in natural, more demanding settings. The rate of N mineralisation in the rhizosphere of Ponderosa pine (Pinus ponderosa Douglas ex Lawson) seedlings grown ex-situ was found to be greater than in the surrounding bulk soil (Norton and Firestone 1996), suggesting that, as we found for tropical rainforest, rhizosphere processes may also act to accelerate N cycling in temperate forests. Greater rhizosphere v. bulk soil concentrations of Ca, Mg, Na, and P have been reported from Norway spruce (Picea abies (L.) Karst) forest in Sweden (Clegg and Gobran 1997; Yanai et al. 2003), which is also in agreement with our findings from tropical rainforest. In contrast to our findings, A1 and Fe concentrations in the Norway spruce stand were also found to be greater in the rhizosphere than the bulk soil (Gobran et al. 1998), and it may be that in Al- and Fe-rich tropical soils, inherently high Al and Fe concentrations override any rhizosphere and bulk soil differentiation in their concentrations.

The information available for temperate trees suggests, therefore, that rhizosphere processes may drive similar microbial and chemical differentiation between rhizosphere and bulk soil in wet tropical and temperate settings. Differentiation of forest rhizosphere and bulk soil in other climatic zones including the dry tropics, temperate rainforest, and boreal zones remains to be explored. As for the relationship between rhizosphere v. bulk soil differentiation and the nature of forest nutrient cycling in different climatic zones, it may be that while similar differentiation of forest rhizosphere and bulk soil exists among climatic zones, the drivers of this differentiation differ between climatic zones in response to contrasting environmental stresses. In wet tropical forests, rhizospherc processes that facilitate steady nutrient release within reach of root uptake may be particularly beneficial for the local retention of ecosystem nutrients under hot, high-rainfall conditions with rapid organic matter turnover and high leaching potential. In contrast, in temperate and boreal forests, rhizosphere process may be critical for increasing organic matter turnover rates and plan-soil-microorganism nutrient exchange under temperature-limiting, and for certain forest types organic matter recalcitrance limiting, conditions, alongside facilitating efficient utilisation and stabilisation of seasonal nutrient pulses. In arid zones, rhizosphere processes may be critical for soil water retention and the acceleration of mineral weathering. Further research is required linking forest rhizosphere v. bulk soil microbial and chemical differentiation with specific rhizosphere processes across climatic zones.


The biological and chemical naturc of the rhizosphere soil of this lowland tropical rainforest was found to be markedly different from that of the surrounding bulk soil. This suggests that rhizosphere processes strongly influence soil nutrient cycling in lowland tropical rainforest, and are likely to play an important role in its interaction with global biogeochemical, hydrological, and climatic cycles. This role may often be underrepresented by routine sampling of rhizosphere and surrounding bulk soil mixed together as a composite sample.

Given the paucity of information regarding the rainforest rhizosphere, further research into rhizospheric rainforest processes and their relationships with ecosystem productivity, stability, and environmental drivers is critically required to better understand the dynamics of rainforest systems on both local and global scales.


Authors would like to thank Drs Gary Bacon, Tim Blumfield, and Kylie Goodall for their assistance with field sampling, Professor Nigel Stork for the access to the site, and Marijke Heenan for laboratory assistance. This study was also supported by the Australian Research Council (DP0664154, DP0667184, FT0990574).


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Received 17 August 2011, accepted 8 October 2011, published online 17 November 2011

Hannah Toberman (A), Chengrong Chen (A,C), and Zhihong Xu (B)

(A) Environmental Futures Centre, Griffith School of Environment, Griffith University, Nathan, NSW 4122, Australia.

(B) Environmental Futures Centre, School of Bio-molecular and Physical Sciences, Griffith University, Nathan, NSW 4122, Australia.

(C) Correponding author. Email:
Table 1. Elemental composition (mean concentration [+ or -] s.e.,
n=5) of rainforest bulk and rhizosphere soil

Element        Bulk soil        Rhizosphere soil


P         443.1 [+ or -] 23.5   487.0 [+ or -] 24.5
S         425.8 [+ or -] 45.6   516.1 [+ or -] 53.9
Na        195.1 [+ or -] 38.0   235.7 [+ or -] 37.5
B          38.4 [+ or -] 1.2    57.51 [+ or -] 12.2
Cu         19.2 [+ or -] 3.0     34.9 [+ or -] 5.9
Zn         45.0 [+ or -] 8.8     52.5 [+ or -] 7.9
Mo         1.74 [+ or -] 0.2      7.4 [+ or -] 4.1


K           5.1 [+ or -] 0.7      5.5 [+ or -] 0.6
Mg          1.8 [+ or -] 0.6      1.9 [+ or -] 0.6
Fe         25.6 [+ or -] 2.5     29.7 [+ or -] 2.4
Al         59.0 [+ or -] 4.3     58.4 [+ or -] 3.5
Ca          0.7 [+ or -] 0.2      1.0 [+ or -] 0.3
Mn          1.1 [+ or -] 0.5      1.1 [+ or -] 0.4

Element   Significance level

P         P=0.005# (t=4.64)
S         P=0.001# (t=7.09)
Na        P=0.003# (t=5.37)
B         P=0.084 (t= 1.68)
Cu        P=0.035# (t=2.45)
Zn        P=0.001# (t=6.57)
Mo        P=0.121 (t=1.37)

K         P=0.017# (t=3.14)
Mg        P=0.003# (t=5.23)
Fe        P=0.131 (t=1.30)
Al        P=0.324 (t= 0.49)
Ca        P=0.013# (t=3.43)
Mn        P=0.435 (t=0.17)

Significance determined by paired t-test; d.f. =4 (P values [less
than or equal to] 0.05 in bold)

Note: Significance determined by paired t-test; d.f. =4 (P values
[less than or equal to] 0.05 indicated with #.)

Table 2. Carbon substrate use (mean value [+ or -] s.e., n=5) of
microbial communities in rainforest bulk and rhizosphere soil
determined by Biolog[TM] assay

Biolog[TM] assay      Bulk soil              Rhizosphere
parameter                                        soil

Average well colour   1.11 [+ or -] 0.1     1.3 [+ or -] 0.1
Sum of activity       98.4 [+ or -] 1.9   123.8 [+ or -] 7.6
Substrate richness    81.6 [+ or -] 2.5    85.8 [+ or -] 1.6
Shannon's diversity    3.5 [+ or -] 0.1     3.7 [+ or -] 0.1

Biolog[TM] assay        Significance
parameter                  level

Average well colour   P=0.013# (t=3.5)
Sum of activity       P=0.013# (t=3.5)
Substrate richness    P=0.040# (t=2.3)
Shannon's diversity   P=0.005# (t=4.5)

Significance determined by paired t-test; d.f. =4 (P values [less
than or equal to] < 0.05 in bold)

Note: Significance determined by paired t-test; d.f. =4 (P values
[less than or equal to] 0.05 indicated with #.

Table 3. Elemental ratios (mean [+ or -] s.e., n=5) of total carbon,
nitrogen, phosphorus, and sulfur of the rainforest bulk and
rhizosphere soil

Elemental      Bulk soil          Rhizosphere soil
C: N        10.8 [+ or -] 0.3    11.7 [+ or -] 0.2
C: P        93.9 [+ or -] 9.9   112.8 [+ or -] 13.5
C:S         97.7 [+ or -] 4.5   105.6 [+ or -] 6.5
N: P         8.6 [+ or -] 0.8     9.6 [+ or -] 1.0
N:S         9.01 [+ or -] 0.3     9.0 [+ or -] 0.5
P: S         1.1 [+ or -] 0.1     1.0 [+ or -] 0.1

Elemental   Significance level
C: N        P=0.009# (t=3.81)
C: P        P=0.022# (t=2.91)
C:S         P=0.068 (t=1.86)
N: P        P=0.035# (t=2.46)
N:S         P=0.472 (t=0.08)
P: S        P=0.004# (t=-4.76)

Significance determined by paired t-test; d.f. =4 (P values [less
than or equal to]0.05 in bold)

Significance determined by paired t-test; d.f. =4 (P values [less
than or equal to] 0.05 indicated with #.
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Author:Toberman, Hannah; Chen, Chengrong; Xu, Zhihong
Publication:Soil Research
Article Type:Report
Geographic Code:8AUST
Date:Oct 1, 2011
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