Effect of physical, chemical and environmental characteristics on arbuscular mycorrhizal fungi in Brachiaria decumbens (Stapf) pastures

Journal of Applied Microbiology ISSN 1364-5072

ORIGINAL ARTICLE

Effect of physical, chemical and environmental characteristics on arbuscular mycorrhizal fungi in Brachiaria decumbens (Stapf) pastures ´ lvarez2 R.H. Posada1,2, L.A. Franco2, C. Ramos3, L.S. Plazas2, J.C. Sua´rez2 and F. A 1 Jardı´n Bota´nico Jose´ Celestino Mutis, Bogota´, Colombia 2 Departamento de Biologı´a, Facultad de Ciencias, Universidad de la Amazonı´a, Florencia, Caqueta´, Colombia 3 Lab. Ecologı´a terrestre, Depto. de Ciencias Ecolo´gicas, Universidad de Chile, Santiago, Chile

Keywords Amazonian foothill, arbuscular mycorrhizal fungi, Brachiaria decumbens, pastures. Correspondence Rau´l Hernando Posada, Calle 63A, No 32-09 Piso 2, Bogota´, Colombia. E-mail: [email protected]

2007 ⁄ 1275: received 11 September 2006, revised 24 April 2007 and accepted 4 July 2007 doi:10.1111/j.1365-2672.2007.03533.x

Abstract Aim: To evaluate the effects of soil physical and chemical factors (pH, conductivity, humidity, available phosphorus and organic matter) and environmental factors (temperature, relative air humidity, altitude and atmospheric pressure) on arbuscular mycorrhizal fungi (AMF)–Brachiaria decumbens grass relationship. Furthermore to establish patterns of microbiological responses that allow to differentiate the study sites in two relief types. Methods and Results: Mycorrhizal characteristics (spore density, external hyphae and root colonizations by hyphae, vesicles and arbuscules), physical and chemical factors in soil and environmental factors were measured. Conclusions: The effect of physical, chemical and environmental factors on microbiological variables was related to the type of relief ‘valley and hilly terrain’; the AMF behaviour was affected only over narrower ranges of evaluated variables. Similarly, the colonization of B. decumbens roots by AMF hyphae, vesicles and the mycorrhizal spore density follow different patterns according to the relief type. Significance and Impact of the Study: The type of relief is one of the factors to be taken into consideration to evaluate the AMF inoculum and root colonization of these pastures, because of the influence of slope – as physical property of soil – on AMF.

Introduction Arbuscular mycorrhizal fungi (AMF) are important symbionts for most terrestrial plants. AMF take up nutrients, especially phosphorus from the soil, and these nutrients are then exchanged for carbon from the host plant. In forests, more than 80% of pioneer and early successional plant species have AMF symbiosis (Fontenla et al. 1998; Siqueira et al. 1998; Andrade et al. 2000; Siqueira and Saggin-Ju´nior 2001; Gehring and Connell 2006). AMF have therefore an important role in the recuperation and restoration of both deforested zones and gaps, influencing the establishment ability and persistence of the pioneer plants, and affecting the plant succession. 132

Soil characteristics, plant species and climate may regulate the AMF community (Escudero and Mendoza 2005). The occurrence of mycorrhiza is influenced by the land slope and the geographic and topographic locality (Dickinson 1974). High temperatures result in a greater extent of infection by AMF (Diederich and Moawad 1993); under specific conditions, the spore density correlates with fluctuations in temperature (Koske 1987). In grasses, low moisture levels lead to increases in root colonizations and decrements of the spore production by AMF (Simpson and Daft 1990; Rickerl et al. 1994; Camargo-Ricalde and Espero´n-Rodrı´guez 2005). However, both very dry and flooded soils decrease colonization by AMF (Lodge 1989; Miller and Bever 1999; Miller 2000). In general,

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vesicle colonization (Stevens and Peterson 1996) and the external hyphae (Schack-Kirchner et al. 2000) are not typically affected by the water gradient. The pH affects the distribution and abundance of different fungal species (Read et al. 1976; Porter et al. 1987a,b; Wang et al. 1993). Small increases in pH are associated with greater root colonization by AMF in acid soils with low phosphorus availability (Soedarjo and Habte 1995; Heijne et al. 1996). Besides the difficulty in separating the influences of host plant species and soil characteristics on root colonization and the inoculum (external hyphae and spore density) density (Escudero and Mendoza 2005), there is not a clear separation between plant and soil factors. There is growing evidence that diversity and distribution of AMF depend on the community structure and characteristics of the ecosystem (Van der Heijden and Sanders 2002). Brachiaria decumbens (Stapf) is a grass species introduced to the Amazonian foothills in Colombia in 1970 as a forage pasture to improve the cattle productivity (Cuesta 1978; Siqueira et al. 1990; Vela´squez and Cuesta 1990). Since then, extensive monocultures of this grass have replaced the forest coverage. Although B. decumbens has root colonizations of 75% in Brazilian soils with high phosphorus content (Oliveira et al. 1997), continuity of these pastures can affect the AMF populations, resulting in the reduction of soil biological and productive capacities (Robertson et al. 1997). Commonly, the mycorrhizal fungi follow heterogeneous distribution patterns, according to the soil and environmental characteristics where the plant species are (Camargo-Ricalde and Espero´n-Rodrı´guez 2005); the study of this association with just one dependent plant species helps to take the decision about the requirement or not of previous soil enrichment with mycorrhizal supply when sowing the seedlings and saplings – of pioneer trees to restoration programmes. The objectives to study on B. decumbens pastures were to: (i) determine the most influential soil and environmental variables, and how these variables affect AMF behaviour, and (ii) establish patterns of microbiological responses that allow to differentiate the study sites in two relief types. Materials and methods This study was conducted at 26 sites located in the Amazonian foothills of Caqueta´, Colombia, in the area between 128¢50Æ3¢¢–126¢41¢¢N and 7540¢14¢¢–7528¢26¢¢W. This is situated in a zone of confluence between the Andean Cordillera and the Amazonian forest, with mean annual temperature of 28C, mean annual rainfall of 3500 mm, and mean air relative humidity of 87%. The sites were

Arbuscular mycorrhiza in pastures

pastures resulting from clearing of tropical rain forest, and comprised two types of relief – hilly terrain and fertile valley with a floodplain. Twenty-six sites of 1000 m2 in 18 farms were selected to take samples in the hilly areas -slope 20–35 from the horizontal (APY, ARY, FBY, JMY, UAY, AAY, ABYA, FMY, GSY, DCY, ESYA, ESYB, FGY, NAY, ABYB), and in the valley plains (slope 0–11 from the horizontal (CNX, ESX, JAX1, JAX2, ACX, GSX, VPX, FGX, NAXA, NAXB, VAX), with B. decumbens (Stapf) as pasture, and the samples were collected between January and April of 2003 (dry season). A cylinder of 38 mm diameter and 250 mm length was used to take soil samples of 0–0Æ2 m deep – at 0–0Æ1 m from the plant, completing 10 randomly selected samples per site (260 in total). All samples were thoroughly homogenized. Two subsamples (each 200 g) were used to evaluate spore density and external mycelia; one root subsample (1 g) was used to evaluate colonization, and one soil subsample (100 g) for physical and chemical determinations. Environmental conditions were measured with a field KONUS digital thermohygrometer and an altimeter-barometer. The labelled samples were separated into roots and soil in the laboratory, and were stored at 2C for later assessment. The AMF spore density was determined according to Sieverding (1983), by wet sieving with 45, 120 and 500 lm sieves and decanting, followed by centrifugal flotation (500 g l–1 sucrose). The results were expressed as spore number 10 g–1 dry soil. Coenocytic extra-radical hyphae or external hyphae were extracted according to Herrera et al. (1986). Air-dried samples were added to H2O2 (0Æ2 l l–1 H2O2), blended for 30 s, rinsed on the 45 lm sieve, air-dried for 48 h and weighed. A further sample of 0Æ02 g was mixed with two drops of glycerin (100%) on a microscope slide. The number of coenocytic hyphae of AMF that intersected four squared transects (two horizontal and two vertical, separated by 5 mm) on each slide were counted at 100· magnification using a compound microscope. The results were expressed in meters of external hyphae (m g–1 soil). Roots were cleared and stained by the Philips and Hayman (1970) modified method. Cleared roots were acidified with HCl (10 g l–1 HCl) for 300–900 s and stained in acid Trypan blue (0Æ5 g l–1 Trypan blue); the roots were mounted on microscope slides for assessment by the magnified intercept method as described by Pabo´n (2000), Posada (2001) and Aristizabal et al. (2004). Colonization of roots (% aseptate hyphae colonization, % vesicle colonization, % arbuscule colonization and % septate hyphae colonization) was estimated as the number of colonized intersections divided by the total number of observed intersections; septate hyphae colonization was measured as an indicative of fungal competition against AMF and

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non-AMF in roots and as ecological behaviour of plant species. Soil humidity (%) determination was made by drying samples at 80C for 72 h, the electric conductivity (EC) (lS cm–1) by direct measurement in conductivity-meter and the pH in a 1 : 1 soil:water slurry; the organic matter determination was realized by Wilkley–Black method (% carbon 100 g–1 soil) and the available phosphorus was measured employing the Bray II method (lg g–1) (IGAC 1999). Physical and chemical variables in soil (conductivity, soil relative moisture, organic matter, available phosphorus, pH), environmental variables (altitude, air relative humidity, atmospheric pressure, temperature), and microbiological variables (spore density, external hyphae, colonization by hyphae, colonization by vesicles, colonization by arbuscules and colonization by septate fungi) were summarized in a matrix by sites. Colonization variables and conductivity were –log10(x + 1) normalized and the remainder variables were log10 normalized before the analysis. We used one-way anova to evaluate differences in the variables, between types of relief; and Spearman’s rank correlation coefficients were computed for all pairwise combination of variables measured by relief. The microbiological, physical, chemical and environmental variables with higher influence on the variability between sites were determined by principal component analysis. Similarity between sites by microbiological characteristics was detected clustering the microbiological variables in a correlation matrix by sites and the results were expressed in dendrograms. Canonical correlations were used to determinate the effect of physical, chemical and environmental variables on the AMF behaviour. Statistical analysis was performed using the sas program (SAS Institute Inc., Cary, NC, USA). Results The measured characteristics (physical and chemical of soil, environmental and microbiological), were highly variable (Table 1). Three characteristics differed significantly from one type of relief to another; the phosphorus availability and pH were larger in the valley than in the hilly terrain; but the spore density was larger in the hilly terrain than in the valley. In the hilly terrain, there were highly positive correlations between conductivity and colonization by arbuscules (r = 0Æ672, P = 0Æ0176), between soil humidity and external hyphae (r = 0Æ646, P = 0Æ0192) and between the colonization by hyphae and colonization by vesicles (r = 0Æ950, P < 0Æ0001); there were negative correlations between spore density and altitude (r = –0Æ660, P = 0Æ0183). In contrast, in the valley there were highly positive correlations between colonization by hyphae and colonization 134

Table 1 Mean (±SD) of physical, chemical, environmental and microbiological measures in the sampling sites, according to the type of relief (fertile valley with a floodplain and hilly terrain), obtained by one-way ANOVA Type of relief Characteristics Soil Physical and Chemical Available phosphorus (lg g–1)* pH* Organic matter (%) Conductivity (lS cm–1) Soil humidity (%) Environmental Air relative humidity (%) Altitude (m a.s.l.) Pressure (MPa) Temperature (C) Microbiological Colonization by hyphae (%) Colonization by vesicles (%) Colonization by arbuscules (%) Colonization by septate fungi (%) External hyphae (m g–1) Spore density no.*

Fertile valley

Hilly terrain

22Æ5 5Æ05 3Æ51 0Æ160 32Æ8

± ± ± ± ±

12Æ8 0Æ46 0Æ98 0Æ009 5Æ33

11Æ7 4Æ59 3Æ26 0Æ172 31Æ6

± ± ± ± ±

7Æ44 0Æ27 0Æ56 0Æ027 4Æ22

61Æ0 267 98Æ3 30Æ3

± ± ± ±

6Æ09 37Æ5 0Æ87 2Æ43

62Æ8 334 98Æ7 30Æ6

± ± ± ±

6Æ61 90Æ7 1Æ61 2Æ21

30Æ5 14Æ5 1Æ16 37Æ3 44Æ8 183

± ± ± ± ± ±

29Æ8 19Æ7 2Æ12 20Æ9 27Æ4 78Æ4

30Æ7 14Æ7 0Æ64 39Æ5 47Æ5 242

± ± ± ± ± ±

24Æ3 15Æ7 1Æ10 21Æ7 47Æ4 113Æ5

*Significant at P £ 0Æ05.

by vesicles (r = 0Æ952, P < 0Æ0001), between colonization by hyphae and colonization by arbuscules (r = 0Æ768, P = 0Æ0057), between colonization by vesicles and colonization by arbuscules (r = 0Æ823, P = 0Æ0021); and negative correlations between spore density and colonization by hyphae (r = –0Æ618, P = 0Æ0416), between organic matter and soil humidity (r = –0Æ840, P = 0Æ0012), and between available phosphorus and altitude (r = –0Æ659, P = 0Æ0184). The microbiological characteristics more sensitive to the variability between sites were the root colonizations by hyphae and vesicles (explained variability: 39%); and the inoculum (explained variability: 26%) (Fig. 1). The samples of ABYB showed responses different from other sites (dotted line right and bottom); while the characteristic least sensitive to the variability was the colonization by arbuscules. Among physical and chemical variables in the soil, the first principal component (30Æ8%) joined pH, soil humidity and organic matter; the second principal component (27Æ4%) was the phosphorus availability, and the third one represented the EC (20Æ8%). The valley showed a differentiation of the sites in function from the axes 1 and 2 bigger to the differentiation of sites in the hilly terrain. The samples in the valley had the lower conductivities, and the samples in the hilly terrain had the lower phosphorus availabilities. Samples from ESYA were different

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Arbuscular mycorrhiza in pastures

3 Colonization by vesicles

Colonization by Hyphae

2 VAX VAX ARY VAX ESX VAX ESYA VPXESX VAXAPY CNXCNX FMY FMY FGY CNX ESX CNX FBY GSY ABYAUAY CNX DCY APY DCY GSX FBYGSY FBY NAXB DCY FGX UAY FGY ACX AAYFGYABYA FBY APY FGX DCY ESYA ABYA FGX FGY ACX ESYA ARY UAY ESYB NAXA ACX CNX ACX NAY FGX NAXA JAXA NAY JAXB VPX NAXA JAXA AAY NAXA ESYB Septate Fungi JAXB JAXB JMY AAY DCY JAXA JAXA VPX JAXB ESYB VPX NAY ESYB

Prin 1

1

0

–1

–2

FMY DCY

ABYB

ABYB

External Hyphae Spore Density ABYB

ABYB

Figure 1 Vectors (arrow) and distribution of sampling sites according to the principal microbiological components. Prin1 (colonization by hyphae and vesicles), prin2 (external hyphae and spore density).

ABYB

–3 –2

from those from the other hilly terrain sites (Fig. 2a,b). All the environmental parameters have similar contributions to the variability between sites and we did not identify a principal component. For the microbiological characteristics, there were two defined clusters in the hilly terrain, grouping six sites (cluster 1) and seven sites (cluster 2), respectively, and two nonlinked sites, FMY and ABYB (Figs 3a and 4a). There were four clusters in the valley, grouping two (clusters 3, 5 and 6) and five sites (cluster 4) (Figs 3b and 4b). The clusters were defined by different associations between root colonization (hyphae and vesicles) and inoculum (external hyphae and spore density) for each type of relief. The canonical analysis showed the influence of environmental variables and soil physical and chemical variables (explaining the 37% of the total variance) over some of the microbiological characteristics. In the hilly terrain, low phosphorus availabilities were related to the lowest colonization by hyphae or with increases in colonization by vesicles (41% of total variance) (Fig. 4a). In the valley, low air humidity and the highest temperatures were related to the lowest colonizations (33% of total variance) (Fig. 4b). Discussion Brachiaria decumbens is a species of grass with AMF colonization between 2Æ4% and 79Æ6% in the Amazonian foothills region, irrespective of the type of relief (Table 1); it

–1

0

1

2

3

4

5

Prin 2

is a wide range of colonization, with a variability that depends on AMF responses and of edaphic and climatic local conditions. Only a few of microbiological variables were significantly affected by soil and environmental characteristics. The greatest variations observed between sites were given in the root colonization (hyphae and vesicles), and the inoculum (external hyphae and spores density) (Fig. 1), and precisely the variables that gave place to positive correlations were those of more weight in the principal components. Among these characteristics, the colonization by hyphae and colonization by vesicles correlated in both types of relief. In the valley there were correlation between the colonization by hyphae and colonization by arbuscules too. Soils of the study area are acids (pH 4–6), highly humid (26–45%) and moderate in their organic matter (1Æ8–5Æ1%), as in most of Amazonian environments (IGAC-INPA 1993; Malago´n et al. 1995); these three characteristics were the most influential (first principal component from physical and chemical variables) in the variability of sites. Although the properties of soil can affect the spatial distribution of AMF spores, this relationship depends on the site (Carvalho et al. 2003; Camargo-Ricalde and Espero´n-Rodrı´guez 2005); in this study we found a negative association between organic matter and soil humidity in the valley, but not in the hilly terrain, which explains the importance of the physical and chemical first principal component.

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(a)

Prin 1 3 2 1 0 ESYA

–1 –2 –1.5

–1.0

–0.5

0.0

0.5

1.0

1.5

2. 0

2.5

Prin 2 (b) Prin 2 2.5 2.0

ESYA

1.5 1.0 0.5 0.0 –0.5 –1.0 –1.5 –2

–1

0

1

2

3

4

Prin 3 Figure 2 Distribution of sampling sites according to the principal components of physical and chemical characteristics in the soil, by type of relief. (a) Prin1 (pH, soil humidity and organic matter) vs Prin2 (phosphorus availability). (b) Prin2 (phosphorus availability) vs Prin3 (electrical conductivity). (j, Hilly terrain; h, valley)

The second physical and chemical principal component corresponded to the phosphorus availability (6– 44 ppm); the sites in the hilly terrain had a mean phosphorus availability of 11Æ4 ppm, value that is below the mean for valley (22Æ5 ppm). The third factor was the electrical conductivity (0Æ13–0Æ24 lS); the sites in the valley included the lowest conductivities (0Æ15–0Æ18 lS) (Table 1, Fig. 2a,b) whereas a high electrical conductivity in hilly terrain soils could contribute to liberating the phosphorus trapped by aluminium in soil, making it available to be used by AMF (Fig. 2b). There is not a clear relationship between water regime and AMF, because of the aerobic nature of AMF. We found however, a high positive correlation between the soil humidity and the external hyphae in the soils of the hilly terrain, where the external hyphae varied 9Æ5-fold, a particular case relating to the local conditions. Schack-Kirchner et al. (2000) showed that 136

variations up to 5Æ9-fold in external hyphae are independent of aeration parameters in soil, and thus of the water content. The initiation and colonization levels in trap plants were less reduced by a high EC of soil than by the NH4HCO3. In association with pH, this is related to the delay in the initiation of root colonization, when the soil EC is larger than 500 lS cm–1 (Pattinson et al. 2000). According to our results, the EC was not limiting for root colonization (0Æ13–0Æ24 lS cm–1), but small increases of EC in soil were related to the arbuscule production in the hilly terrain. In the dendrogram for valley sites, FMY and ABYB were nonlinked sites (Figs 3a and 4a), FMY with the highest root colonization and the lowest environmental pressure, and ABYB with the highest inoculum and one of the two higher soil humidities (Fig. 1). This could suggest strong microbiological responses, but the study of environmental factors that affect the root colonization, presence, spore density and external hyphae of AMF at tropical soils is incipient (Escudero and Mendoza 2005). Some AMF species are prolific spore producers while others are not, this fact may explain some of spore density differences, and it is even possible that, the inoculum values do not reveal the intensity of root colonization in a community (Clapp et al. 1995). Plotting patterns and cluster analysis converge to explain the variability of AMF characteristics. The sites were distributed in relation to the microbiological characteristics: root colonizations and spore density, according to the type of relief. In the hilly terrain, the former cluster comprised sites with the lowest root colonizations, and the second cluster sites with the highest root colonizations (Figs 3a and 4a). In the valley the clusters had more complexity than in the hilly terrain: the first group (cluster 3) contains sites with the highest spore densities, the second group (cluster 4) contains sites with the lowest root colonization by vesicles, the third group (cluster 5) contains sites with the lowest spore densities, and the fourth group (cluster 6) contains sites with highest root colonizations (Figs 3b and 4b). The different clusters showed that there is no simple and direct relationship between the development of external hyphae and the development of internal hyphae (Abbott and Robson 1991; Bethlenfalvay et al. 1999). The extreme characteristics of Amazonian soils can induce stress on the AMF (Soedarjo and Habte 1995; Heijne et al. 1996; Stevens and Peterson 1996; SchackKirchner et al. 2000; Mendoza et al. 2002; Escudero and Mendoza 2005), causing strong responses on the mycorrhizal variables, colonization by hyphae, vesicles and arbuscules, external hyphae, density and diversity of spores. Any small change under these prevailing

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(a) Site AAY DCY APY

1

JMY NAY ESYB ABYA FBY UAY

2

ARY ESYA FGY GSY FMY ABYB

0·0

0·2

0·4

0·6 0·8 1·0 1·2 1·4 Average distance between clusters

1·6

1·8

2·0

(b) Site ACX

3 NAXB FGX NAXA

4

VPX JAX1 JAX2 CNX

5 GSX

Figure 3 Dendrograms based on nearest neighbourhood method to represent the microbiological clusters (1, 2, 3, 4, 5, 6) of sampling sites by type of relief, according to correlation matrix. (a) In the hilly terrain, (b) in the valley.

ESX

6 VAX

0·0

0·2

conditions can be decisive for the mycorrhizal development in a tropical environment. There were microbiological responses which were related to restricted ranges in the physical, chemical and environmental characteristics, which were related to the microbiological responses: in the hilly terrain, the lowest phosphorus availabilities (8 ppm or less) were associated with colonizations by hyphae up to 18% or to colonization by vesicles higher than 17%, and a close relationship between spore density and altitude (Allen et al. 1995) was found. On the other hand, at the valley air humidities higher to 50% and temperatures above 31C were

0·4

0·6

0·8

1·0

1·2

1·4

1·6

Average distance between clusters

associated with B. decumbens root colonizations (up to 30% by hyphae and up to 5% by vesicles; microbiological first principal component). In conclusion, the effect of physical, chemical factors of soil and environmental factors on the microbiological variables (spore density, external hyphae, root colonizations by vesicles and arbuscules) was related to the type of relief. Moreover, the behaviour of AMF was affected only under narrower ranges of values for the measured variables, being difficult to establish a large effect of these factors on the AMF conduct. In the Amazonian foothills, the B. decumbens root colonization

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Acknowledgements

(a) V1 2·067 ABYB

FMY 1·116

Non-linked Sites

GSY 0·165

APY

ABYA NAY

–0·787

ESYA

JMY ARY

ESYB

DCY AAY Cluster 1 and 2

UAY FBY –1·738 FGY 0·256 –1·648 –0·696

References 2·160

1·208

W1 (b)

V1 2·025 ACX Cluster 6 1·102

ESX FGX

VAX

JAX1 0·179

VPX NAXB

–0·744

JAX2 NAXA

Cluster 5

GSX

Cluster 4

CNX

–1·666 –1·666

–0·744

0·179

1·102

2·025

W1 Figure 4 Canonical relationships between the environmental and soil characteristics (W) and the microbiological variables (V). (a) In the hilly terrain. Cluster 1 in grey, cluster 2 in black. (b) in the valley.

by AMF hyphae and vesicles, and the mycorrhizal spore density follow different response patterns according to the type of relief. Some authors suggest that the plant factors are more important than soil factors (Koomenn et al. 1987; Mendoza et al. 2002), but this does not help to understand their significance in the community structure. The restoration of zones previously dominated by forest and currently with pastures of B. decumbens requires an understanding of the mycorrhizal condition on soil and their variability. To determine what sites could favour a fast forest recovery, it is necessary to consider the availability of the mycorrhizal inoculum, and to employ this knowledge for selection of shortcycle species with favourable mycorrhizal responses. The type of relief is a key factor for determination of inoculum and root colonization of these pastures, because of their influence on physical and chemical soil characteristics. 138

The authors thank the Amazonia University for financial support and the use of installations; CORPOICA Titaitata for soil analyses; Geovany Lara Zuluaga, Andre´s Olaya Montes, Carlos Alberto Rodrı´guez, Wilson Sa´nchez Chacon, Adriana Patricia Sa´nchez Figueroa, Edith Medina Giro´n of the Symbiotic Microorganisms Investigations Team for their work and collaboration during its development.

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Journal of Applied Microbiology Including Letters in Applied Microbiology & Annual Symposium Published on behalf of the Society for Applied Microbiology Edited by: A. Gilmour Print ISSN: 1364-5072 Online ISSN: 1365-2672 Frequency: Monthly Current Volume: 110 / 2011

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Editorial Information Chief Editor A. Gilmour, Agri-Food and Biosciences Institute, Northern Ireland, UK Fax: +44 (0) 28 90255009 email: [email protected] Managing Editor K. Brister, Wiley-Blackwell, Oxford, UK email: [email protected] Editors B. Austin, Institute of Aquaculture, University of Stirling, Stirling, UK M.M. Bagdasarian, Michigan State University, East Lansing, MI, USA L. Baillie, Welsh School of Pharmacy, Cardiff University, Cardiff, UK M.D. Barton, University of South Australia, Adelaide, Australia E. Bartowsky, The Australian Wine Research Institute, Glen Osmond, Australia A.M. Bojesen, Department of Veterinary Disease Biology, University of Copenhagen, Denmark A. Bosch, Universitat de Barcelona, Barcelona, Spain P. Calik, Middle East Technical University, Ankara, Turkey M.L. Chikindas, The State University of New Jersey, New Brunswick, NJ, USA P.J. Collier, University of Abertay, Dundee, UK K.L. Cook, USDA-ARS Animal Waste Management Research Unit, Bowling Green, KY, USA J.E. Cooper, Queen's University of Belfast, Belfast, UK D.A. Cowan, University of the Western Cape, Bellville, Capetown, South Africa S.P. Cummings, School of Applied Sciences, Northumbria University, Newcastle upon Tyne, UK S.M. Cutting, Royal Holloway, University of London, UK L.M.T. Dicks, University of Stellenbosch, Matieland, South Africa M. Dow, BioSciences Institute, University College Cork, Cork, Ireland N. Fegan, Food Science Australia, Brisbane, Australia C. Gilbert, Laboratoire de Microbiologie et Génétique Moleculaire, Université Claud Bernard Lyon, Lyon, France J. Glassey, University of Newcastle Upon Tyne, Newcastle upon Tyne, UK A.E. Glenn, USDA-ARS Toxicology & Mycotoxin Research Unit, Athens, GA, USA P.C. Gowland, Staffordshire University, Stoke-on-Trent, UK D.A. Grinstead, Diversey Lever Innovation Center, Cincinnati, OH, USA J. Guard, USDA/ARS, Athens, GA, USA J.H. Hill, Department of Plant Biology, Iowa State University, Ames, IA, USA C.R. Jackson, USDA-ARS Resistance Research Unit, Athens, GA, USA F. Jorgensen, Health Protection Agency, Food Water and Environmental Microbiology Network, Porton Down, Salisbury, UK T. Kuchta, Food Research Institute, Bratislava, Slovakia G. LaPointe, Laval University, Quebec, Canada A. Leaphart, Clemson University, Clemson, SC, USA N. Lima, MUM, Minho University, Braga, Portugal J. Lisle, US Geological Survey, Center for Coastal & Watershed Studies, St Petersburg, FL, USA G.T. Macfarlane, MRC Microbiology and Gut Biology Group, Ninewells Hospital and Medical School, Dundee, UK S. Macfarlane, University of Dundee, Dundee, UK J.-Y. Maillard, Welsh School of Pharmacy, Cardiff University, Cardiff, UK D.V. Mavrodi, Washington State University, Pullman, WA, USA B. Mayo, IPLA-CSIC, Villaviciosa, Spain A. McBain, University of Manchester, Manchester, UK J.A. McGarvey, USDA-ARS Plant Mycotoxin Research Unit, Albany, CA, USA A. Mohagheghi, National Renewable Energy Laboratory, Golden, CO, USA F. Mozzi, CERELA-CONICET, Tucumán, Argentina K. Nickerson, Biological Sciences, University of Nebraska, Lincoln, NE, USA D.R. Noguera, University of Wisconsin, Madison, WI, USA C.E. Nwoguh, Health Protection Agency, CEPR, Porton Down, Salisbury, UK G-J.E. Nychas, Department of Food Science & Technology, Laboratory Food Microbiology & Biotechnology of Foods, Athens, Greece G.K. Paterson, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK C.A. Phillips, University of Northampton, UK W. Qin, Lakehead University, Thunder Bay, Canada C. Rees, University of Nottingham, Sutton Bonington, UK S. Roller, London South Bank University, London, UK C.P. Saint, SA Water Centre for Water Management and Re-use, University of South Australia, Mawson Lakes, Australia R. Seviour, Biotechnology Research Centre, La Trobe University, Bendigo, Australia P. Silley, MB Consult Limited, Hampshire, UK T.J. Smith, Biomedical Research Centre, Sheffield Hallam University, Sheffield, UK M.B. Taylor, Department of Medical Virology, NHLS/University of Pretoria, Pretoria, South Africa K.Thomas, University of Sunderland, Sunderland, UK V.P. Valdramidis, University of Malta, Malta A. Venâncio, Dept de Engenharia Biológica, Universidade do Minho, Portugal K. Venema, TNO Nutrition and Food Research, The Netherlands T.M. Wassenaar, Molecular Microbiology and Genomics Consultants, Tannenstrasse, Zotzenhein, Germany J. Wells, USDA-ARS, Meat Animal Research Center, NE, USA R. Zdor, Andrews University, Berrien Springs, MI, USA X.-H. Zhang, College of Marine Life Sciences, Ocean University of China, Qingdao, China

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