Effect of physical, chemical and environmental characteristics on arbuscular mycorrhizal fungi in...

ORIGINAL ARTICLE

Effect of physical, chemical and environmentalcharacteristics on arbuscular mycorrhizal fungi in Brachiariadecumbens (Stapf) pasturesR.H. Posada1,2, L.A. Franco2, C. Ramos3, L.S. Plazas2, J.C. Suarez2 and F. Alvarez2

1 Jardın Botanico Jose Celestino Mutis, Bogota, Colombia

2 Departamento de Biologıa, Facultad de Ciencias, Universidad de la Amazonıa, Florencia, Caqueta, Colombia

3 Lab. Ecologıa terrestre, Depto. de Ciencias Ecologicas, Universidad de Chile, Santiago, Chile

Introduction

Arbuscular mycorrhizal fungi (AMF) are important sym-

bionts 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-Junior 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.

Soil characteristics, plant species and climate may regu-

late the AMF community (Escudero and Mendoza 2005).

The occurrence of mycorrhiza is influenced by the land

slope and the geographic and topographic locality (Dick-

inson 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 (Simp-

son and Daft 1990; Rickerl et al. 1994; Camargo-Ricalde

and Esperon-Rodrıguez 2005). However, both very dry

and flooded soils decrease colonization by AMF (Lodge

1989; Miller and Bever 1999; Miller 2000). In general,

Keywords

Amazonian foothill, arbuscular mycorrhizal

fungi, Brachiaria decumbens, pastures.

Correspondence

Raul 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, conduc-

tivity, 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 relation-

ship. 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 ter-

rain’; 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 coloniza-

tion of these pastures, because of the influence of slope – as physical property

of soil – on AMF.

Journal of Applied Microbiology ISSN 1364-5072

132 Journal compilation ª 2007 The Society for Applied Microbiology, Journal of Applied Microbiology 104 (2008) 132–140

ª 2007 The Authors

vesicle colonization (Stevens and Peterson 1996) and the

external hyphae (Schack-Kirchner et al. 2000) are not typ-

ically affected by the water gradient.

The pH affects the distribution and abundance of dif-

ferent 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 coloni-

zation 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 char-

acteristics of the ecosystem (Van der Heijden and Sand-

ers 2002).

Brachiaria decumbens (Stapf) is a grass species intro-

duced to the Amazonian foothills in Colombia in 1970 as

a forage pasture to improve the cattle productivity

(Cuesta 1978; Siqueira et al. 1990; Velasquez 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 capaci-

ties (Robertson et al. 1997). Commonly, the mycorrhizal

fungi follow heterogeneous distribution patterns, accord-

ing to the soil and environmental characteristics where

the plant species are (Camargo-Ricalde and Esperon-Rod-

rıguez 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 sap-

lings – 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 Amazo-

nian foothills of Caqueta, Colombia, in the area between

1�28¢50Æ3¢¢–1�26¢41¢¢N and 75�40¢14¢¢–75�28¢26¢¢W. This is

situated in a zone of confluence between the Andean

Cordillera and the Amazonian forest, with mean annual

temperature of 28�C, mean annual rainfall of 3500 mm,

and mean air relative humidity of 87%. The sites were

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 ran-

domly 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 thermo-

hygrometer and an altimeter-barometer. The labelled

samples were separated into roots and soil in the labora-

tory, and were stored at 2�C 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 flo-

tation (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 Hay-

man (1970) modified method. Cleared roots were acidi-

fied 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 mag-

nified intercept method as described by Pabon (2000),

Posada (2001) and Aristizabal et al. (2004). Colonization

of roots (% aseptate hyphae colonization, % vesicle colo-

nization, % 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

R.H. Posada et al. Arbuscular mycorrhiza in pastures

ª 2007 The Authors

Journal compilation ª 2007 The Society for Applied Microbiology, Journal of Applied Microbiology 104 (2008) 132–140 133

non-AMF in roots and as ecological behaviour of plant

species.

Soil humidity (%) determination was made by drying

samples at 80�C 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 mea-

sured employing the Bray II method (lg g–1) (IGAC 1999).

Physical and chemical variables in soil (conductivity,

soil relative moisture, organic matter, available phospho-

rus, pH), environmental variables (altitude, air relative

humidity, atmospheric pressure, temperature), and micro-

biological variables (spore density, external hyphae, colo-

nization 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 pair-

wise 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 environ-

mental variables on the AMF behaviour. Statistical analy-

sis 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 var-

iable (Table 1). Three characteristics differed significantly

from one type of relief to another; the phosphorus avail-

ability and pH were larger in the valley than in the hilly

terrain; but the spore density was larger in the hilly ter-

rain than in the valley.

In the hilly terrain, there were highly positive correla-

tions between conductivity and colonization by arbuscules

(r = 0Æ672, P = 0Æ0176), between soil humidity and exter-

nal hyphae (r = 0Æ646, P = 0Æ0192) and between the coloni-

zation 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 correla-

tions between colonization by hyphae and colonization

by vesicles (r = 0Æ952, P < 0Æ0001), between colonization

by hyphae and colonization by arbuscules (r = 0Æ768,

P = 0Æ0057), between colonization by vesicles and coloniza-

tion by arbuscules (r = 0Æ823, P = 0Æ0021); and negative

correlations between spore density and colonization by

hyphae (r = –0Æ618, P = 0Æ0416), between organic mat-

ter 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 characteris-

tic 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 humid-

ity and organic matter; the second principal component

(27Æ4%) was the phosphorus availability, and the third

one represented the EC (20Æ8%). The valley showed a dif-

ferentiation 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 phos-

phorus availabilities. Samples from ESYA were different

Table 1 Mean (±SD) of physical, chemical, environmental and micro-

biological measures in the sampling sites, according to the type of

relief (fertile valley with a floodplain and hilly terrain), obtained by

one-way ANOVA

Characteristics

Type of relief

Fertile valley Hilly terrain

Soil Physical and Chemical

Available phosphorus (lg g–1)* 22Æ5 ± 12Æ8 11Æ7 ± 7Æ44

pH* 5Æ05 ± 0Æ46 4Æ59 ± 0Æ27

Organic matter (%) 3Æ51 ± 0Æ98 3Æ26 ± 0Æ56

Conductivity (lS cm–1) 0Æ160 ± 0Æ009 0Æ172 ± 0Æ027

Soil humidity (%) 32Æ8 ± 5Æ33 31Æ6 ± 4Æ22

Environmental

Air relative humidity (%) 61Æ0 ± 6Æ09 62Æ8 ± 6Æ61

Altitude (m a.s.l.) 267 ± 37Æ5 334 ± 90Æ7

Pressure (MPa) 98Æ3 ± 0Æ87 98Æ7 ± 1Æ61

Temperature (�C) 30Æ3 ± 2Æ43 30Æ6 ± 2Æ21

Microbiological

Colonization by hyphae (%) 30Æ5 ± 29Æ8 30Æ7 ± 24Æ3

Colonization by vesicles (%) 14Æ5 ± 19Æ7 14Æ7 ± 15Æ7

Colonization by arbuscules (%) 1Æ16 ± 2Æ12 0Æ64 ± 1Æ10

Colonization by septate fungi (%) 37Æ3 ± 20Æ9 39Æ5 ± 21Æ7

External hyphae (m g–1) 44Æ8 ± 27Æ4 47Æ5 ± 47Æ4

Spore density no.* 183 ± 78Æ4 242 ± 113Æ5

*Significant at P £ 0Æ05.

Arbuscular mycorrhiza in pastures R.H. Posada et al.


ª 2007 The Authors

from those from the other hilly terrain sites (Fig. 2a,b).

All the environmental parameters have similar contribu-

tions to the variability between sites and we did not iden-

tify 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 (clus-

ters 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 envi-

ronmental variables and soil physical and chemical vari-

ables (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 coloni-

zation 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 var-

iance) (Fig. 4b).

Discussion

Brachiaria decumbens is a species of grass with AMF colo-

nization between 2Æ4% and 79Æ6% in the Amazonian foot-

hills region, irrespective of the type of relief (Table 1); it

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 signifi-

cantly 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 cor-

relations were those of more weight in the principal com-

ponents. 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; Malagon 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 rela-

tionship depends on the site (Carvalho et al. 2003; Cam-

argo-Ricalde and Esperon-Rodrıguez 2005); in this study

we found a negative association between organic matter

and soil humidity in the valley, but not in the hilly ter-

rain, which explains the importance of the physical and

chemical first principal component.

3

2

1

0

–1

–2

–3

Prin

1

–2 –1 0 1 2 3 4 5

Prin 2

ABYB

ABYB

ABYB

ABYB

ABYB

External HyphaeSpore Density

ESYBESYB

ESYB

ESYB

ESYAESYA

JAXA

JAXA

JAXAJAXA

JAXB

JAXB

JAXB

JAXB

VPX

JMY

VPX

VPX

NAY

NAYNAY

NAXANAXA

NAXA

NAXA

AAY

AAY

DCY

DCY

DCYDCY

AAY

ACX

ACXACX

ACX

Septate Fungi

FGXCNX

VAX

VAXVAX

VAXVPXESX

ESX

ESXCNX

CNXAPY

APYFGX

FGX

FGX

FGX

FGY

FGY

FMYFMY

FBY

FBYFMY

ColonizationColonizationby vesiclesby Hyphae

ARY

DCY ABYAUAY

FBYGSYABYAUAY

UAYFBYFGYABYA DCY

ARY

CNXCNXCNX

VAXAPYFGY

GSYGSX

NAXB

ESYA

Figure 1 Vectors (arrow) and distribution of

sampling sites according to the principal

microbiological components. Prin1 (coloniza-

tion by hyphae and vesicles), prin2 (external

hyphae and spore density).


ª 2007 The Authors


The second physical and chemical principal compo-

nent 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 con-

tribute to liberating the phosphorus trapped by alumin-

ium 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

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 sug-

gest 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 oth-

ers 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 charac-

teristics: 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 coloniza-

tions (Figs 3a and 4a). In the valley the clusters had more

complexity than in the hilly terrain: the first group (clus-

ter 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; Schack-

Kirchner 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

Prin 1

3

2

2 3 4

1

1

0

0

–1

–1

–2

–2

–1.5

–1.5

–1.0

–1.0

–0.5

–0.5

0.0

0.0

0.5

0.5

1.0

1.0

1.5

1.5

2.0

ESYA

ESYA2.0

2.5

2.5

Prin 2

Prin 2

Prin 3

(a)

(b)

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)



ª 2007 The Authors

conditions can be decisive for the mycorrhizal develop-

ment in a tropical environment. There were micro-

biological 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 colo-

nizations 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 humid-

ities higher to 50% and temperatures above 31�C were

associated with B. decumbens root colonizations (up to

30% by hyphae and up to 5% by vesicles; microbiolog-

ical first principal component).

In conclusion, the effect of physical, chemical factors

of soil and environmental factors on the microbiologi-

cal variables (spore density, external hyphae, root colo-

nizations 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

SiteAAY

DCY

APY

JMY

NAY

ESYB

ABYA

FBY

UAY

ARY

ESYA

FGY

GSY

FMY

ABYB

Site

ACX

NAXB

NAXA

VPX

JAX1

JAX2

CNX

GSX

ESX

VAX

Average distance between clusters

Average distance between clusters

0·0 0·2 0·4 0·6 0·8 1·2 1·41·0 1·6

1

2

3

4

5

6

FGX

0·0 0·2 0·4 0·6 0·8 1·0 1·2 1·4 1·6 1·8 2·0

(a)

(b)

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.


ª 2007 The Authors


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 short-

cycle 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.

Acknowledgements

The authors thank the Amazonia University for financial

support and the use of installations; CORPOICA Titaitata

for soil analyses; Geovany Lara Zuluaga, Andres Olaya

Montes, Carlos Alberto Rodrıguez, Wilson Sanchez

Chacon, Adriana Patricia Sanchez Figueroa, Edith Medina

Giron of the Symbiotic Microorganisms Investigations

Team for their work and collaboration during its develop-

ment.

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V12·067

1·116

0·165

–0·787

–1·738

ABYBFMY

Non-linked SitesGSY

JMY

ESYB

Cluster 1 and 2

APY

ARY

AAYESYA

ABYA

DCYNAY

FBYFGY

UAY

–1·648 –0·696 0·256 1·208 2·160

W1

V12·025

2·025

1·102

1·102

0·179

0·179

–0·744

–1·666–1·666

W1–0·744

NAXBNAXA

VAX

VPX

Cluster 5 Cluster 4

Cluster 6

CNXGSX

ESX FGX

JAX1

JAX2

ACX

(a)

(b)

Figure 4 Canonical relationships between the environmental and soil

characteristics (W) and the microbiological variables (V). (a) In the hilly

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Journal of Applied MicrobiologyIncluding Letters in Applied Microbiology & Annual Symposium

Published on behalf of the Society for Applied Microbiology

Edited by:A. Gilmour

Print ISSN: 1364-5072Online ISSN: 1365-2672Frequency: MonthlyCurrent Volume: 110 / 2011

Editorial Information

Chief EditorA. Gilmour, Agri-Food and Biosciences Institute, Northern Ireland, UKFax: +44 (0) 28 90255009email: [email protected]

Managing EditorK. Brister, Wiley-Blackwell, Oxford, UKemail: [email protected]

EditorsB. Austin, Institute of Aquaculture, University of Stirling, Stirling, UKM.M. Bagdasarian, Michigan State University, East Lansing, MI, USAL. Baillie, Welsh School of Pharmacy, Cardiff University, Cardiff, UKM.D. Barton, University of South Australia, Adelaide, AustraliaE. Bartowsky, The Australian Wine Research Institute, Glen Osmond, AustraliaA.M. Bojesen, Department of Veterinary Disease Biology, University of Copenhagen, DenmarkA. Bosch, Universitat de Barcelona, Barcelona, SpainP. Calik, Middle East Technical University, Ankara, TurkeyM.L. Chikindas, The State University of New Jersey, New Brunswick, NJ, USAP.J. Collier, University of Abertay, Dundee, UKK.L. Cook, USDA-ARS Animal Waste Management Research Unit, Bowling Green, KY, USAJ.E. Cooper, Queen's University of Belfast, Belfast, UKD.A. Cowan, University of the Western Cape, Bellville, Capetown, South AfricaS.P. Cummings, School of Applied Sciences, Northumbria University, Newcastle upon Tyne, UKS.M. Cutting, Royal Holloway, University of London, UKL.M.T. Dicks, University of Stellenbosch, Matieland, South AfricaM. Dow, BioSciences Institute, University College Cork, Cork, IrelandN. Fegan, Food Science Australia, Brisbane, AustraliaC. Gilbert, Laboratoire de Microbiologie et Génétique Moleculaire, Université Claud Bernard Lyon, Lyon, FranceJ. Glassey, University of Newcastle Upon Tyne, Newcastle upon Tyne, UKA.E. Glenn, USDA-ARS Toxicology & Mycotoxin Research Unit, Athens, GA, USAP.C. Gowland, Staffordshire University, Stoke-on-Trent, UKD.A. Grinstead, Diversey Lever Innovation Center, Cincinnati, OH, USAJ. Guard, USDA/ARS, Athens, GA, USAJ.H. Hill, Department of Plant Biology, Iowa State University, Ames, IA, USAC.R. Jackson, USDA-ARS Resistance Research Unit, Athens, GA, USAF. Jorgensen, Health Protection Agency, Food Water and Environmental Microbiology Network, Porton Down, Salisbury, UKT. Kuchta, Food Research Institute, Bratislava, SlovakiaG. LaPointe, Laval University, Quebec, CanadaA. Leaphart, Clemson University, Clemson, SC, USAN. Lima, MUM, Minho University, Braga, PortugalJ. Lisle, US Geological Survey, Center for Coastal & Watershed Studies, St Petersburg, FL, USAG.T. Macfarlane, MRC Microbiology and Gut Biology Group, Ninewells Hospital and Medical School, Dundee, UKS. Macfarlane, University of Dundee, Dundee, UKJ.-Y. Maillard, Welsh School of Pharmacy, Cardiff University, Cardiff, UKD.V. Mavrodi, Washington State University, Pullman, WA, USAB. Mayo, IPLA-CSIC, Villaviciosa, SpainA. McBain, University of Manchester, Manchester, UKJ.A. McGarvey, USDA-ARS Plant Mycotoxin Research Unit, Albany, CA, USAA. Mohagheghi, National Renewable Energy Laboratory, Golden, CO, USAF. Mozzi, CERELA-CONICET, Tucumán, ArgentinaK. Nickerson, Biological Sciences, University of Nebraska, Lincoln, NE, USAD.R. Noguera, University of Wisconsin, Madison, WI, USAC.E. Nwoguh, Health Protection Agency, CEPR, Porton Down, Salisbury, UKG-J.E. Nychas, Department of Food Science & Technology, Laboratory Food Microbiology & Biotechnology of Foods, Athens,GreeceG.K. Paterson, Department of Veterinary Medicine, University of Cambridge, Cambridge, UKC.A. Phillips, University of Northampton, UKW. Qin, Lakehead University, Thunder Bay, CanadaC. Rees, University of Nottingham, Sutton Bonington, UKS. Roller, London South Bank University, London, UKC.P. Saint, SA Water Centre for Water Management and Re-use, University of South Australia, Mawson Lakes, AustraliaR. Seviour, Biotechnology Research Centre, La Trobe University, Bendigo, AustraliaP. Silley, MB Consult Limited, Hampshire, UKT.J. Smith, Biomedical Research Centre, Sheffield Hallam University, Sheffield, UKM.B. Taylor, Department of Medical Virology, NHLS/University of Pretoria, Pretoria, South AfricaK.Thomas, University of Sunderland, Sunderland, UKV.P. Valdramidis, University of Malta, MaltaA. Venâncio, Dept de Engenharia Biológica, Universidade do Minho, PortugalK. Venema, TNO Nutrition and Food Research, The NetherlandsT.M. Wassenaar, Molecular Microbiology and Genomics Consultants, Tannenstrasse, Zotzenhein, GermanyJ. Wells, USDA-ARS, Meat Animal Research Center, NE, USAR. Zdor, Andrews University, Berrien Springs, MI, USAX.-H. Zhang, College of Marine Life Sciences, Ocean University of China, Qingdao, China

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