2404
Diversity and fruiting patterns of ectomycorrhizal
and saprobic fungi as indicators of land-use
severity in managed woodlands dominated by
Quercus suber — a case study from southern
Portugal
Anabela Marisa Azul, Paula Castro, José Paulo Sousa, and Helena Freitas
Abstract: We assessed the impacts of current management practices used to control shrub strata in Portuguese oak woodlands dominated by Quercus suber L. (montado) on fruiting diversity and abundance of ectomycorrhizal-forming fungi
(ECMF) and saprobic fungi. Fruit bodies were collected over four fruiting seasons in 16 plots (20 m 20 m) selected in
a montado landscape with extensive silvopastoral exploitation. A total of 9484 fruit bodies were found in 171 taxa (74
ECMF, 96 saprobic, and 1 parasitic). Our results show that shrub density control by permanent grazing or by cutting practices followed by soil tillage leads to lower fruiting production and greater changes in taxa composition, particularly for
ECMF fruit bodies, than cutting practices without soil tillage. Principal response curve analysis showed that ECMF reacted
more sensitively to these practices, in particular Laccaria laccata, Hebeloma cistophilum, Russula cyanoxantha, Cortinarius trivialis, and Lactarius volemus. We also observed that shrub cutting without soil tillage allowed ECMF fruiting to recover to predisturbance levels after 3 years. Our data imply that fruit bodies were useful indicators for assessing the
severity of the effects of different land-use practices applied in montado areas on soil fungal populations.
Résumé : Nous avons évalué les impacts des pratiques d’aménagement présentement utilisées pour contrôler la strate arbustive dans les forêts portugaises de chêne dominées par Quercus suber L. (montado) sur la diversité et l’abondance des
fructifications des champignons ectomycorhiziens (CEM) et des champignons saprobies. Les fructifications ont été collectées pendant quatre saisons dans 16 parcelles (20 m 20 m) choisies dans un paysage montado soumis à une exploitation
sylvopastorale extensive. Au total, 9484 fructifications appartenant à 171 taxons ont été récoltées (74 CEM, 96 saprobiontes et un parasite). Nos résultats montrent que le contrôle de la densité des arbustes par le pâturage permanent ou par
des pratiques de coupe suivie d’un travail du sol causent de plus grandes pertes de production de fructifications et des
changements dans la composition des taxons plus importants, particulièrement dans le cas des fructifications de CEM, que
les pratiques de coupe sans travail du sol. L’analyse de la courbe principale de réponse a montré que les CEM ont réagi
avec plus de sensibilité à ces pratiques, en particulier Laccaria laccata, Hebeloma cistophilum, Russula cyanoxantha, Cortinarius trivialis et Lactarius volemus. Nous avons aussi observé que la coupe des arbustes sans travail du sol permettait
aux fructifications de CEM de retrouver les niveaux qui existaient avant l’intervention après 3 années. Nos données signifient que les fructifications sont des indicateurs utiles pour évaluer la sévérité des effets de différentes pratiques d’utilisation des terres appliquées dans les zones montado sur les populations fongiques dans le sol.
[Traduit par la Rédaction]
Introduction
Quercus suber L. (cork oak) woodlands are widespread in
the Mediterranean Basin and cover about 2.2 106 ha in
Europe (Portugal, Spain, France, and Italy) and North Africa
(Morocco, Algeria, and Tunisia). Portugal has the largest
Received 6 January 2009. Accepted 14 September 2009.
Published on the NRC Research Press Web site at cjfr.nrc.ca on
9 December 2009.
A.M. Azul,1 P. Castro, and H. Freitas. Centre for Functional
Ecology, Department of Life Sciences, University of Coimbra,
3001-455 Coimbra, Portugal.
J.P. Sousa. Institute of Marine Research (IMAR), Department of
Zoology, University of Coimbra, 3001-455 Coimbra, Portugal.
1Corresponding
author (e-mail: amjrazul@ci.uc.pt).
Can. J. For. Res. 39: 2404–2417 (2009)
area of Q. suber woodlands (737 103 ha), and most of
these woodlands are under silvopastoral exploitation. This
system is characterized by open oak formations of Q. suber
and Quercus rotundifolia L. (holm oak), usually combined
with a rotation of cultures–pastures–fallow. These agrosilvopastoral ecosystems are well adapted to the Mediterranean environment, and their low levels of disturbance play
an important role in overall ecological diversity and dynamics (Pinto-Correia 1993; Decocq et al. 2004; Azul et al.
2009).
For centuries, managed oak woodlands have combined the
two key aspects of land management: production and conservation. Because of their social and economic benefits,
they represent a good example of sustainable agroforestry
practice in Europe (Council of Europe 1992). However, during the twentieth century, the intensification and extensification of land-use practices induced severe changes in the
doi:10.1139/X09-148
Published by NRC Research Press
Azul et al.
montado landscape (Pinto-Correia and Mascaranhas 1999;
Nunes et al. 2005).
Soil microorganisms influence or directly control most of
the functional processes occurring in the belowground ecosystem such as nutrient cycling, moisture retention, and
erosion protection. Among the vast array of soil microorganisms, ectomycorrhizal-forming fungi (ECMF) and saprobic
fungi are key components of soils and forests. Both contribute to the structure and physical and chemical properties of
soil, and play important roles in the development of disease
suppression in soils (Smith and Read 2008). ECMF develop
symbiotic structures on fine-root tips and form a complex
belowground network, and they are amply recognized for
their species-specific benefits to plants, including the uptake
of the mineralized and organic forms of phosphorus and nitrogen (Högberg and Högberg 2002; Read and Perez-Moreno 2003). Previous work has revealed that ectomycorrhizal
(ECM) fungal communities belowground in the Portuguese
montado are quite diverse in composition and structure and
are significantly affected by land-use practices (Azul 2002;
Azul et al. 2009). The same study showed that ECM fungal
diversity was positively correlated with the low mortality of
Q. suber and with certain land-use regimes, in particular
those based on silvopastoral exploitation where shrub density is artificially maintained at levels of up to 35% of the
total vegetation cover.
The link between shrub management and fruit-body production has not yet been investigated in managed Q. suber
woodlands. Factors driving fungal diversity remain unclear,
and little is known about the effects of land use on fruiting
patterns of ECMF and saprobic fungi. We hypothesize that
fruit-body richness and abundance can be used as sensitive
indicators of the effects of current shrub management practices in Portuguese montados.
The assessment of forest fungal diversity and dynamics
can be difficult because production depends on many interactive factors involved before and during the fungal fruiting
period, including the abiotic environment (rainfall, temperature, relative humidity, evapotranspiration, water content,
and edaphic characteristics), silvocultural practices (tree species, stand age, density, and distribution of vegetation
cover), ecology (community composition, competition, reproduction strategies), landscape (altitude, aspect, and
slope), and management practices (cork removal, grazing,
soil tillage frequency and intensity, fire, wildlife management, introduced species). Our approach may, therefore,
provide valuable data to study the robustness of fruit-body
surveys as indicators of a fungal population’s sensitiveness
to land use in montado areas. Such information could be of
great interest for ecosystem monitoring and fungal conservation, particularly to stakeholders interested in developing
sustainable practices involving nonwood forest products
(e.g., the production of edible wild mushrooms).
Our main goal was to evaluate the effects of land-use
practices employed to control shrub density in managed Q.
suber woodlands on fruit-body production. In this case
study, we selected 16 plots located in the leading cork production area in Portugal: the Alentejo region. The diversity
and abundance of ECMF and saprobic fungi fruit bodies
were monitored over four fruiting seasons in a montado
landscape under extensive silvopastoral exploitation. We
2405
also compared the performance of these indicators to assess
the effects of shrub management regimes on macrofungus
fruit-body community dynamics and vulnerability.
Materials and methods
Study site
Fieldwork was conducted in a managed oak woodland
dominated by Q. suber, typically called montado. The sampling sites were located in Foros Vale Figueira (Montemor-oNovo, Portugal) (38841’10@N, 08820’23@W). Cork is the main
product and is harvested every 9 years; cattle breeding is the
second most lucrative economic activity. Oak formation is
dominated by Q. suber (40–60 trees/ha), but holm oak is also
present. At soil level, sclerophyllous evergreen Mediterranean species dominate, with Cistus salvifolius L., Cistus
crispus L., Cistus ladanifer L., Genista triacanthus Brot., and
Lavandula pedunculata Miller., which represent almost 65%
of the total shrub density. Soils are classified as Orthic Luvisols, with organic layers varying according to the type of soil
management and the year of perturbation; pH is slightly
acidic, ranging from 4.5 to 5.7. The climate is Mediterranean,
characterized by a marked dry season in summer and precipitation occurring mainly from autumn to mid-spring. Temperatures range from 7.5 (mean average in January) to 24 8C
(mean average in July).
Land-use management practices are focused on cork production and silvopastoral exploitation. Shrub management is
required to reduce the risk of fire (Nunes et al. 2005).
Experimental design
Sixteen plots of 20 m 20 m were selected randomly in
four areas of montado across a managed oak woodland landscape with silvopastoral exploitation (total area sampled,
4 4 400 m2 = 6400 m2), representing the current shrub
control practices. The plots were distributed randomly
among the four montado areas, and we assumed that fruiting
incidence per plot was totally independent of the fruiting incidence of the neighbouring plots. The four areas included
(i) the control (C), with no intervention during the study period or the preceding 5 years, with shrubs occupying 65%–
75% of vegetation cover; (ii) the cut plots (Cu), with shrub
management using machinery to cut the plant shoots without
tilling the soil; (iii) the cattle plots (Ca), with shrub density
controlled by permanent grazing of cows and sheep; and (iv)
the mobilized plots (M), with shrub management using machinery to cut plant shoots and till the soil.
Shrub management practices were implemented when
shrubs accounted for 65%–75% of total vegetation cover
and when plants were 4–5 years old; the cutting techniques
mentioned above were performed in early autumn 2004.
Fruit-body assessment was conducted between 2003 and
2006.
Assessment of fruit bodies
Epigeous fruit bodies were monitored every 10 days during the main fruiting period, from September to December,
over four consecutive fruiting seasons. Fruit-body production of both ECMF and saprobic fungi was taken into account. Observations did not include species forming
microscopic, hypogeous, or resupinate fruit bodies, with the
Published by NRC Research Press
2406
exception of the Thelephoraceae family, a group largely unexplored in these ecosystems.
Fruit bodies were counted and identified to species level
according to Bon (1988). Fruit-body sampling consisted of
only a minimal number of specimens for identification and
voucher collections. The vouchers were deposited in the herbarium of COI (Coimbra, Portugal). A pictorial database for
all reported taxa (Tables A1 and A2, in Appendix A) is
available from the corresponding author.
Data analysis
Taxon abundance was estimated as the cumulative number of fruit bodies produced by a given taxon during the
four consecutive fruiting seasons studied. The method
chosen was quantification of the fruit bodies instead of biomass analysis because different species produce different
sizes of mushroom, and biomass measurements would obscure abundant fruiting of smaller fruited individuals. Species frequency refers to the number of times (percentage
values) that a given taxon fruited during the sampling period. Fruit-body production was defined as the total number
of fruit bodies counted over the study period.
Species diversity at each plot was estimated by the following descriptors: (i) species richness, that is, the total
number of taxa found per plot (S), (ii) Shannon diversity index (H), (iii) Simpson’s diversity index (l), (iv) Pielou’s
evenness index (H’), (v) Margalef index (D), and (vi)
Berger–Parker index (d) (Magurran 1988). The Shannon index is sensitive to rare species. The Berger–Parker index accounts for both richness and relative abundance and displays
the proportional importance of the most dominant species.
An analysis of variance was performed using ANOVA
general linear model (SPSS1 for Windows). One-way ANOVA was used to compare all diversity indexes among
land-use practices. Normality and homoscedasticity were
tested by the Kolmogorov–Smirnoff and Bartlett’s tests, respectively. All univariate statistical analyses were performed
using STATISTICA version 6.0 software package.
The relationships between fruit-body abundance and landuse practices at ground level were evaluated using the multivariate technique principal response curve (PRC) analysis
(Van den Brink and Ter Braak 1999), a novel method for
time-dependent multivariate responses of biological communities to stress. This method was developed to analyse
data from mesocosm experiments in aquatic ecotoxicology
(Van den Brink and Ter Braak 1999), and has rarely been
applied in terrestrial ecological studies (Frampton et al.
2000a, 2001). This method is particularly suitable when the
focus is not on the temporal changes of biological communities within treatments (the montado areas, in this case), but
on the changes observed over time in the treated communities (the Cu, Ca, and M areas in this case) in comparison
with the community in the control (the C area). The PRC
method is based on a redundancy analysis (the abbreviated
form of a principal component analysis), and the statistical
model for species abundance data is Yd(j)tk = Y0tk + bkcdt +
3d(j)tk, where Yd(j)tk is the abundance of species k in replicate
j of area d on sampling date t, Y0tk is the mean abundance of
species k on date t in the control area d0, cdt is the response
pattern for every site d on sampling date t, bk is the weight
of each species with this current response pattern, and 3d(j)tk
Can. J. For. Res. Vol. 39, 2009
is an error term with mean zero and variance s 2k . The PRC
creates a graphical representation with time (sampling dates)
as a horizontal line and the response pattern (cdt) of each
area d at each time t in relation to control site on the vertical
axis (by definition, the response pattern of the control at any
time t (c0t) is set to zero, thus limiting any time changes to
those occurring in the control community). When the coefficients cdt are plotted for each time point, the resulting PRC
diagram displays a curve for each area that can be interpreted as the PRC of the community in comparison with
that of the control area (Van den Brink and Ter Braak
1999). The species weight bk indicates how closely the response of each individual taxon matches the overall community response as displayed in the PRC diagram. When
depicted in parallel with the PRC diagram, species weights
allow a comprehensive evaluation of the contribution of individual species to the observed differences. Significant differences between treatment areas and the control at each
time point were determined by using a one-way ANOVA
test on the sample (plot) coordinates derived from the redundancy analysis, followed by a Dunnet’s test when significant
differences were found. Homoscedasticity and normality of
the data were evaluated by Bartlett’s and Kolmogorov–
Smirnoff tests, respectively. PRC analysis was performed
using the CANOCO software package version 4.5 (Ter
Braak and Smilauer 2002). Monte Carlo permutation tests
were used to assess the significance of these relationships
and also of the canonical axes obtained. ANOVAs were performed using STATISTICA version 6.0 software package.
Results
Overview of the macromycete community
In total, 9484 fruit bodies of macromycetes were recorded
in the 16 experimental plots during four consecutive fruiting
seasons. One hundred and seventy-one taxa were identified,
consisting of 74 ECMF, 96 saprobic fungi, and 1 parasitic
fungus, most of them at the species level (Tables A1 and
A2 in Appendix A). The families Russulaceae and Tricholomataceae were the best represented with 22 and 24 taxa, respectively (Tables A1 and A2). Overall, 38 families were
present in the experimental plots.
ECMF accounted for 61% of all fruit bodies, represented
by 19 genera, mainly members of Russula, Tomentella,
Amanita, Boletus, and Lactarius (Table A1). The ECMF
species Astraeus hygrometricus (Pers.) Morgan and Laccaria
laccata (Scop.) Cooke were the most abundant with 1928
and 1891 fruit bodies, respectively, amounting to 40% of
the total fruiting production (Table A1). ECMF exhibited
some heterogeneity in fruiting patterns. We recorded genera
with high species richness and high productivity (e.g., Russula), genera with high species richness but low productivity
(e.g., Amanita), genera with few species but high productivity (e.g., Laccaria), and genera with few species and low
productivity (e.g., Paxillus). The ECMF community consisted of a large number of broad host range temperate species, but up to 20% were strictly Mediterranean species.
The saprobic community was represented by 56 genera,
88% of which were basidiomycetes (Table A2). The families
Tricholomataceae, Agaricaceae, and Coprinaceae were the
best represented, accounting for 46% of the saprobic taxa
Published by NRC Research Press
Azul et al.
2407
Table 1. Estimators of diversity (mean ± SD) for ectomycorrhizal-forming fungi (ECMF) and saprobic fungi.
Community
ECMF
Saprobes
Diversity
index
S
A
H
H’
l
D
d
S
A
H
H’
l
D
d
C
18 ± 7
191 ± 114
2.75 ± 0.52
0.68 ± 0.07
4.49 ± 1.44
3.23 ± 1.15
0.41 ± 0.08
7±5
42 ± 41
1.80 ± 1.01
0.63 ± 0.33
3.14 ± 1.92
1.65 ± 1.01
0.42 ± 0.25
Cu
13 ± 9
116 ± 115
2.11 ± 1.15
0.61 ± 0.20
3.82 ± 2.85
2.64 ± 1.63
0.56 ± 0.26
6±5
55 ± 75
1.88 ± 0.84
0.71 ± 0.25
3.05 ± 1.88
1.52 ± 0.84
0.50 ± 0.28
Ca
4±3
47 ± 29
1.10 ± 0.74
0.54 ± 0.27
1.82 ± 1.11
0.82 ± 0.55
0.69 ± 0.28
7±3
62 ± 45
2.08 ± 0.60
0.76 ± 0.11
3.51 ± 1.23
1.61 ± 0.60
0.48 ± 0.16
M
1±1
7 ± 10
0.53 ± 0.59
0.38 ± 0.43
0.94 ± 0.76
0.47 ± 0.57
0.58 ± 0.44
8±5
72 ± 101
1.93 ± 0.87
0.71 ± 0.23
3.41 ± 2.00
1.76 ± 0.82
0.44 ± 0.20
Differences among
land uses
F[3,63] = 27.7; p<0.001
F[3,63] = 15.2; p<0.001
F[3,63] = 19.6; p<0.001
F[3,63] = 3.2; p<0.05
F[3,63] = 14.8; p<0.001
F[3,63] = 19.1; p<0.001
F[3,63] = 2.5; ns
F[3,63] = 0.4; ns
F[3,63] = 0.5; ns
F[3,63] = 0.4; ns
F[3,63] = 0.8; ns
F[3,63] = 0.2; ns
F[3,63] = 0.2; ns
F[3,63] = 0.4; ns
Note: C, control; Cu, shrub cutting without soil tillage; Ca, shrub density controlled by grazing; M, shrub cutting with soil tillage. S, species richness; A abundance; H, Shannon diversity index; H’, Pielou’s evenness index; l, Simpson’s diversity index; D, Margalef index; d,
Berger–Parker index.
Table 2. Total number of taxa identified and fruit-body production over 4 years of fruiting.
C
Community
ECMF
Saprobes
Total
% ECMF in the global
fungal community
Taxa
56
35
91
62
Cu
Fruit bodies
3051
670
3721
82
Taxa
53
27
80
66
Ca
Fruit bodies
1855
885
2740
68
Taxa
13
31
44
30
M
Fruit bodies
756
993
1749
43
Taxa
11
58
69
16
Fruit bodies
118
1156
1274
9
Note: C, control; Cu, shrub cutting without soil tillage; Ca, shrub density controlled by grazing; M, shrub cutting with soil tillage.
(Table A2). A similar tendency for heterogeneity in fruiting
patterns was also observed among saprobes.
Fruiting macromycetes with economic interest were represented by 19 edible mushroom taxa (58% ECMF) as well as
the medicinal species Ganoderma lucidum (Curtis) P. Karst.,
Schizophyllum commune Fr., Trametes versicolor (L.) Lloyd,
and Russula delica Fr.
Influence of land-use regimes on fungal community
structure
Fruit-body surveys during the study period revealed sharp
differences in fruiting diversity and abundance depending on
the type of shrub management practice adopted (Table 1).
These variations were particularly evident in the ECMF
community, where significant differences among the four
areas were observed for most indices (Table 1). Higher diversity values were obtained in the control plots (C) and in
the plots where shrub strata were cut using machinery without soil tillage (Cu). Lower diversity values were found in
the plots where the shrub layer was controlled using machinery followed by soil tillage (M). The mean abundance of
ECMF in the C plots was 1.6, 4.0, and 26.0 times higher
than that in the Cu, Ca, and M plots, respectively (Table 1).
The richness and abundance of saprobic fungi were less
affected by these practices. No significant differences were
observed in the diversity descriptors among the four shrub
management strategies evaluated (Table 1). However, we
noticed that saprobe abundance was lower in the C and Cu
plots. Saprobic fungi were more abundant in the M plots
where soil was tilled (Table 1).
Different effects of shrub management practices were
clearly noticed on fruit-body diversity and abundance over
the 4 years (Table 2). Under C and Cu practices, ECMF accounted for 64% of the global macromycete community,
which is two and four times higher than the percentage obtained in the Ca and M plots, respectively. Although ECMF
richness was similar in C and Cu plots, the number of fruit
bodies dwindled by almost 61% under Cu practices when
compared with the control. In M plots, ECMF accounted
for only 11 taxa (9%) of the total fruit bodies monitored
(Table 2).
The clumpy distribution of fruit bodies was particularly
noticeable for Astraeus hygrometricus, Laccaria laccata,
and Hebeloma cistophilum Maire in C plots, in which these
fruiting ECMF accounted for 39% of total fruit-body production. Patchiness in the ECMF community was consistently observed in the control areas over the study period,
except in 2005, a year of scarce rainfall. In contrast, in the
M plots, clumps were observed for the fruiting saprobes
Marasmius quercophilus Pouzar and Infundibulicybe geotropa (Bull.) Harmaja (Table A2).
Shrub management practices also influenced the fruiting
macromycete production and patterns of both rare and frequent species (Tables A1 and A2). Diversity and abundance
of edible and medicinal macromycetes followed the same
fruiting patterns as those of the general fruit-body community.
Published by NRC Research Press
2408
Fig. 1. Principal response curves showing the response of fruiting
ectomycorrhizal-forming fungi and saprobes to different land-use
practices to control shrub density in managed oak woodlands dominated by Quercus suber (C, control; Cu, shrub cutting without soil
tillage; Ca, shrub density controlled by grazing; M, shrub cutting
with soil tillage) (ANOVA results: 2003: F[3,12] = 8.85, P < 0.01;
2004: F[3,12] = 20.01, P < 0.001; 2005: F[3,12] = 10.86, P < 0.001;
2006: F[3,12] = 13.26, P < 0.001).
Can. J. For. Res. Vol. 39, 2009
Statistical differences over time (PRC analysis) were found
between the C plots and the Ca and M plots during the 4
year study. Significant differences between C and Cu plots
were only found in 2004 (Fig. 1), which corresponded with
the occurrence of a disturbance, that is, shrub removal.
Temporal variation in species richness and abundance of
fruit bodies was less evident in the Ca plots (Fig. 3). Temporal variation in the richness and abundance of fruiting
ECMF species was rather low also in the M plots, that is,
those with soil tillage (Fig. 3).
PRC analysis (Fig. 1) showed that shrub management
consisting of cutting with soil tillage did not lead to the recovery of fruiting macromycetes in terms of species composition 3 years after the disturbance.
Discussion
We observed 13 edible taxa (nine ECMF and four saprobes)
during the monitored period. Richness of edible ECMF fruit
bodies was 1.8 times higher in the C plots than in the Cu plots
and 9 times higher than in the Ca and M plots. Richness of
edible saprobes was higher in the C and M plots (both with
four taxa). Three edible saprobe taxa were observed in the Ca
and Cu plots. Fructification was 4.1 times higher in the C plots
(203 fruit bodies) than in the Cu (49 fruit bodies) and M plots
(50 fruit bodies), and 5.6 times higher than in the Ca plots (36
fruit bodies).
The PRC analysis (Fig. 1) showed an apparent spatial gradient related to the procedures used to control shrub density,
which explained 44.1% of the total variance. This analysis
approximated the control with the plots where shrubs were
cut with machinery without soil tillage. The same analysis
also revealed that shrub density controlled by cattle grazing
or using machinery followed by soil tillage lead to higher
deviations in species composition. Sampling data accounted
for 7.8% of the total variance. Monte Carlo permutation
tests revealed that the differences among the treatment areas
and sampling times were statistically significant (P < 0.04),
with time of sampling contributing 6% of the total variance
in abundance. Deviation in species composition was more
significant for the fruiting ECMF (Fig. 2; Table A1). Within
this community, the species most affected were Laccaria
laccata, Hebeloma cistophilum, Russula cyanoxantha
(Shaeff.) Fr., Cortinarius trivialis J. E. Lange, Lactarius volemus Fr., Lactarius aurantiacus (Pers.) Gray, Russula foetens (Pers.) Pers., Russula sororia (Fr.), Romagn, Russula
amoenolens Romagn, Amanita phalloides (Vaill. Ex Fr.)
Link, Russula delica Fr. and Lactarius chrysorrheus Fr. By
contrast, the specie Lactarius atlanticus Bon appeared to be
less influenced by the shrub cutting practices employed.
Temporal variations in fungal community
The influence of land-use regimes in fungal composition
differed by fruiting season. ECMF showed higher temporal
dispersion compared with saprobic fungi (Figs. 1 and 3).
Macromycete community
In Portugal, a few studies have reported the fruit-body diversity associated with Q. suber, and none have been conducted in oak woodlands to determine the effects of
management practices. Our study represents the first attempt
to evaluate the robustness of fruit-body surveys as indicators
of the status of fungal populations subjected to different silvopastoral practices in managed oak woodlands. Our work
demonstrated that Portuguese montados under extensive silvopastoral exploitation comprise a high diversity of fruiting
macromycetes (74 ECMF, 96 saprobic fungi, 1 parasitic fungus). These results are comparable to those found in an oldgrowth Quercus ilex L. (holm oak) forest (Richard et al.
2004) as well as in old-growth coniferous forests in Europe
(O’Dell et al. 1999; Peter et al. 2001; Bonet et al. 2004;
Fernández-Toirán et al. 2006).
The Russulaceae family had the highest diversity among
ECMF macromycetes in managed oak woodlands. The predominance of Russulaceae was observed belowground in Q.
suber woodlands under different land uses (Azul 2002; Azul
et al. 2009). A similar tendency has been reported in Mediterranean forests (Richard et al. 2005; Bergemann and
Garbelotto 2006; Courty et al. 2008) and in the Northern
Hemisphere (Avis et al. 2003; Tedersoo et al. 2003;
Lilleskov et al. 2004). Russulaceae includes a very large array of species with diverse ecological requirements, which
may contribute to its domination in forest systems. Further
investigations are needed to assess the functional importance
of this family in soil processes, particularly in Mediterranean areas increasingly exposed to environmental problems
such as soil degradation (Pinto-Correia 1993; Mouillot et al.
2005; Rios-Dı́az et al. 2006), drought (European Environment Agency 2004), or diseases (Brasier and Scott 2008).
Impacts of shrub management on fruit-body abundance
and diversity
Fruit-body surveys revealed that ECMF were more sensitive to shrub management, and their response reflected a
trend in the severity of the land-use techniques used to control shrub density in montado. As evidenced by our results,
the richness of ECMF was 5.1 and 4.3 times higher in the
control plots than in the areas where shrubs were cut followed by soil tillage and those controlled by cattle, respectively. The understorey shrubs in the studied oak woodlands
Published by NRC Research Press
Azul et al.
2409
Fig. 2. Taxa weightiness (bk) derived from the principal response curve analysis indicating the relative contribution of individual taxa to the
macromycete community response to current shrub management techniques, applied in the four experimental stands. Taxa presenting the
highest positive bk values were the most affected by the shrub management techniques (lower fruiting abundance when compared with control); taxa with the most negative bk values were less affected by the shrub control techniques (higher fruiting abundance when compared
with control). Taxa with a bk value around zero had fruiting abundance values that were similar to those of the control.
are dominated by Cistus spp. These species mainly form ectomycorrhizal associations (Molina et al. 1992; Comandini
et al. 2006). We observed that Amanitaceae, Boletaceae,
Russulaceae, Tricholomataceae, and some species of Gasteromycetes, e.g., Astraeus hygrometricus, recorded as being
directly associated with Cistus spp. roots (Comandini et al.
2006), were significantly affected by shrub control practices,
in particular when cutting followed by soil tillage was used.
Disturbances caused by clear-cutting practices have been
shown to have significant impacts on the diversity and composition of ECMF (Hagerman et al. 1999; Byrd et al. 2000;
Smith et al. 2005). Therefore, the removal of understorey
shrubs is likely to affect the ECM fungal community in
montado as well (Azul 2002; Azul et al. 2009), with a cost
to the fruit-body production. Agroforestry practices, in particular the use of machinery and livestock, are also known
causes of soil compaction, which, in turn, affects soil water
content and plant growth (Bouwman and Arts 2000; Hamza
and Anderson 2005) and may possibly directly affect fruitbody production.
ECMF fruit bodies dominated the fruit-body community
with 70% and 80% of these fungi monitored in Cu and C
plots, respectively. Similar ECMF/saprobic fungi ratios
were reported by Richard et al. (2004) in an old-growth Q.
ilex forest with no artificial perturbation at soil level. The
higher abundance of ECMF fruit bodies in C and Cu plots
highlights the potential influence of vegetation cover on
macromycetes fruiting patterns, which may be explained by
the positive correlation observed between symbiotic fungi
with photosynthates and living roots (Nara et al. 2003),
while saprobic fungi depend more on wood debris. Mycelia
of saprobic fungi have been shown to remobilize and translocate biomass and store mineral nutrients (Boddy 1999),
and many ECM fungal species likely have similar functions
(Abuzinadah and Read 1986; Perez-Moreno and Read
2000). Moreover, Högberg et al. (1999) showed that nutrient
Published by NRC Research Press
2410
Can. J. For. Res. Vol. 39, 2009
Fig. 3. Temporal variation in fungal community richness and abundance (ectomycorrhizal-forming fungi (ECMF) and saprobic fungi) as
result of land-use practices used to control shrub density (C, control; Cu, shrub cutting without soil tillage; Ca, shrub density controlled by
grazing; M, shrub cutting with soil tillage).
mobilization in ECM fungal species was closely related to
specific phytobiont sources, in particular the generalist fungi
that received most of their carbon from the upper-canopy
trees. These findings convey the notion that shrub management not only influences the activity of the interacting mycelial systems but the specificity of mycobiont–phytobiont
associations as well. The absence–disappearance of mycorrhizal hosts, however, might not always imply the absence
of inoculum in the soil. Bergero et al. (2003) found that ericoid mycorrhizal fungi may persist and maintain mycorrhizal viability in habitats lacking ericaceous hosts. A
supporting argument is the ability of some ericoid fungi to
be tightly associated with Q. ilex (Bergero et al. 2000).
Management consisting of cutting practices without soil
tillage appeared to be the best technique to sustain ECMF
community resilience. Cistus spp. roots most likely survive
after cutting and resprout during the succeeding 2 years,
helping the recovery of ECMF richness and abundance after
3 years. This procedure preserves the root systems of both
live and dead roots, thereby contributing to the survival of
mycorrhizal tips and mycelial network functioning.
Hagerman et al. (1999) reported that mycorrhizal tips may
survive in the roots of cut trees for up to 3 years after
clear-cutting. Mycorrhizal associations and hyphal networks
are known to facilitate the sharing of resources such as carbon, nutrients, or water (Southworth et al. 2005; Simard
2009), thereby influencing soil processes and plant community dynamics. Thus, fungal recovery after a disturbance is
essential for sustaining ecosystem ecological processes.
Cattle husbandry represents another montado exploitation
activity that is central to the regional economy. In this case
study cattle grazing was demonstrated to be efficient at controlling shrub density, but caution is recommended, since
perceptible disturbance was observed on mushroom production and diversity. The permanent presence of cattle, even
though restricted to a limited number of individuals, implies
multiple ecological consequences, as different plant species
respond differently to herbivory (Ayres et al. 2004). Our results call for further research to investigate the influence of
livestock on ECMF, particularly its implications on fungivory, nitrogenous inputs, and soil compaction provided by
the animals.
We observed that climate conditions greatly affected fruitbody diversity and abundance in montado, as has been
found by other studies (O’Dell et al. 1999; Martı́nez de
Aragón et al. 2007). Drought conditions clearly reduced
macromycete fructification in the control plots. However, as
stated above, the absence of ECMF fruit bodies may not reflect the ECM fungal functioning below ground. Previous
studies conducted in montados have reported high diversity
in the ECM fungal community below ground, even under
drought conditions (Azul 2002; Azul et al. 2009). Despite
the constraints in assessing fruit-body production due to the
abiotic environment, mainly low precipitation and high temperatures, it was possible to produce effectual information
concerning the impacts of shrub management on ECMF and
saprobic fungi diversity and abundance in montado areas.
The synergistic use of quantitative and qualitative data to
assist with complex planning involving multiple objectives
and decision makers has been addressed by Martins and
Borges (2007). Agrosilvopastoral management planning
should be viewed as a strategic process organized in differPublished by NRC Research Press
Azul et al.
ent phases, where basic biological and ecological information are included in the decision model, together with qualitative and quantitative information, including the selection
of specific areas to preserve the maximum ecosystem integrity. With the increasing use of wild mushrooms as an important economic resource, we believe that fruit-body
surveys should be incorporated in management strategies
for mycological resources.
Some of the criteria to consider in selecting bioindicators
are that they be readily accessible, represent vital habitat
features or processes, and be sensitive to ecosystem alterations (Ferris and Humphrey 1999). Although results cannot
be generalized for forests where shrub density is controlled,
fruit-body abundance and diversity were measurable and reproducible in the Portuguese montado areas and were sensitive indicators of the fungal population’s vulnerability to
current techniques applied to control shrub density. We believe that fruit-body production may be a good indicator of
and a powerful tool for explaining the ecological impacts of
land use on the soil fungal community.
Acknowledgements
The authors thank Fernanda Azul for technical assistance
in the field. The authors are also grateful to S.R. Costa for
critical reading of the manuscript. We also thank the three
anonymous reviewers for their valuable suggestions. Financial support was provided by FCT-MCTES (Portuguese
Foundation for Science and Technology) and European fund
FEDER, project POCTI/AGG/ 42349/ 2001. A.M. Azul was
supported by an individual grant from FCT-MCTES,
(SFRH7BPD/5560/2001).
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Appendix A
The Appendix begins on the following page.
Published by NRC Research Press
Taxon
Amanita battarrae (Boud.) Bon
Amanita cesarea (Scop.) Pers.
Amanita franchetii (Boud.) Fayod
Amanita muscaria (L.) Lam.
Amanita pantherina (DC.) Krombh.
Amanita phalloides (Vaill. ex Fr.) Link
Amanita rubescens Pers.
Amanita vaginata (Bull.) Lam.
Astraeus hygrometricus (Pers.) Morgan
Boletus aereus Bull.
Boletus appendiculatus Schaeff.
Boletus edulis Bull.
Boletus porosporus Imler ex Bom & G.
Moreno
Boletus reticulatus Schaeff.
Boletus satanas Lenz
Bovista aestivalis (Bonord.) Demoulin
Bovista plumbea Pers.
Cortinarius amoenolens Rob. Henry ex P.D.
Orton
Cortinarius trivialis J.E. Lange
Cortinarius variicolor (Pers.) Fr.
Hebeloma cistophilum Maire
Hebeloma sp. 1
Hebeloma sp. 2
Helvella acetabulum (L.) Quél.
Helvella queletii Bres.
Inocybe asterospora Quél.
Inocybe cookei Bres.
Inocybe rimosa (Bull.) P. Kumm.
Laccaria laccata (Scop.) Cooke
Lactarius atlanticus Bon
Lactarius aurantiacus (Pers.) Gray
Lactarius chrysorrheus Fr.
Lactarius quietus (Fr.) Fr.
Lactarius rugatus Kühner & Romagn
Lactarius volemus (Fr.) Fr.
Lactarius zonarius (Bull.) Fr.
Paxillus involutus (Batsch) Fr.
Peziza badia Pers.
Peziza sp.
12
10
2
5
2
22
0
5
491
18
4
3
1
2
1
11
0
4
131
23
323
7
0
7
6
1
0
10
1120
0
52
42
16
6
56
1
1
11
39
Thermophilic
Thermophilic
Broad
Broad
Broad
Angiosperms
Angiosperms
Cistus specific
—
—
Broad
Angiosperms
Quercus sp.
Broad
Broad
Broad
Broad
Broad
Quercus sp.
Quercus sp.
Quercus sp.
Quercus sp.
Quercus sp.
Broad
Broad
Broad
A
Host range
Broad
Thermophilic
Broad
Broad
BroadR
Broad
Broad
Broad
Broad
Thermophilic
Angiosperms
Broad
Broad
C
4.29
0.75
10.59
0.23
0.00
0.23
0.20
0.03
0.00
0.33
36.71
0.00
1.70
1.38
0.52
0.20
1.84
0.03
0.03
0.36
1.28
0.07
0.03
0.36
0.00
0.13
RA
0.39
0.33
0.07
0.16
0.07
0.72
0.00
0.16
16.09
0.59
0.13
0.10
0.03
3
2
4
3
0
2
1
1
0
4
4
0
4
3
1
1
3
1
1
1
3
1
1
1
0
2
FR
4
3
2
2
1
3
0
1
4
3
1
3
1
25
0
212
1
1
0
0
0
20
67
81
4
27
0
1
1
55
3
0
2
4
9
0
17
8
0
A
10
0
0
4
2
52
7
10
962
0
0
0
0
Cu
1.35
0.00
11.43
0.05
0.05
0.00
0.00
0.00
1.08
3.61
4.37
0.22
1.46
0.00
0.05
0.05
2.96
0.16
0.00
0.11
0.22
0.49
0.00
0.92
0.43
0.00
RA
0.54
0.00
0.00
0.22
0.11
2.80
0.38
0.54
51.86
0.00
0.00
0.00
0.00
2
0
3
1
1
0
0
0
1
3
2
1
2
0
1
1
2
1
0
1
1
1
0
2
1
0
FR
2
0
0
3
2
3
2
2
4
0
0
0
0
0
0
29
0
0
0
0
0
0
8
29
3
0
0
0
0
0
0
0
45
0
0
0
136
43
0
0
0
0
0
0
0
0
0
438
0
0
0
0
A
Ca
0.00
0.00
3.84
0.00
0.00
0.00
0.00
0.00
0.00
1.06
3.84
0.40
0.00
0.00
0.00
0.00
0.00
0.00
0.00
5.95
0.00
0.00
0.00
17.99
5.69
0.00
RA
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
57.94
0.00
0.00
0.00
0.00
0
0
2
0
0
0
0
0
0
1
2
1
0
0
0
0
0
0
0
4
0
0
0
2
2
0
FR
0
0
0
0
0
0
0
0
4
0
0
0
0
0
0
0
0
0
0
0
0
0
1
68
0
0
1
0
0
1
0
0
0
0
0
0
0
37
0
A
0
0
0
0
0
0
0
0
0
0
0
0
0
M
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.85
57.63
0.00
0.00
0.85
0.00
0.00
0.85
0.00
0.00
0.00
0.00
0.00
0.00
0.00
31.36
0.00
RA
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0
0
0
0
0
0
0
0
0
1
3
0
0
1
0
0
1
0
0
0
0
0
0
0
2
0
FR
0
0
0
0
0
0
0
0
0
0
0
0
0
2.7
0.9
4.0
0.5
0.0
0.3
0.2
0.1
0.4
1.0
5.5
–0.2
2.4
1.2
0.6
0.3
2.5
0.1
0.1
–0.6
0.9
0.4
0.1
–0.4
–1.3
0.2
TW
1.2
0.6
0.1
0.5
0.2
1.9
0.2
0.6
3.9
0.9
0.2
0.2
0.1
Table A1. List of ectomycorrhizal-forming fungi taxa in the four experimental stands and information related to their fruiting pattern and taxa weightiness (principal response curve
analysis) during the period 2003–2006.
Azul et al.
2413
Published by NRC Research Press
0
0
0
0
0
0
0
0
4
3
6
29
Broad
Broad
Broad
Broad
Broad
1
1
0
84
32
120
64
33
88
13
4
76
4
10
17
0
7
0
0
0
7
2
1
—
—
—
—
—
Broad
Broad
Host range
Broad
Broad
Broad
Angiosperms
Broad
Broad
Broad
Broad
Broad
Quercus sp.
Broad
Broad
—
—
—
—
Broad
Broad
Broad
Broad
Thermophilic
Broad
Broad
C
A
0.00
0.13
0.10
0.20
0.95
0.00
0.00
0.00
0.00
0.00
0.00
0.00
RA
0.03
0.03
0.00
2.75
1.05
3.93
2.10
1.08
2.88
0.43
0.13
2.49
0.13
0.33
0.56
0.00
0.23
0.00
0.00
0.00
0.23
0.07
0.03
0
1
2
3
4
0
0
0
0
0
0
0
FR
1
1
0
2
3
4
3
3
4
2
2
2
2
2
2
0
2
0
0
0
1
1
1
5
2
0
0
11
2
6
5
4
3
5
8
Cu
A
0
3
16
32
25
24
9
5
4
2
0
38
0
17
0
1
6
1
0
1
10
17
8
0.27
0.11
0.00
0.00
0.59
0.11
0.32
0.27
0.22
0.16
0.27
0.43
RA
0.00
0.16
0.86
1.73
1.35
1.29
0.49
0.27
0.22
0.11
0.00
2.05
0.00
0.92
0.00
0.05
0.32
0.05
0.00
0.05
0.54
0.92
0.43
4
1
0
0
2
2
2
3
3
2
4
4
FR
0
1
1
1
1
1
2
2
2
1
0
2
0
2
0
1
1
1
0
1
3
4
4
0
0
1
0
11
0
0
0
0
0
0
0
Ca
A
0
0
0
0
0
1
0
3
0
0
0
4
0
0
0
0
5
0
0
0
0
0
0
0.00
0.00
0.13
0.00
1.46
0.00
0.00
0.00
0.00
0.00
0.00
0.00
RA
0.00
0.00
0.00
0.00
0.00
0.13
0.00
0.40
0.00
0.00
0.00
0.53
0.00
0.00
0.00
0.00
0.66
0.00
0.00
0.00
0.00
0.00
0.00
0
0
1
0
4
0
0
0
0
0
0
0
FR
0
0
0
0
0
1
0
1
0
0
0
1
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
M
A
1
0
0
0
0
2
0
0
0
0
0
4
0
0
0
0
0
0
1
0
0
1
0
0.00
0.00
0.00
0.00
0.85
0.00
0.00
0.00
0.00
0.00
0.00
0.00
RA
0.85
0.00
0.00
0.00
0.00
1.69
0.00
0.00
0.00
0.00
0.00
3.39
0.00
0.00
0.00
0.00
0.00
0.00
0.85
0.00
0.00
0.85
0.00
0
0
0
0
1
0
0
0
0
0
0
0
FR
1
0
0
0
0
1
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
1
0
0.1
0.2
0.2
0.3
1.1
0.1
0.2
0.2
0.1
0.1
0.1
0.2
TW
0.0
0.1
0.3
2.0
1.4
2.9
1.7
1.0
2.2
0.6
0.2
2.1
0.2
0.8
0.7
0.0
0.5
0.0
0.0
0.0
0.4
0.4
0.2
Note: C, control; Cu, shrub cutting without soil tillage; Ca, shrub density controlled by grazing; M, shrub cutting with soil tillage; A, fruit-body abundance determined as the number of the specimens over
the four fruiting seasons; RA, relative abundance determined as the number of total fruit bodies of a given taxon per total fruit bodies; FR, fruiting regularity determined as the number of seasons of fruitbodies occurrence; TW, taxa weightiness. Taxon names and authors follow the Index Fungorum (http://www.indexfungorum.org, 25 June 2009).
Taxon
Pisolithus arhizus (Scop.) Rauschert.
Rhizopogon luteolus Fr. & Nordholm
Russula amoena Quél.
Russula amoenolens Romagn.
Russula atropurpurea (Krombh.) Britzelm
Russula cyanoxantha (Shaeff.) Fr.
Russula delica Fr.
Russula fellea (Fr.) Fr.
Russula foetens (Pers.) Pers.
Russula fragilis Fr.
Russula ochroleuca (Pers.) Fr.
Russula sororia Fr.
Russula sp. 1
Russula sp. 2
Russula sp. 3
Russula sp. 4
Russula xerampelina (Schaeff.) Fr.
Scleroderma areolatum Ehrenb.
Scleroderma bovista Fr.
Scleroderma citrinum Pers.
Scleroderma polyhizum (J.F. Gmel.) Pers.
Thelephora atra Weinm.
Tomentella brevispina (Bourdot & Galzin)
M.J. Larsen
Tomentella sp. 1
Tomentella sp. 2
Tomentella sp. 3
Tomentella sp. 4
Tomentella sp. 5
Tomentella stuposa (Link) Stalpers
Tomentella sublilacina (Ellis & Holw.)
Wakef
Tomentella subtestacea Bourdot & Galzin
Tricholoma colossus (Fr.) Quél.
Tricholoma sulphureum (Bull.) P. Kumm.
Xerocomus chrysenteron (Bull.) Quél.
Xerocomus subtomentosus (L.) Quél.
Table A1 (concluded).
2414
Can. J. For. Res. Vol. 39, 2009
Published by NRC Research Press
Taxon
Agaricus arvensis Schaeff.
Agaricus augustus Fr.
Agaricus campestris L.
Agaricus praeclaresquamosus A.E. Freeman
Agaricus silvicola (Vittad.) Peck
Agaricus xanthodermus Genev.
Aleuria aurantia (Pers.) Fuckel
Auricularia mesenterica (Dicks.) Pers.
Bisporella citrina (Batsch) Korf & S.E. Carp.
Calvatia cyathiformis (Bosc) Morgan
Chlorophyllum rhacodes (Vittad.) Vellinga
Clitocybe fragans (With.) P. Kumm.
Clitocybe gibba (Pers.) P. Kumm.
Clitocybe phaeophthalma (Pers.) Kuyper
Clitocybe squamulosa (Pers.) Fr.
Collybia fusipes (Bull.) Quél.
Collybia kuehneriana Singer
Conocybe macrospora (G.F. Atk.) Hauskn.
Conocybe pubescens (Gillet) Kühner
Coprinellus domesticus (Bolton) Vilgalys, Hopple & Jacq.
Johnson
Coprinus comatus (O.F. Müll.) Pers.
Coprinus micaceus (Bull.) Fr.
Coprinus picaceus (Bull.) Gray
Coprinus plicatilis (Curtis) Fr.
Crepidotus mollis (Schaeff.) Staude
Crepidotus variabilis (Pers.) P. Kumm.
Cyathus olla (Batsch) Pers.
Cyathus striatus (Huds.) Willd.
Entoloma conferendum (Britzelm.) Noordel.
Flammulina velutipes (Curtis) Singer
Ganoderma applanatum (Pers.) Pat.
Ganoderma lucidum (Curtis) P. Karst.
Gymnopilus penetrans (Fr.) Murrill
Gymnopilus spectabilis (Fr.) Singer
Hygrocybe conica (Scop.) P. Kumm.
Hymenochaete rubiginosa (Dicks.) Lév.
Hypholoma fasciculare (Huds.) P. Kumm.
Infundibulicybe geotropa (Bull.) Harmaja
Inonotus hispidus (Bull.) P. Karst.
RA
0.00
0.00
0.00
0.00
0.15
0.00
0.15
0.00
0.15
0.00
0.15
0.00
0.15
0.00
0.60
0.00
0.00
0.00
0.00
0.00
0.30
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.30
0.00
0.00
0.15
0.15
0.00
0.00
0.00
1.19
19.55
0.15
0
0
0
0
1
0
1
0
1
0
1
0
1
0
4
0
0
0
0
0
2
0
0
0
0
0
0
0
2
0
0
1
1
0
0
0
8
131
1
A
C
1
0
0
0
0
0
0
0
1
0
0
1
1
0
0
0
1
4
1
FR
0
0
0
0
1
0
1
0
1
0
1
0
1
0
1
0
0
0
0
0
0
0
10
28
0
0
0
0
0
0
0
0
3
0
0
22
0
124
0
0
0
0
0
0
0
0
3
0
0
0
0
0
0
1
15
0
0
0
9
A
Cu
0.00
0.00
1.13
3.16
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.34
0.00
0.00
2.49
0.00
14.01
0.00
RA
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.34
0.00
0.00
0.00
0.00
0.00
0.00
0.11
1.69
0.00
0.00
0.00
1.02
0
0
4
3
0
0
0
0
0
0
0
0
2
0
0
1
0
3
0
FR
0
0
0
0
0
0
0
2
0
0
0
0
0
0
1
1
0
0
0
1
0
0
18
54
0
1
0
0
353
23
0
0
0
104
0
2
23
22
0
2
0
0
0
0
0
0
0
0
34
0
14
2
37
0
0
0
69
47
0
A
Ca
0.00
0.00
1.81
5.44
0.00
0.10
0.00
0.00
35.55
2.32
0.00
0.00
0.00
10.47
0.00
0.20
2.32
2.22
0.00
RA
0.20
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
3.42
0.00
1.41
0.20
3.73
0.00
0.00
0.00
6.95
4.73
0.00
0
0
4
3
0
1
0
0
4
1
0
0
0
3
0
1
1
1
0
FR
1
0
0
0
0
0
0
0
0
2
0
1
1
1
0
0
0
4
4
0
14
23
14
29
1
0
139
64
25
0
1
0
1
59
2
0
0
13
0
0
2
9
1
3
3
0
12
0
6
11
0
1
0
3
12
18
0
0
0
A
M
1.21
1.99
1.21
2.51
0.09
0.00
12.02
5.54
2.16
0.00
0.09
0.00
0.09
5.10
0.17
0.00
0.00
1.12
0.00
RA
0.00
0.17
0.78
0.09
0.26
0.26
0.00
1.04
0.00
0.52
0.95
0.00
0.09
0.00
0.26
1.04
1.56
0.00
0.00
0.00
3
2
3
2
1
0
2
2
3
0
1
0
1
3
1
0
0
1
0
FR
0
1
1
1
1
2
0
1
0
1
2
0
1
0
2
1
1
0
0
0
–0.2
–0.4
–0.9
–0.9
–0.1
–0.1
–0.5
–0.4
–3.3
–0.3
–0.1
0.1
0.1
–1.3
–0.1
–0.1
0.1
2.1
0.1
TW
–0.1
–0.1
–0.2
0.0
0.0
–0.1
0.1
–0.3
0.1
–0.8
–0.2
–0.4
0.0
–0.5
0.1
0.0
–0.2
–1.4
–1.1
0.1
Table A2. List of saprobe taxa in the four experimental stands and information related to their fruiting pattern and taxa weightiness (principal response curve analysis) during the
period 2003–2006.
Azul et al.
2415
Published by NRC Research Press
Taxon
Lentinellus cochleatus (Pers.) P. Karst.
Lepiota clypeolaria (Bull.) P. Kumm.
Lepiota josserandii Bon & Boiffard
Lepista glaucocana (Bres.) Singer
Lepista nuda (Bull.) Cooke
Lepista sordida (Schumach.) Singer
Lepista sordida var. lilacea (Quél.) Bom
Lycoperdon echinatum Pers.
Lycoperdon molle Pers.
Lycoperdon perlatum Pers.
Lycoperdon pratense Pers.
Lycoperdon pyriforme Schaeff.
Lycoperdon umbrinum Pers.
Macrolepiota procera (Scop.) Singer
Marasmius androsaceus (L.) Fr.
Marasmius oreades (Bolton) Fr.
Marasmius quercophilus Pouzar
Megacollybia platyphylla (Pers.) Kotl. & Pouzar
Melanoleuca brevipes (Bull.) Pat.
Melanoleuca melaleuca (Pers.) Murrill
Meripilus giganteus (Pers.) P. Karst.
Micromphale foetidum (Sowerby) Singer
Mycena inclinata (Fr.) Quél.
Mycena pura (Pers.) P. Kumm.
Mycena pura var. rosea (Schumach.) J.E. Lange
Neottiella rutilans (Fr.) Dennis
Omphalina sp.
Omphalotus olearius (DC.) Singer
Otidea alutaceae (Pers.) Massee
Panaeolus antillarum (Fr.) Dennis
Panaeolus semiovatus (Sowerby) S. Lundell & Nannf.
Panaeolus sphinctrinus (Fr.) Quél.
Peniophora quercina (Pers.) Cooke
Phanerochaete sanguı́nea (Fr.) Pouzar
Pleurotus ostreatus (Jacq.) P. Kumm.
Pluteus cervinus (Schaeff.) P. Kumm.
Polyporus arcularius (Batsch) Fr.
Psathyrella candolleana (Fr.) Maire
Psathyrella velutina (Pers.) Singer
Pseudohydnum gelatinosum (Scop.) P. Karst.
Rhodocollybia butyracea (Bull.) Lennox
Table A2 (continued).
0
5
1
1
0
0
0
2
0
45
0
3
31
8
0
0
168
1
0
29
0
0
0
0
0
0
27
72
0
0
0
0
0
0
0
0
0
0
0
1
0
C
A
RA
0.00
0.75
0.15
0.15
0.00
0.00
0.00
0.30
0.00
6.72
0.00
0.45
4.63
1.19
0.00
0.00
25.07
0.15
0.00
4.33
0.00
0.00
0.00
0.00
0.00
0.00
4.03
10.75
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.15
0.00
FR
0
2
1
1
0
0
0
1
0
4
0
1
2
2
0
0
4
1
0
3
0
0
0
0
0
0
3
4
0
0
0
0
0
0
0
0
0
0
0
1
0
Cu
A
0
0
0
0
0
4
0
0
0
43
0
0
0
2
0
0
45
0
0
0
0
0
24
0
0
0
0
68
16
0
0
0
1
0
0
0
3
0
0
0
0
RA
0.00
0.00
0.00
0.00
0.00
0.45
0.00
0.00
0.00
4.86
0.00
0.00
0.00
0.23
0.00
0.00
5.08
0.00
0.00
0.00
0.00
0.00
2.71
0.00
0.00
0.00
0.00
7.68
1.81
0.00
0.00
0.00
0.11
0.00
0.00
0.00
0.34
0.00
0.00
0.00
0.00
FR
0
0
0
0
0
1
0
0
0
2
0
0
0
2
0
0
3
0
0
0
0
0
1
0
0
0
0
1
1
0
0
0
1
0
0
0
2
0
0
0
0
Ca
A
0
1
0
0
7
0
0
0
50
23
0
0
0
32
0
28
0
0
1
0
1
0
0
4
1
0
0
0
0
0
0
0
0
0
0
0
0
9
0
0
0
RA
0.00
0.10
0.00
0.00
0.70
0.00
0.00
0.00
5.04
2.32
0.00
0.00
0.00
3.22
0.00
2.82
0.00
0.00
0.10
0.00
0.10
0.00
0.00
0.40
0.10
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.91
0.00
0.00
0.00
FR
0
1
0
0
3
0
0
0
2
3
0
0
0
2
0
1
0
0
1
0
1
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
2
0
6
1
0
28
1
0
0
8
17
0
142
0
0
0
0
28
0
0
0
89
55
0
0
25
77
8
0
1
6
3
0
21
21
0
1
M
A
RA
0.09
0.00
0.00
0.00
0.17
0.00
0.52
0.09
0.00
2.42
0.09
0.00
0.00
0.69
1.47
0.00
12.28
0.00
0.00
0.00
0.00
2.42
0.00
0.00
0.00
7.70
4.76
0.00
0.00
2.16
6.66
0.69
0.00
0.09
0.52
0.26
0.00
1.82
1.82
0.00
0.09
FR
1
0
0
0
1
0
2
1
0
3
1
0
0
3
1
0
3
0
0
0
0
1
0
0
0
1
1
0
0
2
2
2
0
1
1
1
0
2
1
0
1
TW
–0.1
0.2
0.1
0.1
–0.4
0.1
–0.2
0.0
–0.7
1.0
0.0
0.1
0.8
–0.4
–0.2
–0.3
1.6
0.1
–0.1
1.0
–0.1
–0.2
0.2
–0.1
–0.1
–0.3
0.3
1.0
0.2
–0.4
–0.7
–0.2
0.0
–0.1
–0.1
–0.1
0.0
–0.5
–0.2
0.1
–0.1
2416
Can. J. For. Res. Vol. 39, 2009
Published by NRC Research Press
C
A
91
1
0
0
9
3
9
0
6
0
1
1
0
0
0
0
RA
13.58
0.15
0.00
0.00
1.34
0.45
1.34
0.00
0.90
0.00
0.15
0.15
0.00
0.00
0.00
0.00
FR
4
1
0
0
2
2
4
0
2
0
1
1
0
0
0
0
Cu
A
315
0
0
28
11
0
7
0
11
10
6
1
0
0
0
75
RA
35.59
0.00
0.00
3.16
1.24
0.00
0.79
0.00
1.24
1.13
0.68
0.11
0.00
0.00
0.00
8.47
FR
4
0
0
1
2
0
3
0
3
4
3
1
0
0
0
4
Ca
A
0
1
0
0
0
0
0
0
18
2
0
0
10
0
0
0
RA
0.00
0.10
0.00
0.00
0.00
0.00
0.00
0.00
1.81
0.20
0.00
0.00
1.01
0.00
0.00
0.00
FR
0
1
0
0
0
0
0
0
2
1
0
0
1
0
0
0
0
6
6
0
4
0
5
1
8
0
0
6
25
1
1
86
M
A
RA
0.00
0.52
0.52
0.00
0.35
0.00
0.43
0.09
0.69
0.00
0.00
0.52
2.16
0.09
0.09
7.44
FR
0
1
1
0
1
0
2
1
2
0
0
3
1
1
1
2
TW
3.3
–0.1
–0.1
0.2
0.6
0.2
0.5
–0.1
–0.2
0.1
0.1
–0.1
–0.7
–0.1
0.0
–0.1
Note: C, control; Cu, shrub cutting without soil tillage; Ca, shrub density controlled by grazing; M, shrub cutting with soil tillage; A, fruit-body abundance determined as the number of the specimens over
the four fruiting seasons; RA, relative abundance determined as the number of total fruit bodies of a given taxon per total fruit bodies; FR, fruiting regularity determined as the number of seasons of fruitbodies occurrence; TW, taxa weightiness. Taxon names and authors follow the Index Fungorum (http://www.indexfungorum.org, 25 June 2009).
Taxon
Rickenella fibula (Bull.) Raithelh.
Schizophyllum commune Fr.
Sericeomyces serenus (Fr.) Heinem.
Sphaerobolus stelllatus Tode
Stereum hirsutum (Willd.) Pers.
Stereum reflexum D.A. Reid
Terana caerulea (Lam.) Kuntze
Trametes hirsuta (Wulfen) Lloyd
Trametes versicolor (L.) Lloyd
Tremella encephala Pers.
Tremella foliacea Pers.
Tremella mesenterica Retz.
Trichaptum biforme (Fr.) Ryvarden
Volvariella gloiocephala (DC.) Boekhout & Enderle
Xylaria filiformis (Alb. & Schwein.) Fr.
Xylaria hypoxylon (L.) Grev.
Table A2 (concluded).
Azul et al.
2417
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