American Journal of Botany 97(5): 893898. 2010.

BRIEF COMMUNICATION

BOLETE DIVERSITY IN TWO RELICT FORESTS OF THE MEXICAN

BEECH (FAGUS GRANDIFOLIA VAR. MEXICANA; FAGACEAE)1
Ernesto Ch. Rodrguez-Ramrez and Claudia E. Moreno2
Centro de Investigaciones Biolgicas, Universidad Autnoma del Estado de Hidalgo, Apartado Postal 69 Plaza Jurez 42001
Pachuca, Hidalgo, Mexico
The current distribution of the endangered Mexican beech [Fagus grandifolia var. mexicana (Martinez) Little] is restricted to
relict isolated populations in small remnants of montane cloud forest in northeastern Mexico, and little is known about its associated biota. We sampled bolete diversity in two of these monospecific forests in the state of Hidalgo, Mexico. We compared alpha
diversity, including species richness and ensemble structure, and analyzed beta diversity (dissimilarity in species composition)
between forests. We found 26 bolete species, five of which are probably new. Species diversity and evenness were similar between
forests. Beta diversity was low, and the similarities of bolete samples from within and between forests were not significantly different. These results support the idea that the two forests share a single bolete ensemble with a common history. In contrast,
cumulative species richness differed between the forests, implying that factors other than the mere presence of the host species
have contributed to shaping the biodiversity of ectomycorrhizal fungi in relict Mexican beech forests.
Key words: beta diversity; Boletaceae; community ecology; conservation; Fagaceae; Fagus grandifolia var. mexicana; Hidalgo; Mexico; montane cloud forest; species richness.

We studied the species diversity of Boletales in Mexican

beech forests, a rare and endangered habitat. At the southernmost limit of the distribution of the genus Fagus (Fagaceae),
the Mexican beech F. grandifolia var. mexicana (Martinez)
Little is restricted to the montane cloud forests of northeastern
Mexico (Williams-Linera et al., 2003; Fang and Lechowicz,
2006; Fig. 1), and little is known about its associated biota.
Monodominant isolated populations of the Mexican beech have
been found in small remnants (240 ha) at fewer than 10 isolated localities of the eastern Sierra Madre, at altitudes ranging
from 1400 to 2000 m a.s.l. (Williams-Linera et al., 2000, 2003).
Community characteristics of the Mexican beech forests are
similar to those of Chinese beech forests (Fang and Lechowicz,
2006), usually with a mix of species of Quercus, Magnolia,
Acer, and Podocarpus (Rzedowski, 1993; Williams-Linera
et al., 2000). These rare Mexican beech forests are relicts of a
formerly extensive cloud forest of Fagus grandifolia from the
Pliocene (Williams-Linera et al., 2003). At present, the Mexican
beech has a smaller climatic range and occurs in areas with a
considerably lower mean annual temperature (14.815.6C)

and higher mean annual precipitation (1741 mm) than F. grandifolia does (19.5C, 1426 mm) at its southern distribution limit
(Fang and Lechowicz, 2006). The species probably grows at its
ecological limits and requires microhabitats with very high
humidity (Williams-Linera et al., 2000). Given the restricted
spatial distribution and unusual stand characteristics (WilliamsLinera et al., 2000) of this endemic beech, its monospecific
forests may not survive without conservation efforts (WilliamsLinera et al., 2003, Tllez-Valds et al., 2006).
In this paper, we focus on the species diversity and composition of the bolete (Basidiomycetes: Boletales) ensemble growing in two monodominant Mexican beech forests in the state of
Hidalgo, central Mexico. Given that most boletes are obligate
ectomycorrhizal symbionts, their biogeographical distribution
depends on that of their host plants (Ortz-Santana et al., 2007;
Halling et al., 2008; Smith and Pfister, 2009). As symbionts in
forest ecosystems, boletes are intimately involved in basic processes such as nutrient uptake and cycling, and the decomposition of organic matter. In temperate forests, boletes are typically
a conspicuous element of the mycobiota during the rainy season. Some of them are also of human interest because of their
toxic or psychotropic compounds (e.g., Boletus manicus in
Papua New Guinea; Thomas, 2003). The fruit bodies of several
Mexican boletes are edible and much appreciated by the locals
for their culinary qualities (Estrada-Martnez et al., 2009).
Mexico has a very high diversity of boletes, comprised of 212
taxa belonging to 20 of the 25 genera of the world (GarcaJimnez and Garza-Ocaas, 2001).
To obtain an overview of the bolete diversity in relict monospecific forests of Mexican beech, we compared alpha diversity, including the species richness and structure of bolete
ensembles in two Mexican beech forests, and analyzed beta
diversity (dissimilarity in species composition) between forests.

1 Manuscript received 18 September 2009; revision accepted 19 February

2010.

The authors thank U. A. Rodrguez R., R. Escorcia, and B. Montiel for

technical support in field sampling, A. Moreno (Laboratorio de Micologa,
CIB-UAEH) and J. Garca-Jimnez (Laboratorio de Micologa, UAT) for
their review and suggestions, and B. Delfosse for improving the English.
The first author is especially grateful to B. Muoz-Vazquez and to
CONACYT, which provided a grant to pursue his M. Sc. degree. This
research was supported in part by projects 95828 FOMIX CONACYT
HIDALGO and 84127 SEP-CONACYT Basic Science.
2 Author for correspondence (e-mail: cmoreno@uaeh.edu.mx)
doi:10.3732/ajb.0900284

American Journal of Botany 97(5): 893898, 2010; http://www.amjbot.org/ 2010 Botanical Society of America

893

894

American Journal of Botany

[Vol. 97

Fig. 1. Location of the two Mexican beech forests sampled in the state of Hidalgo, Mexico. Distributions of Fagus grandifolia and F. grandifolia var.
mexicana were drawn from biodiversity occurrence data obtained from 42 databases accessed through GBIF Data Portal (http://www.gbif.net, 200911-14). The current distribution of the cloud forest in Hidalgo was drawn from Velzquez et al. (2002).

In isolation, the two beech forests may have independently accumulated different bolete species, leading to differences in
alpha diversity and high beta diversity between forests. Alternatively, the bolete communities may have uniform alpha
diversity and low beta diversity, reflecting the shared environmental conditions or common historical origins of the relict
beech forests. Understanding the patterns of diversity among
ectomycorrhizal fungi will permit us to make conservation recommendations that take into account not only the trees, but also
the microbial environment upon which the trees depend.
MATERIALS AND METHODS
Study areasThe study was carried out in two well-conserved, isolated
forests where Fagus grandifolia var. mexicana is monodominant in the state of
Hidalgo, Mexico (Fig. 1). One forest is La Mojonera, in the Zacualtipan municipality, located ca. 203740N and 983715W, at 1958 to 1991 m a.s.l.
The other forest is Medio Monte in the municipality of San Bartolo Tutotepec,
located ca. 202450N and 981424W, at 1800 to 1944 m a.s.l. In both forests, the soil type is Andisol, suborder Vitrands (nomenclature follows the U.S.
Soil Taxonomy of the United States Department of Agriculture) with the clear
presence of organic matter. The linear distance between forests is ca. 50 km,
and both are surrounded by a matrix of montane cloud forest, with some patches
of cattle pastures. We did not find any other potential ectomycorrhizal hosts,
either within or surrounding the permanent sampling plots of either forest.
To characterize any environmental differences between the two forests, we
assessed five variables at 20 randomly selected sampling sites in the permanent
plots (see below) where boletes were sampled: arboreal cover, distance to the
nearest tree, diameter at breast height (dbh) of the nearest tree, slope, and litter
depth. At each sampling site, these variables were measured four times, once in
the direction of each cardinal point, and the mean value was calculated at each
point for each variable. The two forests have statistically significant differences

in mean slope (t = 3.88, df =38, P 0.001), median arboreal cover (U = 285,

N = 20, P = 0.02) and the dbh of the nearest tree (U = 125, N = 20, P = 0.04).
Slope is steeper and there is more cover in La Mojonera than in Medio Monte,
and dbh is greater in Medio Monte than in La Mojonera. Median litter depth (U =
207.5, N = 20, P = 0.850) and mean distance to the nearest tree (t = 0.242,
df = 38, P = 0.810) are not statistically different between the two forests.
Field samplingBolete fruit bodies were collected once every 15 d over
5 mo in the rainy season of 2007 (from July to November), for a total of 22
samples, 11 in each forest. No fruit bodies were found during four of those 11
sampling forays (July and late November in La Mojonera; July, late October,
and early November in Medio Monte), resulting in seven successful samplings
at each forest.
We followed two sampling procedures: sampling in permanent plots and
opportunistic sampling (Mueller et al., 2004). Permanent plots of 100 100 m2
were set up in representative areas of each forest, as far as possible from human
settlements and roads. In each plot, we set 10 transects, 100 m in length and
10 m apart. We marked 20 sampling sites in each transect, each separated by
5 m, for a total 200 sites in the plot. At each site, all bolete fruit bodies were
collected in a circular, 5-m2 subplot around the point, for a total sampling area
of 0.1 ha in each forest, resampled 11 times. During each sampling, opportunistic sampling was conducted by two people who directly searched for fruit bodies for 2 h outside the permanent plot.
Taxonomic identificationAll the fruit bodies encountered in the field
were photographed and put into waxed paper bags for transport to the laboratory. Taxonomic identification was based on macroscopic morphological
descriptions and color changes with chemical reagents (KOH 310%, FeSO4
10%, and NH4OH 370%). Also, microscopic samples of dehydrated material
were examined to characterize the size (length and width) and shape of microscopic structures such as basidiospores, basidia, and cystidia. All this information was used to identify specimens with the taxonomic keys available and
expert opinion. Dehydrated specimens were deposited in the Mycological Collection of the Universidad Autnoma del Estado de Hidalgo (M-UAEH), and
voucher information is provided in Appendix 1. A taxonomic description of

May 2010]

Rodrguez-Ramrez and MorenoBoletes in Mexican beech forests

each species and a dichotomous taxonomic key is available in RodrguezRamrez (2009).

Data analysisTo include only standardized samples for the alpha diversity analyses, we used only data collected in the permanent plots, but for the
beta diversity analysis, we used data collected with both procedures (permanent
plots and opportunistic sampling).
Before analyzing alpha diversity, we assessed the completeness of the
bolete inventories in each forest as the proportion of observed species richness
relative to maximum expected richness. Expected richness was calculated using
two nonparametric richness estimators, ICE and ACE, which are based on incidence and abundance data, respectively (Colwell, 2006). These estimators were
calculated with the program EstimateS version 8.0.0 (Colwell, 2006). Given
that total number of fruit bodies collected in each forest was markedly different,
we compared cumulative species richness using rarefaction to standardize samples. Rarefaction curves based on the number of fruit bodies collected, with
standard errors, were calculated with the software Species Diversity and Richness version 3.0.2 (Henderson and Seaby, 2002). Species abundance structure
was plotted in rankabundance graphs. The Shannon diversity and Pielou evenness indexes were calculated with 95% confidence intervals obtained by bootstrap resampling using the Species Diversity and Richness software (Henderson
and Seaby, 2002).
To assess beta diversity between the two sampled forests, we drew Venn
diagrams with the number of species and genera in three groups: those present
only in La Mojonera, those present only in Medio Monte, and those shared by
both forests. As a measure of beta diversity, we calculated the complementarity
of the two forests, using the index described by Colwell and Coddington (1994),
at the genus and species levels. Then, to test statistical differences in similarity
between the two forests, we performed a nonparametric one-way analysis of
similarity (ANOSIM; Clarke and Warwick, 1994). The null hypothesis of the
ANOSIM was that there are no statistical differences in species composition
between the two forests, i.e., mean similarity between pairs of samples within a
forest is not different from the similarity between pairs of samples from different forests. Then, to search for temporal or spatial groups of samples according
to their similarity in species composition, we constructed single linkage cluster
dendrograms. To see the influence of using presence/absence or fruit body
abundance data, we calculated both the ANOSIM and cluster analysis using
two similarity measures: qualitative and quantitative Srensen coefficients.
These two analyses were performed using the PRIMER ver. 5.0 program
(Clarke and Gorley, 2001).

RESULTS
We found 484 fruit bodies from 26 bolete species in the
Mexican beech forests sampled (Table 1), five of which are
probably new species, and thus new records for Mexico (to be
described elsewhere). Within the permanent plots, we found
333 fruit bodies from 20 bolete species in La Mojonera forest
and 144 fruit bodies from 14 species in Medio Monte. With opportunistic sampling, we found four additional species represented by seven fruit bodies, along with many species that we
had also found in the permanent plots (Table 1). For the permanent plots of both forests, the ICE richness estimator predicted
a higher maximum number of species (26 species for La
Mojonera and 16.26 species for Medio Monte) than the ACE
estimator (21 and 14.64 species for La Mojonera and Medio
Monte, respectively). Thus, according to the incidence-based
estimator, the species inventory within the permanent plot at
La Mojonera is 77% complete, and the inventory of Medio
Monte is 86% complete; while for the abundance-based estimators both inventories are >95% complete.
Even after we standardized the sampling effort to a total of
144 fruit bodies per forest, rarefaction curves showed a significantly higher cumulative richness in the permanent plot at
La Mojonera (20 species) than at Medio Monte (14 species,
Fig. 2). Ecological diversity and evenness at La Mojonera
are also higher (H = 2.328, J = 0.753) than at Medio Monte

895

Table 1.

Boletaceae species collected in two Mexican beech forests in the

state of Hidalgo, Mexico. Key codes indicate fruit body abundance,
shown in Fig. 3.

Species
Boletellus russellii (Frost) E. J. Gilbert (1931)
Boletus hypocarycinus Singer (1945)
Boletus miniato-olivaceus Frost (1874)
Boletus rubropunctus Peck (1904)
Boletus sp. 1
Leccinum albellum (Peck) Singer (1945)
Leccinum eximium (Peck) Singer (1973)
Leccinum rugosiceps (Peck) Singer (1905)
Leccinum sp. 1
Leccinum tablense Halling & G. M. Mueller (2003)
Phlebopus sp. 1
Phylloporus leucomycellinus Singer & M. H. Ivory (1978)
Phylloporus sp. 1
Pulveroboletus cramesinus (Secr. ex Watling) M. M. Moser ex Singer
(1966)
Retiboletus retipes (Berk. & M. A. Curtis) Manfr. Binder & Bresinsky
(2002)
Strobilomyces confusus Singer (1945)
Tylopilus felleus (Bull. ex Fr.) Karsten (1818)
Tylopilus rubrobrunneus Mazzer & A. H. Smith (1976)
Tylopilus tabacinus (Peck) Singer (1896)
Tylopilus vinosobrunneus Hongo (1979)
Xanthoconium separans (Peck) Halling & Both (1998)
Xerocomus sp. 1
Pulveroboletus ravenelii (Berk. & M. A. Curtis) Murrill (1909)a
Boletellus betula (Schwein.) E. J. Gilbert (1931)a
Boletus pallidus Frost (1874)a
Boletus roseolateritius Bessette, Both & Dunaway (2003)a

Key
O
R
S
A
Q
T
D
P
N
H
L
V
K
M
I
U
G
B
E
J
F
C

a Species collected only during opportunistic sampling outside permanent

sampling plots (see Materials and Methods).

(H = 2.269, J =0.734), but not significantly so, given that their

95% confidence intervals overlap. Thus, the rankabundance
graphs are similar for the permanent plots of both forests
(Fig. 3), where the most abundant species is Boletus rubropunctus, which accounted for 35.79% of the total fruit bodies in
La Mojonera and 24.64% in Medio Monte. Tylopilus rubrobrunneus was also very abundant at both sites, while T. tabacinus was abundant at La Mojonera but rare at Medio Monte. The

Fig. 2. Rarefaction curves for boletes in the two Mexican beech

forests studied, for the species collected in permanent plots. The bars are
standard errors.

896

[Vol. 97

American Journal of Botany

DISCUSSION

Fig. 3. Rankabundance plots of bolete ensembles collected in permanent plots in the two Mexican beech forests studied. Species codes are
given in Table 1. Relative species abundance (ni/N) was plotted on a logarithmic scale against the species-rank ordered by species from those with
the most fruit bodies to those with the fewest.

rarest species at both sites was Strobilomyces confusus, with

only one fruit body in each forest.
For beta diversity between forests, the complementarity
index is only 9% at the genus level (Fig. 4), given that 10 genera
were shared and only one genus was exclusive to La Mojonera
(Xerocomus). At the species level, the complementarity value
reaches 42.30% (Fig. 4) because 15 species were shared between the two forests, nine of which (Boletus hypocarycinus,
Boletus sp. 1., B. betula, B. pallidus, B. pallidoroseus, Leccinum tablense, Leccinum sp. 1., Tylopilus vinosobrunneus, and
Xerocomus sp. 1) were found exclusively at La Mojonera and
two (L. eximium and Phylloporus leucomycellinus) at Medio
Monte only.
Bolete samples from within the same forest were not significantly more similar than samples from between forests based
on either the abundance data (ANOSIM: R = 0.15; P = 0.052)
or the incidence data (R = 0.15; P = 0.051). Neither the cluster
analysis from the indexes of similarity nor the abundance of
boletes revealed clear temporal or spatial groupings of
samples.

Fig. 4. Venn diagrams with a schematic representation of bolete beta

diversity components: the total number of taxa (genera and species) found
in only one of the two forests (exclusive) and the number of species shared
by both Mexican beech forests. The percentage of complementarity in
species composition between forests was calculated using the index described by Colwell and Coddington (1994).

At present, Mexican beech is restricted to isolated populations in the Sierra Madre Oriental mountain range, probably
because of historical events such as the retreat and expansion of
its distribution during glacial and interglacial periods in the
Pliocene and Pleistocene (Williams-Linera et al., 2003). These
events may have shaped the biodiversity associated with these
relicts of Mexican beech forests, including that of the ectomycorrhizal fungi. Our results support the idea that independent of
the isolation of forests, there is a single bolete ensemble with a
common history in the two forests studied.
The community structure of the boletes is similar in the two
forests in terms of diversity and evenness, with Boletus rubropunctus and Tylopilus rubrobrunneus the most abundant species. Beta diversity was low, and ANOSIM detected no
significant difference in sample similarity within and between
forests. This result can be considered robust given that the completeness of our bolete inventories is high, whereas undersampling would result in lower observed similarity values compared
with the true similarity values from complete species inventories (Chao et al., 2005). However, time intervals between sampling events, as well as environmental and phenological
conditions may influence fruit body detectability in samples
(Unterseher et al., 2005; Osono and Takeda, 2006).
Baselga et al. (2007; Baselga, 2010) explained how beta
diversity may be caused by two different phenomena: true species turnover and nestedness. Nestedness occurs when the biota
of sites with smaller numbers of species are subsets of the biota
at richer sites, reflecting a nonrandom process of species loss.
In contrast, spatial turnover implies the replacement of some
species by others as a consequence of environmental sorting or
spatial and historical constraints (Baselga, 2010 and references
therein). In this study, though low, the beta diversity of boletes
that we found resulted from the rate of species turnover, because some species were replaced by different species in both
forests, so the forests species compositions are not subsets of
each other. La Mojonera forest clearly harbors more bolete species richness than Medio Monte does. This richness may be
related to the current environmental conditions at La Mojonera.
Bolete diversity might be responding to the steeper slope and
greater degree of arboreal cover than recorded for Medio Monte.
However, more research on the particular responses of ectomycorrhizal fungi to forest structure and microclimate are needed
to understand the symbiosis. For example, ectomycorrhizal
species richness may be positively related to forest size
(Newton and Haigh, 1998; Peay et al., 2007) and soil type
(Gehring et al., 1998). In La Mojonera, the forest is considered
one of the most important populations of Mexican beech in
terms of its conservation status because it is structurally well
developed and regenerating, as indicated by its seedling and
sapling densities (Williams-Linera et al., 2003). This Fagus
population at La Mojonera is probably the largest and most genetically heterogeneous population in Mexico (Prez, 1999).
Plant and landscape ecology studies are needed to characterize
the current status of the relict Mexican beech forests. Also, an
assessment of the threats to its conservation is needed, given
that at present there are no laws or programs to protect Fagus
and the species associated with it.
Although a significant proportion of ectomycorrhizal fungi
might exhibit host specificity (Newton and Haigh, 1998; Ishida
et al., 2007), fortunately from a conservation perspective, several of the bolete species that we report in this study have other

May 2010]

Rodrguez-Ramrez and MorenoBoletes in Mexican beech forests

hosts in addition to the Mexican beech. Boletus rubropunctus

the most abundant specieshas been thoroughly studied in
several Quercus hosts (Smith and Pfister, 2009). Boletellus
betula, B. miniato-olivaceus, B. russellii, Strobilomyces confusus, Tylopilus eximium, T. felleus, Leccinum rugosiceps, Retiboletus retipes, and Pulveroboletus ravenelii have been found
in temperate subhumid forests of Hidalgo, where Pinus, Quercus,
and Alnus are the dominant tree genera (Rodrguez-Ramrez,
2007).
The 26 species reported in this paper, and the other five species that have been reported for this vegetation type (Leccinum
talamancae, L. chromapes, L. griseum, Boletus stramineum
and B. zelleri; Rodrguez-Ramrez, 2007), give us a current total of 31 bolete species associated with Mexican beech forests
in the state of Hidalgo. Considering the taxonomic and field
limitations that constrain mycologists, the results we present
are an important contribution to the knowledge of fungi occurring with this particular host.
LITERATURE CITED
Baselga, A. 2010. Partitioning the turnover and nestedness components
of beta diversity. Global Ecology and Biogeography 19: 134143.
Baselga, A., A. Jimnez-Valverde, and G. Niccolini. 2007. A multiple-site similarity measure independent of richness. Biology Letters
3: 642645.
Chao, A., R. L. Chazdon, R. K. Colwell, and T.-J. Shen. 2005. A
new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters 8: 148159.
Clarke, K. R., and R. N. Gorley. 2001. PRIMER v5: User manual/
tutorial. Plymouth Marine Laboratory, Plymouth, UK.
Clarke, K. R., and M. Warwick. 1994. Change in marine communities: An approach to statistical analysis and interpretation. Plymouth
Marine Laboratory, Plymouth, UK.
Colwell, R. K. 2006. EstimateS: Statistical estimation of species richness and shared species from samples, version 8.0. Website http://
viceroy.eeb.uconn.edu/estimates. University of Connecticut, Storrs,
Connecticut, USA.
Colwell, R. K., and J. A. Coddington. 1994. Estimating terrestrial
biodiversity through extrapolation. Philosophical Transactions of
the Royal Society of London. Series B, Biological Sciences 345: 101
118 .
Estrada-Martnez, E., G. Guzmn, D. Cibrin, and R. Ortega. 2009.
Contribucin al conocimiento etnomicolgico de los hongos comestibles silvestres de mercados regionales y comunidades de la Sierra
Nevada (Mxico). Interciencia 34: 2533.
Fang, J., and M. J. Lechowicz. 2006. Climatic limits for the present
distribution of beech (Fagus L.) species in the world. Journal of
Biogeography 33: 18041819.
Garca-Jimnez, J., and F. Garza-Ocaas. 2001. Conocimiento de
los hongos de la familia Boletaceae de Mxico. Ciencia UANL
4: 336343.
Gehring, C. A., T. C. Theimer, T. G. Whitham, and P. Keim. 1998.
Ectomycorrhizal fungal community structure of pinyon pines growing
in two environmental extremes. Ecology 79: 15621572.
Halling, R. E., T. W. Osmundson, and M.-A. Neves. 2008. Pacific
boletes: Implications for biogeographic relationships. Mycological
Research 112: 437447.

897

Henderson, P. A., and R. M. H. Seaby. 2002. Species diversity and richness III, version 3.0.2. Pisces Conservation, Lymington, Hampshire,
UK.
Ishida, T. A., K. Nara, and T. Hogetsu. 2007. Host effects on ectomycorrhizal fungal communities: Insight from eight host species in
mixed coniferbroadleaf forests. New Phytologist 174: 430440.
Mueller, G. M., J. P. Schmit, S. M. Huhndorf, L. Ryvarden, T. E.
ODell, D. J. Lodge, P. R. Leacock, et al. 2004. Recommended
protocols for sampling macrofungi. In G. M. Mueller, G. F. Bills, and
M. S. Foster [eds.], Biodiversity of fungi: Inventory and monitoring
methods, 168171. Elsevier Academic Press, San Diego, California,
USA.
Newton, A. C., and J. M. Haigh. 1998. Diversity of ectomycorrhizal
fungi in Britain: A test of the speciesarea relation, and the role of
host specificity. New Phytologist 138: 619627.
Ortiz-Santana, B., D. J. Lodge, T. J. Baroni, and E. E. Both. 2007.
Boletes from Belize and the Dominican Republic. Fungal Diversity
27: 247416.
Osono, T., and H. Takeda. 2006. Fungal decomposition of Abies needle
and Betula leaf litter. Mycologia 98: 172179.
Peay, K. G., T. D. Bruns, P. G. Kennedy, S. E. Bergemann, and M.
Garbelotto. 2007. A strong speciesarea relationship for eukaryotic soil microbes: Island size matters for ectomycorrhizal fungi.
Ecology Letters 10: 470480.
Prez, P. M. 1999. Las hayas de Mxico: Monografa de Fagus grandifolia spp. mexicana. Universidad Autnoma Chapingo, Chapingo,
Mxico.
Rodrguez-Ramrez, E. Ch. 2007. Taxonoma de la familia Boletaceae,
en los bosques templados de Zacualtipn, Hidalgo, Mxico. B.Sc. thesis, Universidad Autnoma del Estado de Hidalgo, Hidalgo, Mexico.
Rodrguez-Ramrez, E. Ch. 2009. Diversidad de la familia Boletaceae
en dos bosques de Fagus grandifolia var. mexicana en el estado de
Hidalgo, Mxico. M.Sc. thesis, Universidad Autnoma del Estado
de Hidalgo, Hidalgo, Mexico.
Rzedowski, J. 1993. Diversity and origins of the phanerogamic flora
of Mexico. In T. P. Ramamoorthy, R. Bye, A. Lot, and J. Fa [eds.],
Biological diversity of Mexico: Origins and distribution, 129144.
Oxford University Press, New York, New York, USA.
Smith, M. E., and D. H. Pfister. 2009. Tuberculate ectomycorrhizae
of angiosperms: The interaction between Boletus rubropunctus
(Boletaceae) and Quercus species (Fagaceae) in the United States and
Mexico. American Journal of Botany 96: 16651675.
Tllez-Valds, O., P. Dvila-Aranda, and R. Lira-Saade. 2006.
The effects of climate change on the long-term conservation of Fagus
grandifolia var. mexicana, an important species of the cloud forest in
eastern Mexico. Biodiversity and Conservation 15: 10951107.
Thomas, B. 2003. Boletus manicus Heim. Journal of Psychoactive Drugs
35: 393394.
Unterseher, M., P. Otto, and W. Morawetz. 2005. Species richness
and substrate specificity of lignicolous fungi in the canopy of a template, mixed deciduous forest. Mycological Progress 4: 117132.
Velzquez, A. J., F. Mas, and J. L. Palacio. 2002. Anlisis del cambio
de uso del suelo. Instituto de Geografa, UNAM, Instituto Nacional de
Ecologa, SEMARNAT, Mxico, D.F., Mexico.
Williams-Linera, G., M. Duvell, and C. Alvarez-Aquino. 2000. A
relict population of Fagus grandifolia var. mexicana at the Acatlan
Volcano, Mexico: Structure, phenology, litterfall and dendroecology.
Journal of Biogeography 27: 12971309.
Williams-Linera, G., A. Rowden, and A. C. Newton. 2003.
Distribution and stand characteristics of relict populations of Mexican
beech (Fagus grandifolia var. mexicana). Biological Conservation
109: 2736.

898

American Journal of Botany

Appendix 1. Voucher information of Boletaceae species collected at two Fagus grandifolia var. mexicana forest in the state of Hidalgo, Mexico. All dehydrated
specimens are deposited in the Mycological Collection of the Universidad Autnoma del Estado de Hidalgo, Mexico.
Taxon; Voucher specimen; Collection locale.
Boletellus russellii (Frost) E. J. Gilbert (1931); M-UAEH749, M-UAEH782,
M-UAEH783; La Mojonera, Zacualtipn de ngeles. Boletus hypocarycinus Singer (1945); M-UAEH754; La Mojonera, Zacualtipn de
ngeles. B. miniato-olivaceus Frost (1874); M-UAEH781; La Mojonera,
Zacualtipn de ngeles. B. rubropunctum Peck; M-UAEH751,
M-UAEH762; Medio Monte, San Bartolo Tutotepec, and La Mojonera,
Zacualtipn de ngeles. Boletus sp. 1; M-UAEH752; La Mojonera,
Zacualtipn de ngeles. Leccinum albellum (Peck) Singer (1945);
M-UAEH766; Medio Monte, San Bartolo Tutotepec. L. eximium
(Peck) Singer (1973); M-UAEH767, M-UAEH768; Medio Monte, San
Bartolo Tutotepec. L. rugosiceps (Peck) Singer (1905); M-UAEH771,
M-UAEH772; La Mojonera, Zacualtipn de ngeles. L. sp.1;
M-UAEH753; La Mojonera, Zacualtipn de ngeles. L. tablense Halling
y G. M. Mueller (2003); M-UAEH750, M-UAEH761; La Mojonera,
Zacualtipn de ngeles. Phlebopus sp.1; M-UAEH763, M-UAEH764;
La Mojonera, Zacualtipn de ngeles. Phylloporus leucomycellinus
Singer y M.H. Ivory (1978); M-UAEH748; Medio Monte, San Bartolo
Tutotepec. Phylloporus sp.1; M-UAEH773; Medio Monte, San Bartolo

Tutotepec. Pulveroboletus cramesinus (Secr. ex Watling) M.M. Moser

ex Singer (1966); M-UAEH779, M-UAEH780; La Mojonera, Zacualtipn
de ngeles. Retiboletus retipes (Berk. y M.A. Curtis) Manfr. Binder y
Bresinsky (2002); M-UAEH769, M-UAEH770; Medio Monte, San Bartolo
Tutotepec, and La Mojonera, Zacualtipn de ngeles. Strobilomyces
confusus Singer (1945); M-UAEH169; Medio Monte, San Bartolo
Tutotepec. Tylopilus felleus (Bull. ex Fr.) Karsten (1818); M-UAEH760;
La Mojonera, Zacualtipn de ngeles. T. rubrobrunneus Mazzer y A. H.
Smith (1976); M-UAEH745, M-UAEH746, M-UAEH755, M-UAEH756,
M-UAEH757, M-UAEH758, M-UAEH759; Medio Monte, San Bartolo
Tutotepec, and La Mojonera, Zacualtipn de ngeles. T. tabacinus (Peck)
Singer (1896); M-UAEH742, M-UAEH743, M-UAEH784, M-UAEH785;
La Mojonera, Zacualtipn de ngeles, and Medio Monte, San Bartolo
Tutotepec. T. vinosobrunneus Hongo (1979); M-UAEH774, M-UAEH775,
M-UAEH776; La Mojonera, Zacualtipn de ngeles. Xanthoconium
separans (Peck) Halling y Both (1998); M-UAEH777, M-UAEH778;
Medio Monte, San Bartolo Tutotepec. Xerocomus sp.1; M-UAEH744; La
Mojonera, Zacualtipn de ngeles.