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Ernesto Ch. Rodr Í Guez-Ram Í Rez and Claudia E. Moreno
Ernesto Ch. Rodr Í Guez-Ram Í Rez and Claudia E. Moreno
BRIEF COMMUNICATION
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.
American Journal of Botany 97(5): 893898, 2010; http://www.amjbot.org/ 2010 Botanical Society of America
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[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
May 2010]
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.
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
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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.
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]
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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