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Scientia fungorum

versión On-line ISSN 2594-1321

Sci. fungorum vol.50  Xalapa  2020  Epub 10-Mar-2021 

Artículos científicos originales

Diversity of soil culturable fungi in the tropical montane cloud forest of Veracruz, Mexico

Diversidad de hongos cultivables en el bosque mesófilo de montaña en Veracruz, México

Rosa María Arias Mota1  *

Gabriela Heredia Abarca2 

1 Instituto Tecnológico Superior de Xalapa. Reserva Territorial SN, Santa Bárbara, C.P. 91096, Xalapa, Veracruz, México.

2 Instituto de Ecología, A.C. Km. 2.5 antigua carretera a Coatepec 351, El Haya, C.P. 91073, Xalapa, Veracruz, México.


Background: Cloud forest is one of the most threatened ecosystems in the world and more than half of its original area has been transformed for other land uses. Consequently, macro- and microorganisms of this ecosystem have likely undergone changes.

Objective: To analyze the diversity of saprobic filamentous soil cultured fungi in four cloud forest fragments and evaluate the similarity in species composition among fragments.

Methods: To detect and isolate soil microfungi, the soil particle filtration technique was used. Emerging colonies were transferred to a culture medium for subsequent quantification and identification. For each species, permanent and semi-permanent slide preparations were made, and taxonomic identification was performed based on morphological features.

Results and conclusions: From 20 soil samples and 2000 inoculated particles, 233 species were distinguished. The most common species were Myrmecridium schulzeri , Pestalotiopsis maculans, Trichoderma atroviride, Virgaria nigra, Trichoderma cremeum, Fusarium solani, Cordana terrestris, Aspergillus fischeri, and Penicillium olsoni. The most abundant species were Talaromyces flavus and Pestalotiopsis maculans. All the forest fragments had a high richness, diversity, and evenness in addition to a high turnover and high number of exclusive species.

Keywords: abundance; diversity index; complementarity; filamentous fungiz


Antecedentes: El bosque de niebla es el ecosistema más amenazado a nivel mundial, ya que la mitad de las áreas en donde prosperaba han sido transformadas. De manera que, las poblaciones de macro- y microorganismos de este ecosistema han sufrido cambios.

Objetivo: Analizar la diversidad de hongos saprobios filamentosos del suelo en cuatro fragmentos de bosque y evaluar la similitud de la diversidad y la composición de las especies entre los fragmentos.

Métodos: Para la detección y aislamiento de los micromicetos se utilizó la técnica de filtración de partículas de suelo. Las colonias que emergieron se transfirieron a medio de cultivo para su posterior cuantificación e identificación. Para cada una de las especies se hicieron preparaciones permanentes y semipermanentes, para su identificación morfológica.

Resultados y conclusiones: A partir de 20 muestras de suelo y 2000 partículas inoculadas, se distinguieron 233 especies. Las especies más comunes fueron Myrmecridium schulzeri, Pestalotiopsis maculans, Trichoderma atroviride, Virgaria nigra, Trichoderma cremeum, Fusarium solani, Cordana terrestris, Aspergillus fischeri y Penicillium olsoni. Las más abundantes fueron Talaromyces flavus y Pestalotiopsis maculans. Todos los sitios examinados exhibieron una alta riqueza, diversidad y equitatividad, con un alto recambio y un número elevado de especies exclusivas.

Palabras clave: abundancia; complementariedad; hongos filamentosos; índice de diversidad


Soil micromycetes critically affect ecosystems by participating in the degradation of soil organic matter and nutrient cycling. They also play an important role in soil trophic chains as a basic food source for fungivorous organisms as mites, springtails, and earthworms (Dighton, 2003). Micromycetes are mainly distributed in the superficial soil horizons and the rhizosphere zone, representing a high percentage of the total microbial biomass in soil (Swift et al., 1994). Because microfungi synthesize different kind of enzymes, along with macromycetes, bacteria, actinomycetes, and soil mesoand macrofauna, they participate to the decomposition of plant and animal remains, thereby contributing toward the elimination of organic wastes generated by ecosystems and nutrient recycling. During decomposition, micromycetes also liberate several minerals in soluble form, such as inorganic ions that can be more easily absorbed by plant roots, therefore supporting the fertility of ecosystems (Dighton, 2003).

Despite the ecological importance of soil saprobic micromycetes, there are very few studies addressing their diversity in tropical and semitropical forests. Tropical montane cloud forests (TMCF) exhibit a high diversity of plant species and communities, as a result of high humidity and mild temperatures that create favorable conditions for the coexistence of temperate and Neotropical flora (Rzedowski, 1996). Impressively, even though TMCF only covers 0.8 % of Mexico, it contains 10 to 12 % of all plant species recorded in Mexico, including 2,500 endemic plant species. Therefore, TMCF is considered the most diverse type of vegetation per unit area (Rzedowski, 1996). TMCF has an enormous value not only because of its high biodiversity and associated uses, but also because of the important ecosystem services that it provides, such as carbon capture, water catchment, water purification, erosion control, and sediment control in rivers.

These forests also provide regulating services, preventing or mitigating natural disasters such as landslides and flooding that affect large areas in Mexican lowlands (Bruijnzeel and Hamilton, 2001). Unfortunately, TMCF is the most threatened ecosystem in the world, with more than half of its area that has been transformed to other land uses. In Veracruz, Mexico, TMCF has mostly been modified or disappeared because of human settlements and the establishment of agricultural crops. Human activities and disturbances, such as habitat destruction, urban development, industrialization, agriculture, contamination, and pesticide use, can potentially affect the fungal diversity of these forests (Tsui et al., 1998). Given this context, the aim of the present study was to analyze the diversity and community structure of cultured saprobic filamentous soil fungi in four TMCF fragments with distinct landscape quality.

Materials and methods

Study area

The study was carried out in the Coatepec-Huatusco region, in the center of Veracruz, Mexico (elevation 1,500-2,100 masl). The average annual rainfall in the region varies between 1300 and 2200 mm, and the average annual temperature ranges from 12 to 19 ºC. Typically, there are three defined seasons: a relatively dry and temperate season from October to March (with cold northerly fronts), a dry and warm season from April to May, and a humid and warm season from June to October (Williams-Linera, 1997).

Four tropical TMCF fragments were selected in the central region of Veracruz. The soil type was classified as umbric andosol. The soil physico-chemical characteristics of the four study plots were determined following the protocols described in Geissert and Ibañez (2008) (Table 1). The composition of tree species is similar between the plots, although species dominance changes from one fragment to another (Williams-Linera and López-Gómez, 2008; García-de la Cruz et al., 2013) (Table 1).

Table 1. Study sites. Tropical montane cloud forest (TMCF) fragments in the central region of Veracruz. Soil physicochemical properties (organic carbon, available phosphorus (P), organic matter (OM) (gr/kg), soil pH, carbon-nitrogen ratio (C/N), Nitrogen (N), elevations and relief in the study sites. Index landscape quality and tree composition 

TMCF OC Available OM PH C/N N Elevation Relief Landscape Tree
Study sites (G KG-1) p (GR/KG) (GR/KG) Masl Quality Composition
key (mg/kg)
Tropical montane cloud forest 1 MIRADOR 30.08 1.75 6.8 5.16 12 2.86 1900 Hills of moderate to strong slope 276 Eriobotrya japonica, Quercus sartorii, Tapirira mexicana, Trema micrantha, Zinowiewia integerrima.
Tropical montane cloud forest 2 SANTUARIO 68.3 1.5 11.78 5.82 13.4 5 1500 Hills of moderate to strong slope 230 Carpinus caroliniana, Clethra mexicana, Liquidambar styraciflua, Myrsine coriacea, Quercus xalapensis, Senecio arborescens, Turpinia insignis.
Tropical montane cloud forest 3 MASCOTA 47.67 2.22 24.9 3.97 10.7 4.37 2000 Steeply sloping canyon slope 275.6 Alchornea latifolia, Clethra mexicana, Quercus affinis, Quercus leiophylla y Quercus salicifolia, Liquidambar styraciflua, Turpinia insignis.
Tropical montane cloud forest 4 CAÑADAS 41.33 0.1 10 4.53 9.9 4.05 2100 Steeply sloping canyon slope 280.2 Beilschmiedia mexicana, Brunellia mexicana, Hampea integerrima Quercus insignis, Quercus leiophylla, Quercus sartorii, Styrax glabrescens, Turpinia insignis, Tapirira mexicana.

Soil physicochemical properties, according to Geissert and Ibañez (2008)

Index landscape quality to López-Barrera and Landgrave (2008)

Elevations to Williams-Linera et al. (1997)

Tree composition to Williams-Linera and López-Gómez (2008); García-De La Cruz et al. (2013)

Sampling design

Two surveys (May and September 2017) were carried out in the four TMCF sites. At each site, five sampling points separated by 50 m (to ensure their independence) were chosen. To avoid edge effects, a distance of at least 100 m was placed between sampling points and the nearest road. The center of each sampling point was a tree. From these central points, two 1-m perpendicular axes were marked. At the ends of each axis, a 100 g soil sample was taken from a depth of 0-10 cm. In the laboratory, at room temperature (26 °C) the four soil samples of each sampling point were mixed to obtain a compound sample. The soil was dried at ambient temperature (26 °C) to remove excess water and stored at 5 ºC for 5 d until processing for isolation of fungi. In total, 40 compound samples (4 sampling sites × 5 sampling points × 2 samples) were analyzed.

Isolation, quantification, and identification of saprobic filamentous microfungi

To detect and isolate microfungi, we used a soil particle filtration technique (Bills et al., 2004). Fifty soil particles from each compound sample were sown in dichloran rose-bengal chloramphenicol (DBRC) agar in 10 Petri dishes (50 particles × 5 points = 250 particles × 4 sites = 1000 particles per survey × 2 surveys = a total of 2000 inoculated particles).

The Petri dishes containing the particles were incubated for 15 d. All emerging colonies were quantified and transferred to tubes with potato dextrose agar (PDA) culture medium for subsequent quantification and identification. For each species, semi-permanent slide preparations were made in lactic acid. Morphological identification was performed using taxonomic keys and specialized literature (Domsch et al., 1980; Gams and Bissett, 1998). Non-fruiting fungal colonies were quantified and classified as sterile mycelia.

Analysis of variables

For each survey, species accumulation curves were calculated to compare the richness of filamentous fungi among forest fragments and to estimate the specific richness per fragment and at the landscape level using the non-parametric Jackknife 1 and bootstrap richness estimators. The following variables were calculated to evaluate and compare the diversity of saprobic filamentous soil fungi among sites: a) total abundance of colonies, calculated as the total number of colonies isolated from 250 soil particles (50 particles × 5 sampling points = 250 × 2 surveys = 500 particles per site); b) relative abundance (RA %) of each species, calculated by dividing the number of colonies of a given species by the total number of isolated communities from a given site, and multiplying the result by 100; c) frequency of occurrence (FO %), calculated as the number of sampling dates on which a given species was isolated divided by the total number of sampling dates, multiplied by 100; d) species richness (S), equivalent to the total number of species present in each site; e) species diversity according to the Shannon-Wiener (H´) index; f) equitativity, calculated by dividing the Shannon diversity index by the logarithm of the number of taxa. These calculations were performed in the PAST software (ver. 1.84) (Hammer et al., 2001).

To determine dominance patterns, Whittaker (abundance-dominance) curves were calculated for each site; the total abundance of each species was plotted against the range of species (ordered from highest to lowest abundance). To detect differences in the abundance, richness, and diversity of species among sites, one-way analyses of variance (ANOVAs) were conducted after checking requirements for normal distribution and homogeneity of variance of data using Kolmogorov-Smirnov and Bartlett’s tests, respectively. When the effects of these latter factors were shown to be significant by the ANOVAs, paired Tukey HSD post hoc tests were performed. These analyses were conducted in the Statistical software (ver. 7). Complementarity between sites was estimated in the PAST software (ver. 1.84) using the Bray-Curtis index based on abundance data. A simple linear regression was performed in Statistical (ver. 7) to understand the relationships between species abundance, richness, and diversity and the landscape quality index (within a 2-km radius of each site) and physico-chemical soil characteristics of the sites.


Species richness

In the four TMCF sites, 233 species from 51 genera were recorded, 95 sterile strains and 11 Xilarial type strains. The largest and the fewest number of species were found at the MASCOTA site (MS) and SANTUARIO site (SS), representing 45 and 25 % of the total number of species recorded respectively (Table 2). According to the Jackknife 1 and bootstrap estimators, the species inventory at the landscape level represented 52-64 % of the expected morphospecies. The estimators confirmed that 57 species (Jackknife 1) to 133 species (bootstrap) are missing from the inventory (Table 2). The accumulation curves for the morphospecies did not stabilize for any of the TMCF fragments (Figure 1). With respect to species richness per site, the MS and SS had the highest (107 spp.) and the lowest (60 spp.) species richness respectively. Statistical analyses showed significant differences (F= 4.58, p= 0.008) in species richness among sites (Table 3).

Table 2. Observed and estimate species of saprobic filamentous microfungi in four tropical montane cloud forest (TMCF) fragments of central Veracruz, Mexico 

TMCF Observed species Estimate species Estimate species Inventory
Study sites Jack 1 Boostrap %
MIRADOR 99 173 125 79%
SANTUARIO 60 105 78 77%
MASCOTA 107 179 137 78%
CAÑADAS 93 160 120 77%
LANDSCAPE 233 370 294 80%

Figure 1. Accumulation curves of observed species from the assembly of saprobic fungi in four fragments of tropical montane cloud forest in Veracruz state, Mexico. 

Table 3. Abundance* (number of colonies isolated to 250 soil particle), Richness **, diversity ** (Shannon Index H´) and equitativity** of saprobic filamentous microfungi in four tropical montane cloud forest fragments of central Veracruz, México. s.d (Standar deviation) 

Forest Abundance Richness Diversity (h’) Equitativity
fragment Total Average±s.d Total Average±s.d Total Average±s.d Total Average±s.d
MIRADOR 184 18.43 ± 8.87 ab 99 13.2 ± 5.86 a 4.2 2.37 ± 0.49 a 0.93 0.96± 0.02 a
SANTUARIO 108 10.8 ± 3.93 b 60 7.3 ± 2.3 b 3.6 1.78 ± 0.44 b 0.90 0.91± 0.13 a
MASCOTA 217 21.9 ± 7.26 a 107 14.8 ± 4.51 a 4.3 2.52 ± 0.27 a 0.95 0.95± 0.03 a
CAÑADAS 155 15.5 ± 9.66 ab 93 11.5 ± 5.52 b 4.2 2.20 ± 0.48 b 0.94 0.96± 0.04 a

*Average of ten replicates in two sampling.

** Average of ten replicates in two sampling.

† Shared superscripts (a, b) by study sites indicate no signifiicant differences between them (p≤ 0.05).

Abundance and dominance patterns

The slopes of the abundance-dominance curves of the MIRADOR (MIS) and CAÑADAS sites (CS) are similar and less pronounced than those of the SS and MS (Figure 2). No species maintained the same position in the hierarchical order of dominance across the four forest fragments. Talaromyces flavus was abundant at the SS, whereas Myrmecridium schulzeri was abundant at the MS. Trichoderma atroviride and a sterile strain (53) were abundant at the SS, MS, and CS. Pestalotiopsis maculans was abundant at the MIS and moderately abundant at the CS. The majority of species were rare (68 %). Forty-seven percent were singletons (single individuals), and 20 % were doubletons (two individuals) (Figure 2). The total abundance of colonies varied from 108 to 217. Significant differences in total abundance were found among sites (F= 3.67, p= 0.02), with the highest abundance corresponding with the MS and the lowest with the SS (t= 0.014) (Table 3).

Figure 2. Whittaker plots (Rank/abundance plots) illustrating the abundance of colonies of the saprobic fiilamentous microfungi detected in the study sites. 

Diversity and equitativity

The diversity index for the four forest fragments ranged from 3.6 to 4.3, significantly varying among fragments (F= 5.36, p= 0.003). The highest value was found at the MS (Table 3), which significantly differed (ANOVA; F= 5.36, p= 0.003) from the SS (F= 5.36, p= 0.003). The equitativity among sites ranged from 0.90 to 0.94, without significant differences among sites (F= 0.93, p= 0.43) (Table 3).

Frequency of occurrence

In terms of distribution at the landscape level, the following species were detected across all sites in at least one of the two surveys: M. schulzeri, P. maculans, T. atroviride, V. nigra, T. cremeum, F. solani, C. terrestris, and P. olsoni (Table 4). The percent relative abundance of the species ranged from 2.9 to 76.5 % (Table 4). A high percentage of the species presented values lower than <5 %. Species with values between 10 and 16.7 % in at least one survey included Fusarium poae, F. tricinctum, T. cremeum, and T. koningii. With respect to frequency of occurrence, the following categories were established for the species: very frequent (FO= 100 %), frequent (FO= 75 %), occasional (FO= 50 %), and sporadic (FO= 25 %). Most of the micromycetes isolated were sporadic (153 spp., 64.5 %); some were occasional (55 spp., 23.2 %), and few frequent (16 spp., 6.7 %) or very frequent (12 spp., 5.06 %).

Table 4. Frequency of occurrence % (Fr) and relative abundance average of the saprobic filamentous microfungi found at the study sites over the survey. *Only strains identified at the species level are included 

Species Fr mis ss ms cs Species Fr mis ss ms cs
Acremonium chryrosogenum 25 - - - 0.3 Fusarium poae 25 - - - -
Acremonium kiliense 50 - - - 0.5 Fusarium semitectum 25 - - - -
Acremonium murorum 50 - - 0.8 0.8 Fusarium solani 100 1.3 1.1 0.4 1.4
Acremonium potronii 25 - - - - Fusarium solani var. coeruleum 25 - - - -
Acremonium roseolum 50 1.1 - - - Fusarium stilboides 25 0.4 - - -
Acremonium strictum 25 - - - - Fusarium trichothecioides 25 - - - -
Aspergillus niveus 25 - 2.2 - - Geomyces pannorum 50 - - 0.7 0.4
Aspergillus ochraceus 25 - - 0.8 - Geotrichum candidum 75 0.5 - - -
Aspergillus versicolor 25 - - - - Gliocadium penicilloides 25 - 1.4 - -
Beauveria bassiana 50 - - - - Gliocadium solani 50 - - 0.4 -
Chaetomium ampullare 25 - - - - Gonytrichum macrocladum 25 - 0.8 - -
Chaetomium aureum 25 - - - - Hypoxilon serpens 25 - - - 0.4
Chaetomium fumicola 25 - 0.8 - - Hypoxilon serpens var. serpens 25 - - - -
Chaetomium globosporum 25 - - - - Marianaea elegans 50 2.5 - - 2.5
Chaetomium robustum 50 - - 0.7 - Metharrhizium anisoplae 25 - - - -
Chloridium chlamydosporis 50 - - - - Metharrizium marquandie 50 2.0 - - 1.4
Chrysosporium serpens 25 - - 0.7 - Monocillium indicum 25 - 0.6 - -
Cladosporium cladosporioides 50 - 0.8 - - Mortierella vinosa 25 - 1.7 - -
Cladosporium sphaerospermum 50 1.1 1.7 - - Myrothecium roridum 50 0.6 1.4 - -
Cordana oblongispora 25 0.6 - - - Myrmecridium schulzeri 100 1.5 0.8 1.8 0.4
Cordana pauiceptata 25 - - - - Nectria haematococa 25 0.4 - - -
Cylindrocarpon oidium 25 - - 1.6 - Neosartoria fischeri 100 - - 0.4 0.5
Eladia saccula 25 - 0.7 - - Oidiodendron tenuisinum 25 - 1.4 - -
Eupenicillium ludwigii 25 - 0.8 - - Paecillomyces clavisporus 25 - - - -
Eurotium chevalieri 25 - - - - Paecilomyces carneus 25 - - - 0.8
Fusarium decemcellulare 50 0.5 4.5 - - Paecilomyces clavisporus 50 0.7 - - -
Fusarium fusaroides 25 0.6 - - - Paecilomyces griseoviridis 25 - - 1.8 -
Paecilomyces hawaiiensis 25 - - - - Scopularopsis brumptii 25 - - 0.8 -
Paecilomyces lillacinus 50 0.8 - - - Sesquicillium candelabrum 50 - - - -
Penicillium brevicompactum 50 - - 0.6 - Sporotrix schenckii 25 - - - 0.4
Penicillium citrinum 25 - - 0.4 - Stachybotris albipes 25 - - 0.8 -
Penicillium decumbens 75 - 1.5 2.9 0.5 Stachybotris parvisporus 75 5.1 - 0.9 2.5
Penicillium duclauxii 25 - - - - Talaromyces flavus 75 0.6 3.6 - -
Penicillium fellutanum 50 0.7 - 1.9 - Talaromyces intermedius 25 - - 1.2 -
Penicillium glandicola 75 0.7 - 0.4 1.4 Talaromyces trachysperum 25 - - - 0.7
Penicillium implicatum 50 0.5 - 1.2 - Talaromyces udagawae 25 - - 2.1 -
Penicillium islandicum 25 - - - 1.4 Talaromyces wortmanii 25 0.6 - - -
Penicillium italicum 50 - 2.2 - - Torula herbarum 25 - - 1.1 -
Penicillium lividum 75 - - - - Trichoderma anam. Podostroma alutaceum 25 - 0.7 - -
Penicillium melinii 50 0.6 - - - Trichoderma atrovirde 100 - 3.6 2.5 2.8
Penicillium olsoni 100 - 0.6 - 1.5 Trichoderma cremeum 100 0.4 - 0.8 0.9
Penicillium restrictum 25 0.5 - - - Trichoderma hamatum 25 - - 1.4 -
Penicillium rugulosum 50 - - - 1.4 Trichoderma harzianum 75 - 0.8 - 0.9
Penicillium verruculosum 75 - 7.3 0.4 - Trichoderma koningi 25 - - - 0.3
Penicillium vulpinum 50 - - - 0.5 Trichoderma longipiles 25 - - 0.7 -
Pestalotiopsis maculans 100 3.0 0.8 0.8 1.7 Trichoderma oblongispora 75 - 1.1 0.4 -
Pestalotiopsis uvicola 25 - - - - Trichoderma pseudokoningii 25 - - - -
Phialocephala phycomyces 25 - - - - Trichoderma strictipitis 50 - - 0.7 -
Phialophora mustae 25 - - 0.7 - Trichoderma viride 50 - - 0.7 -
Phialophora richardsiae 75 0.4 - 0.8 0.3 Verticilliu suchalsporium 50 - - 2.0 -
Pseudobotrytis terrestris 100 0.6 - - 2.5 Verticillium alboatrum 25 - - 0.4 -
Pyrenochaeta unguis 50 0.7 - 0.7 - Verticillium fungicola 75 0.4 0.8 - 0.5
Sagenomella diversispora 25 - - - - Virgaria nigra 100 2.2 1.5 0.7 0.3
Scopularipsis brevicaulis 50 - - - 0.7

Complementarity among sites

The complementarity between the four sites was extremely high. The values of the complementarity index ranged from 68 to 84 %, with an average of 74.89 % (Table 5). The highest complementarity (greatest difference in fungal composition) was found between the MIS and SS (84.2 %). The lowest degrees of complementarity (greatest similarity in fungal composition) were found between the MIS and CS (68.7 %) as well as between the MS and CS (68.5 %) (Table 4). The MIS and MS had the greatest number of shared species (39). Forty-five percent of the species at the MS were exclusive (49 spp.). Meanwhile, 37 and 38 species were exclusive to the MIS and CS respectively, and 26 species to the SS (Table 5).

Table 5. Complementary matrix in the composition of saprobic fiilamentous microfungi calculated by the Bray Curtis index (above diagonal) and number of species shared (under diagonal) in the study sites 

Tmcf Mirador Santuario Mascota Cañadas
Study Sites
MIRADOR 99/38 15.75 26.3 31.27
SANTUARIO 21 60/26 22.0 24.3
MASCOTA 39 24 107/49 31.55
CAÑADAS 36 22 33 93/37

Numbers in black indicate the total number of species for each site/ exclusive species. The percentages of complementarity that vary from zero, when both fragments are identical in species composition, up to 100, when the species of both fragments are completely different, down the number of shared species.

Relationship of abundance, species richness, and species diversity with landscape quality and soil physico-chemical characteristics

In the simple regression analyses, a significant relationship was only found between the diversity of saprotrophic filamentous fungi and the landscape quality index, indicating that a greater diversity of morphospecies was found as the landscape quality increased (p= 0.018) (Figure 3). Some interesting tendencies were observed between soil pH and morphospecies diversity (p= 0.14), abundance (p= 0.16), and richness (p= 0.14), even though the results were not significant (Figure 3).

Figure 3. Relationship between diversity index. A: With index landscape quality. B: With species richness. C: With abundance. D. With the soil pH of forest fragments. 


Fungi are important components of the biodiversity of tropical forests. The colonization and decomposition of soil organic matter are performed by a wide range of microorganisms, yet fungi and bacteria play a particularly important role in nutrient recycling. The overview of studies on soil fungal diversity largely depends on the techniques used to detect fungal communities. The soil particle filtration technique is widely used because it favors the isolation of fungi whose hyphae are associated with soil particles and, therefore, are active in soil (Bills et al., 2004). Soil washing generally eliminates the spores of rapid-growth fungi and allows slow growing species to be expressed. However, fungi are nutritionally diverse, so there is not a single cultivation medium appropriate for all fungal species. In addition, many isolated fungi may require natural substrates to form fruiting bodies, complicating taxonomic identification by traditional methods (Bills and Polishook, 1994). Considering these limitations, molecular techniques would be of great assistance in identifying isolated fungal strains. Thus, a detailed morphological description was made of each of the 104 sterile strains, and their abundance was quantified in each survey. In this way, all the isolates were accounted for enabling calculation of the evaluated parameters.

Most of the studies on saprobic soil micromycetes in primary ecosystems have been carried out in temperate regions, as coniferous forests in Canada (De Bellis et al., 2007), the United States (Gochenaur, 1978), and China (Cheng et al., 2015). Fewer studies have been carried out in Africa (Persiani et al., 1998), Malaysia (Varghese, 1972; Bettuci and Roquebert, 1995), Brazil (Pfenning, 1997), and India (Panda et al., 2010; Saikia and Joshi, 2012; Chandini and Rajeshwari, 2017).

The present study demonstrated the high richness of saprotrophic soil fungi in TMCF in Mexico. A total of 233 species were identified from 666 isolates. Most studies on saprobic soil micromycetes in tropical forests have reported a smaller number of taxa, except for Persiani et al. (1998), who reported 519 species in a forest along the Ivory Coast. Previous studies recorded 38 species in Malaysia (Varghese, 1972); in India 63 species (Saikia and Joshi, 2012), 81 species (Chandini and Rajeshwari, 2017) and 118 species (Panda et al., 2010) and 80 species in a tropical forest of Brazil (Pfenning, 1996). In recent years, DNA sequence-based methods have been used to survey soil fungal diversity of various terrestrial ecosystems, including forests; He et al. (2017) recorded 7501 OTU, 43 % were saprobic fungi. Shi et al (2014) detected 7630 OTUs, saprobic fungi representing 80 % of these. Bueé et al. (2009) recorded an average of 830 fungal operational taxonomic units (OTUs) per site in temperate forest.

Soil is an important habitat because it shelters a wide diversity of species and provides a wide variety of important environmental services. At the landscape level, the representativeness of the inventory was 52 to 64 % according to the richness estimators (Jackknife 1 and bootstrap). For each site, the representativeness of the inventories ranged from 42 to 79 %. Overall, the inventories of all forested sites and each forested site included more than 50 % of the estimated species. We consider that the sampling effort allowed to detect an overview of the composition of the soil fungal community. Molecular methods offer the prospect of a more thorough documentation of diversity. However, while numerous recent studies (Buée et al., 2009, Jumpponen and Jones 2009) have utilized high‐throughput sequencing to examine various aspects of fungal biodiversity, these studies have failed to saturate a sampling (rarefaction) curve.

In this study the community of soil fungal species in the TMCF fragments presented a Raukier pattern: few species were abundant, and many species were uncommon or had low abundances. A group of species common to cloud forests were detected in all fragments: M. schulzeri, P. maculans, T. atroviride, V. nigra, T. cremeum, F. solani, C. terrestris, A. fischeri, and P. olsoni. However, these species were not always the most abundant. The most abundant species were T. flavus at the SS, M. schulzeri at the MS, and P. maculans at the MIS. Talaromyces flavus has been frequently observed in North America, Europe, and Australia (Beuchat, 1986). Its ascospores can reportedly survive high temperatures. Pestalotiopsis maculans is a common and abundant habitant in the leaf litter of some TMCF trees in Mexico (Heredia et al., 2000) and Costa Rica (Bills and Polishook, 1994). The presence of this latter microfungi at all the studied sites shows that it can successfully grow from the leaf litter through the first soil horizons. Myrmecridium schulzeri, a lignicolous ascomycete that represents the imperfect state of the genus Ophiostoma, is associated with the decomposing wood of different TMCF tree species.

Different studies suggest that fungal diversity is greater in tropical regions than temperate regions (Suryanarayanan et al., 2009). In tropical forests, employing traditional survey methods there have been reported diversity index (H´) values of 1.8 (Grantina, 2011), 2.4-2.5 (Saravanakumar and Kaviyarasan, 2010), 3.4 (Devi et al., 2012), 3.1-3.5 (Satish et al., 2007), 3.7 (Banakar et al., 2012), and 4.1 (Panda et al., 2007). Devi and Dkhar (2014) reported H´ values of 2.7 for fungi in an Indian forest with similar vegetation and altitudinal characteristics as cloud forest. Comparatively, the fungal diversity index in the present study ranged from 3.6 to 4.3, confirming the high species diversity of the studied TMCF.

Of the 233 species detected, the MS had the highest number (107 spp.), followed by MIS (99 spp.), CS (93 spp.) and, finally, SS (60 spp.). With respect to beta diversity, the study sites presented a high richness, diversity, and equitativity of filamentous saprotrophic fungal morphospecies at the regional level. In addition, high morphospecies complementarity and high morphospecies turnover among the fragments was found. This may be related with the degree of alteration of the sites reflected by the amount of open areas and the landscape quality. In particular, the SS had the lowest diversity. López-Barrera and Landgrave (2008) assigned this latter site a low value on the landscape quality index, while the rest of the fragments were considered high quality. The landscape quality index considered a 2-km radius around each point and contemplated open areas and areas without vegetation cover in addition to incipient, intermediate, and dense shade, which may be interpreted to correspond with certain types of vegetation.

The qualitative and quantitative differences in fungal populations between fragments indicate that vegetation and proximity to urban areas influence the micro-fungal populations of the soil. Disturbances to soil and vegetation could be a determining factor of the lower fungal count at the disturbed forest site (SS). Liu et al. (2016) reported that soil microbial diversity decreased with increasing disturbance. Carney and Matson (2006) showed evidence of the human alteration of soil microbial communities via the modification of plant community composition and diversity. On the other hand, high plant diversity also has a strong impact on the soil microbial community, mainly because of increased plant production (Liu et al., 2016).

Environmental factors that influence plant and animal distribution have been more widely studied than those that control the patterns of distribution and community composition of soil microorganisms (Rousk et al., 2010). Regarding the microbial communities, McCulley and Burke (2004) found that plant species composition, soil type, seasonal variability, temperature, and availability of organic substances are primarily factors that controlled them. Meanwhile, saprophytic fungi are sensitive to soil conditions, pH, texture, moisture, and oxygen level (Setala and McLean, 2004).

Contrary to what we expected, in this study we didn’t found any significant correlation (p>0.05) between the physico-chemical soil parameters and the diversity, richness, and abundance of saprobic fungi. However, some interesting tendencies were observed for soil pH, which influenced the abundance, richness, and diversity of saprobic fungal species (70 % related), although not significantly (p= 0.14, p= 0.16, p= 0.14 respectively). Specifically, abundance, diversity, and richness were higher in the sites with a pH of around 4-5 (CS, MIS, and MS) and lower in the SS, with a pH fluctuating around 6. The impact of pH on soil microbial communities has been widely described in previous studies. Generally, studies on fungal biomass have shown that lower pH tends to favor fungal development (Rousk and Nadkarni, 2009). In a boreal forest, Högberg et al. (2007) observed that fungi strongly decreased as the range of soil pH increased. Pennanen et al. (1998) also found that fungal growth increased at pH values of lower than 4 in forest soil, and similar findings were reported by Banakar et al. (2012). The results described herein estimate the composition and diversity of the soil fungal community in four TMCF sites. The findings clearly reveal that TMCF soil in the central region of Veracruz, Mexico, exhibits a high richness, diversity, and equitativity of saprobic filamentous fungal species, as well as a high turnover rate and high number of exclusive species. Greater knowledge of the ecology of soil fungal communities can enable the development of strategies to conserve native saprobic species or to use them for bioprospecting industrially important enzymes or biomolecules.


We thank all landowners for granting access to the field sites. Alisson Marie Jermain revised the English version of the manuscript.


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Received: July 08, 2020; Accepted: September 09, 2020; Published: October 10, 2020

*Corresponding author. Rosa María Arias Mota,


The authors declare that they have no conflicts of interest.

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