The cultural significance of wild mushrooms in San Mateo Huexoyucan, Tlaxcala, Mexico

SMH is located in the southwestern region of Tlaxcala, Mexico (Figure 1). This region is part of the trans-Mexican volcanic belt and has an elevation of 2,252 meters above sea level [14]. SMH belongs to the Panotla Municipality and has a total population of 1732 individuals, including 898 women and 834 men. The main activities in SMH are agriculture and stockbreeding [14]. Mushroom collection is limited to rainy seasons and is conducted in open areas surrounding the community and near oak tree forests located several kilometers away from the town. The wild vegetation observed in the upper parts of the municipality includes a community of Pinus pseudostrobus, Quercus glabrescens, Quercus spp., and white cedar (Cupressus benthamii). There is abundant secondary bush vegetation in the areas between the surrounding hills where the most common species include Juniperus deppeana, Eysenhardtia polystachya, Opuntia spinulifera, Wigandia urens, and Amelanchier denticulata. The most common species in the plain area of SMH include Agave spp., Schinus molle, Tecoma stans, Cassia tomentosa, Buddleia cordata, Argemone spp., Erythrina spp., Ricinus communis, Casimiroa edulis, Opuntia ficus-indica, Nicotiana glauca, and Jacaranda mimosifolia[15]. SMH has a sub-humid climate with summer rains and an average annual temperature of 13.6°C [16].

Local traditional mushroom knowledge was assessed by extensive field trips and interviews with 166 people [17]. Due to the length and time involved in conducting the interviews, only 33 individuals from SMH, including 25 women and 8 men (ages 6 to 95 years) were randomly selected for in-depth interviews on the CS of local mushrooms using the CSI.

The interviews incorporated free listing where each person was asked to name 20 mushrooms to obtain mushroom FM and MO [18]. Interviewees were asked seven questions about the 20 most frequently mentioned mushroom species for a total 140 questions. The CSI was then calculated as previously described [6] and modified for mushrooms [13]. The CSI was further modified based on community-specific characteristics to exclude economic importance. Interviews were conducted between 2009 and 2011, and responses were analyzed by interviewee age and gender.

The EMCSI of mushrooms in the SMH area was determined using six sub-indices or cultural variables and the following equation:where PAI is the perceived abundance index, FUI is the frequency of use index, TSAI is the taste score appreciation index, MFFI is the multi-functional food index, KTI is the knowledge transmission index, and HI is the health index.

Interviewees were asked seven questions for each mushroom species. To determine PAI, interviewees were asked “How many of these mushrooms can be found in the forest?” with an image of different abundance categories (Figure 2) [13]. The following categories were used: none or no answer (0), rare (2.5), medium (5), abundant (7.5), and very abundant (10).

The hierarchy of answers for the other six sub-indices is shown in Table 1. Interviewees were asked, “How often do you eat this mushroom?” to determine FUI. TSAI was assessed by asking the interviewees “How much do you like this mushroom?” and “Which face expresses what you feel eating this mushroom?” while using a graphical stimulus (Figure 3) [13]. The MFFI was determined by asking interviewees “How do you cook this mushroom?” High values were allocated to species cooked alone, (i.e., dishes comprised solely of a single species of mushroom), and values diminished as other ingredients were added. The KTI assessed how many generations of SMH villagers had been picking and using mushrooms using the question “Did your mother or father, grandmother or great grandmother use this mushroom?” When interviewees reported only recently using the mushroom, they were also asked, “Who taught you the use of this mushroom?” The HI was measured by asking “In your opinion, how safe or healthy is eating this mushroom?” and “Is this mushroom harmful?”

All sub-indices were evaluated using the same scale of 0 to 10. A value of 0 indicates no negative values. All values were given the same weight, and each sub-index was averaged across all persons interviewed.

Photographs of fresh mushrooms were used as recognition stimuli (Figure 4). A pilot-test was conducted where the photographs were shown to several persons to evaluate their usefulness and accuracy for the different mushroom species.

The Edible Mushroom CS Pondered Index was calculated (EMCSPI) by multiplying the EMCSI by the Mention Index (MI = number of mentions/number of persons interviewed × 10).

The Ordinal Rank Value (ORV), also known as OM [19] was calculated using the following equations:

Spearman correlations were used to compare the six CS sub-indices between each mushroom species using STATVIEW software [20].

Interviewees were asked several questions to calculate the CS of a mushroom to them (intracultural evaluation) [1] and to determine their significance criteria. The following questions were asked [21]: “Which mushroom do you consider the most important?”; “Why is this mushroom important?”; “Is there any other reason why this mushroom is important to you?”; and “Anything else?” [21]. These interviews were conducted in 2010 during the dry season. The answers and their frequency were analyzed. The significance criteria mentioned most frequently were considered most important. Using these data and the results of an ethnomycological analysis previously conducted in the community [17], the Economic Index established by Garibay-Orijel et al.[13] could be disregarded. Mushrooms were most frequently used for eating, and only a few individuals collected mushrooms to sell in the SMH community.

The relationships between mushroom significance calculated by the CS sub-indices were analyzed using the Index of Euclidean distance. Grouping was analyzed using a principal components analysis (PCA), where rows identified the species that formed groups and columns determined the relationship between the six CS sub-indices. A multi-dimensional scaling (MDS) analysis was also conducted to confirm and improve the PCA results. The original matrix included 20 mushroom species (those mentioned by 10% of the persons interviewed), and the values obtained for each sub-index and the pondered index. These analyses were performed using NTSYS-pc software [22].

Mushrooms were collected from the Quercus forest closest to SMH during the rainy seasons of 2009 and 2010. SMH families and individuals, including seniors and/or children, accompanied the investigators during collection. Traditional mushroom names, sampling areas, and the season mushrooms were collected were also recorded. Mushrooms were collected and processed as previously described [23] and then were stored at the TLXM Herbarium of the Autonomous University of Tlaxcala. During the rainy season of 2010, the wild mushrooms were collected, photographed, and subsequently identified using general and specialized field guides according to genus. In addition, specialized literature was reviewed [24‐27].

The mushroom species mentioned most often by the 33 individuals interviewed included A. aff. basii (31 mentions), A. campestris (30 mentions), Ramaria spp. (22 mentions), Russula spp. (17 mentions), Ustilago maydis (17 mentions), Boletus variipes (13 mentions), and M. oreades (12 mentions; Table 2). Only four of these mushrooms species were mentioned by more than 50% of interviewees, followed by six species mentioned by more than 30% of interviewees and 10 species mentioned by less than 30% of interviewees. A previous study reported similar results in Ixtlán de Juárez, Oaxaca [13]. In that research, 95 individuals were interviewed, and 21 traditional mushroom names, corresponding to 37 mushroom species, were identified. Amanita caesarea complex, Ramaria spp., Neolentinus lepideus, and Agaricus pampeanus were recognized by more than 50% of those interviewed. Several of these mushrooms are known nationally or globally, while others have economic importance. Most of these mushrooms were highly prized for their taste. Other mushrooms, while mentioned less frequently, were also used and appreciated, and individuals were very familiar with these species.

The EMCSPI represents the significance of a mushroom species to the SMH community after the number of persons mentioning each mushroom and the total number of persons (N = 33) interviewed are taken into account. EMCSPI values ranged from 2.18 to 388.05. Using this measure, the species with the most CS included A. aff. basii (388.05), A. campestris (381.17), Ramaria spp., Russula spp. (277.80), and B. variipes (114.32). These species, except for a single Boletus species, are consistent with those observed in previous studies. Here, the ranking of these species’ significance changed because the value obtained for the mention index (MI) was included. Thus, the EMCSPI is based on the relative value of the number of mentions, and species with many mentions have a higher value. The remaining mushrooms had values under 100; the species with the least CS were R. mexicana, L. perlatum, L. gpo. decastes, A. gpo. vaginata, and S. strobilaceus.

In the present study, six mushroom species were considered significant by intracultural evaluation: A. aff. basii (14 people), A. campestris (12), C. cyathiformis (3), L. indigo (2), B. variipes (1), and M. oreades (1). The interviewees reported 11 reasons for the significance of these mushrooms: taste (27 mentions [m]), naturally grown (16 m), nutritional value (14 m), lack chemical additives (9 m), abundance in the forest (8 m), meat-like taste (3 m), rapid growth (2 m), pleasant smell (2 m), frequent consumption (2 m), expensive price (1 m), and non-poisonous (1 m). These results are consistent with the CS obtained using the various indices (EMCSI and EMCSPI).

The phenogram in Figure 5 shows two groups of species (Euclidian distance of 12.03). Group A is comprised of the species with the most CS based on the diverse variables included in the analysis (A. aff. basii, A. campestris, Ramaria spp., Russula spp., U. maydis, B. variipes, and M. oreades; Table 3). The species most similar in this group are B. variipes and M. oreades, followed by A. aff. basii and A. campestris. Group B is divided into two sub-groups (Euclidian distance of 5): (a) H. lactifluorum, C. cyathiformis, L. indigo, Lactarius sp., and P. opuntiae; and (b) C. gibba, A. rubescens, R. mexicana, L. perlatum, L. aff. decastes, Amanita gpo. vaginata, C. gpo. cibarius, and S. strobilaceus. In the first Group B sub-group, the closest species are C. cyathyformis and L. indigo. In the latter sub-group, S. strobilaceus is independent from all other members with a Euclidian distance of 2, while L. perlatum and L. gpo. decastes are most similar with identical values in four sub-indices (HI, PAI, TSAI, and EMCSI).

A PCA was used for multivariate analyses (Figure 6). Comparisons between principal component 1 (PC 1) vs. PC 2 resulted in four main groups of mushrooms. Group A had values <2.23 (Figure 6, left), Group B had values >2.23, and Groups C and D had values >4.15 (Figure 6, right). Group A is comprised of the species with the least significance: R. mexicana, A. rubescens, L. perlatum, L. aff. decastes, C. gpo. cibarius, C. gibba, A. gpo. vaginata, and S. strobilaceus. Group B is comprised of five species with more significance than those in group A: L. indigo, C. cyathiformis, H. lactifluorum, L. yazooensis, and P. opuntiae. Group C is comprised of M. oreades, B. variipes and U. maydis, and Group D is comprised of Russula spp., Ramaria spp., A. campestris, and A. aff. basii. A. campestris and A. aff. Basii were the most distant in Group D. Similarity between these two genera were observed among the mushrooms in this group, which included several species mentioned by more than half the interviewees (Russula spp. and Ramaria spp).

The different species were grouped based on similar values obtained in the different sub-indices. The first three components explained 99.24% of the variation using Eigen analyses. The most important variables that affected grouping were the TSAI (0.99), HI (0.98), KTI, and FUI (0.97) in PC 1; the MI (0.31) and MFFI (-0.23) in PC 2; and the PAI (0.32) in PC 3. These species were hierarchically arranged based on their significance to the SMH community, which was reflected in the sub-indices values. The PCA, which compared the sub-indices, showed that the PAI and FUI grouped together while the HI and KTI, the TSAI and MFFI, and the MI did not (Figure 7).

Six mushroom species explained the observed variation in PC 1 (H6, C. cyathiformis, L. indigo, C. gibba, H18, and L. perlatum; values >0.90) and PC 2 (Russula species and B. variipes; values > 0.90; Table 3). The first three components explained 92.96% of the variation. These results are consistent with those obtained from the sub-indices. A. campestris was the most significant mushroom species due to its abundance (PAI), nutritional value (HI), and generational knowledge (KTI); similarly, A. aff. basii was also significant due to its frequent use (FUI), taste (TSAI), and reputation (MI). High values were also obtained for the Russula and Ramaria mushrooms since these species were considered sufficiently nutritional and were consumed alone.

The multidimensional scaling analysis (MDS) had a stress value of 0.2249 and had results consistent with those of the PCA for grouping some species at the maximum number of iterations (Figure 8): Group A) R. mexicana, L. perlatum, A. rubescens, C. cibarius, C. gibba, L. aff decastes, A. aff. basii, A. gpo. vaginata, A. campestris, S. strobilaceus, L. indigo, and C. cyathiformis; Group B) Russula spp., Ramaria spp. M. oreades, Lactarius sp., and B. variipes; and Group C) H. lactifluorum, Ustilago maydis, and P. opuntiae. All sub-indices had similar contributions to the CS of the mushroom species, and no significant differences were observed. However, A. campestris or A. aff. basii remained the most significant, and the different groups formed by both analyses contained species with similar significance values.

The economic index used in Ixtlán was eliminated from the present study because mushrooms are primarily used for food in SMH and have little economic importance. One of the main limitations of our study was the lack of a complete list of wild mushrooms that grow in the SMH, which might have affected the calculated index values. We identified three Ramaria species (R. suaveolens, R. botrytoides, and R. percisina) and ten Russula genus species (R. anthracina, R. cyanoxantha, R. aff. decipiens, R. delica, R. macropoda, R. mariae, R. mexicana, R. ornaticeps, R. romagnesiana, and R. xerampelina). Other species of both genera (between four to six more species) were acknowledged and used by the local people but only had generic names and were not accurately identified.

The Quercus forests have a diverse selection of wild mushroom species, particularly mushrooms of the Amanita, Ramaria, and Russula genera. While free listing, individuals reported common names that were not always associated with specific taxa. Because many traditional criteria, such as odor and taste, are used to identify mushrooms with similar morphologies, using photographs as a stimulus also had severe limitations that could affect the CS calculated for some species. The high CS of A. aff. basii in the SMH community was one of the most relevant results of this study. This mushroom grows in oak forests in the center of Mexico. Several studies of mushroom CS in Mexico have shown that certain species have greater CS. Ramaria spp., B. pinophilus, A. aff. basii, C. gpo. cibarius, and L. decastes are the most frequently mentioned species in the temperate areas of Mexico [14, 10, 29, 11, 30, 31]. A. gpo. caesarea is well known at a broad geographic level and is highly valued in Mexico, Turkey, and Nepal. In contrast, B. gpo. pinophilus is highly valued in Europe and Central America, and C. gpo. cibarius is highly valued in 45 different countries worldwide [32]. Notably, in different cultures in Mexico, certain mushroom species are particularly relevant, including: Turbinellus floccosus (Schwein.) Earle ex Giachini and Castellanoin in San Isidro Buensuceso, Tlaxcala [10]; Neolentinus lepideus in Ixtlán de Juárez, Oaxaca [11]; and Helvella spp. in Corral de Piedra and San Juan in the Amanalco municipality [32]. This pattern is also observed worldwide [33].

The present study also showed that mushrooms growing in open areas, such as A. campestris, M. oreades, U. maydis, and C. cyathiformis, also had CS. This suggests that the relevance of other environments where saprotrophic mushrooms are available is also important. SMH is located relatively far from the forest, and mushroom collectors have to pass through farming areas and plains to reach it. When passing through these open areas, collectors also gather any mushrooms they find in those environments. During the dry season, uncontrolled fires decimate the forests and generate many large open areas. Therefore, mushrooms outside the forest become more important as an available resource for the local population.