People from the three communities still conserve the tradition of collecting mushrooms, mostly for self-consumption and some for sale, depending on the abundance. We recorded 155 Spanish common names and 21 Otomí common names (Table 2), and “hyethe” was the main word used to refer to mushrooms, that means “in rainy season” or jo (that means “sponge”) as Núñez-López [31] reported for some species. A total of 33 mushrooms species had ethnomycological value (Table 3), mainly Boletes [22] and Agarics [17].
Table 2 Correspondence between scientific and folkloric name Table 3 Cultural significance values for edible wild fungi in Tesquedó, Xajay, and Tenasdá communities in Amealco, Querétaro, Mexico EMCSI sub-indexes
Citation Index (QI). Amanita basii Guzmán & Ram.-Guill., Lactarius indigo (Schwein.) Fr. and Fistulinella wolfeana Singer & J. García, which was the first record of edibility [47], were the most mentioned species during the surveys; these results are comparable to those of Alonso-Aguilar et al. [23] where A. basii is the most important mushroom in San Mateo Huexoyucan, Tlaxcala, México, and Montoya et al. [16] found it only by using a free list. We can argue that most of the time, the first mushroom cited is the most important. In contrast, other genus such as Ramaria Fr. ex Bonord is considered the most important to people of La Laguna de Fúquene, Andes Nororientales [26]. Here, Helvella crispa (Scop.) Fr. was mentioned to be consumed by only one person. Lyophyllum P. Karst had few mentions, which might be because only few people know where to find it [29] (Fig. 1).
perceived abundance index (PAI). Lactarius indigo, Russula aff. brevipes Peck, R. aff. cyanoxantha (Schaeff.) Fr., and Fistulinella wolfeana had the highest values, while Amanita novinupta Tulloss & J.E. Lindgren, Boletus auripes Peck, Gymnopus dryophilus (Bull.) Murrill, Helvella crispa, and Suillus granulatus (L.) Roussel had the lowest values. It is important to point out that Russula and Agaricus campestris L. were the most abundant according to with Peña-Cañón & Enao-Mejía [26], while A. campestris is the most abundant for Alonso-Aguilar et al. [23]; this result could be linked to the vegetation or the season where the study was carried out. Even when Russula spp. or S. granulatus is common in the forest, people preferred to collect other mushrooms because they do not consider these palatable. Sometimes, when Ramaria spp. is not common, people prefer to walk long distances to find it. In this case, as mentioned by Bautista [29], some species such as A. basii are more difficult to find due to the condition of forests. Some informants mentioned that the number of mushrooms they could find is decreasing, arguing that the abundance and uses were higher in the past.
Frequency of Use Index (FUI). Amanita basii, Boletus spp., Fistulinella wolfeana, Lactarius indigo, Ramaria spp., and Ustilago maydis (DC.) Corda are consumed four times, or more, during the rainy season, and sometimes even four times a week, depending on their abundance. Peña-Cañón and Enao-Mejía [26] and Alonso-Aguilar et al. [23] mentioned that the most commonly used fungi were Russula sp. and A. basii, and Garibay-Orijel et al. [22] said that Cantharellus Juss and Pleurotus (Fr.) P. Kumm. are the most abundant mushrooms in Ixtlán de Juárez, Oaxaca. Hypomyces lactifluorum (Schwein.) Tul. & Tul. has a minor index, probably because people have to scrape the ground to find it. Less-used mushrooms were Helvella crispa, Gymnopus dryophilus, and Lycoperdon marginatum Vittad.; the first is due to its low abundance, the second because only some people consider it as non-edible, and the third is due to the need of finding a considerable number of individual mushrooms to prepare a hearty meal. It is important to note that the frequency of use of determined species is determined by the access and the amount available.
Taste score appreciation index (TSAI). In general, all mushrooms were well accepted by people who consume them; Amanita basii was the most palatable species according to many informants as we could see with Alonso-Aguilar et al. [23]. In contrast, species of the genus Ramaria were the most appreciated according to Peña-Cañón and Enao-Mejía [26], and Gomphus clavatus (Pers.) Gray had the highest value of the overall species reported by Garibay-Orijel et al. [22]. Only few species were not appreciated, such as Harrya chromapes (Frost) Halling, Russula aff. lepida Fr., Suillus granulatus, and Xerocomus illudens (Peck) Singer, mainly because some Russula species have a spicy flavor, and some have a sour taste, such as the case of these boletes.
Multifunctional food index (MFFI). The main form of mushroom consumption was by roasting, only by cooking on a griddle (comal), with a little salt. Many people cook them with green sauce or “pasilla” chili sauce. The only mushrooms consumed alone were Amanita basii, Ustilago maydis, Boletus auripes Peck, and Hypomyces lactifluorum for being very palatable. Fistulinella wolfeana and Lactarius indigo can only be eaten roasted and have fewer larvae inside. Some people like to mix mushrooms, and the most frequent combination include Cantharellus cibarius Fr., Boletus variipes Peck, and Lactarius indigo, referring this as a very delicious combination. Calvatia cyathiformis (Bosc) Morgan and Agaricus campestris could also be consumed mixed together because they have a meat-like taste. Lycoperdon perlatum Pers. and L. marginatum were also consumed alone, as U. maydis in “quesadillas,” but the latter could be eaten mixed with squash blossoms. Ramaria spp. could be prepared alone too, and in many cases with eggs. Some mushrooms can be preserved for long periods, such as L. indigo and F. wolfeana, which are dried on rocks in the sun, or hanged on a chain, as reported by Estrada-Torres and Aroche [7]. Ramaria spp. is shredded into fine strands, and Hypomyces lacrifluorum is cut into thin slices and left in the sun, sometimes preserved frozen for up to 3 months. Our results on the MFFI are consistent with those of Garibay-Orijel et al. [22], Alonso-Aguilar et al. [23], and Peña-Cañón and Enao-Mejía [26] where we can see a close relationship with this sub-index and the TSAI sub-index, but in every case, the way of cooking varies.
Knowledge transmission index (KTI). Perhaps, this is the main index of the survey because it allowed to detect how traditional knowledge has been transferred from one generation to another. Méndez et al. [48] and Garibay-Orijel et al. [49] reported that women play a key role in transmitting and preserving knowledge because men were working out of town most of the time and only spend a few days at home. However, knowledge is diverse. We found that some people knew more than 30 different mushrooms, while some others only knew 3 species. In many cases, people refer to some species that were consumed by their parents or grandparents, but they do not eat them actually, which eventually represents the loss of this knowledge. Some younger people have not shown interest in learning the traditional uses of fungi. The ethnic group with the smaller ethnomycological knowledge was the mestizos, while Otomí people usually detected and use more fungi species in the area. Some species, such as Exudoporus frostii (J.L. Rusell) Vizzini, Simonini & Gelardi or Boletus cf. speciosus Frost, were considered poisonous by some informants, because they have blue spots (like other boletes that change color); however, a woman (and her family) who learned that E. frostii is edible, has shared that knowledge with their neighbors, situation previously observed by Garibay-Orijel et al. [22] and Peña-Cañón and Enao-Mejíar [26] too. For most species, knowledge can be traced for 50 years through two or three generations. It was also noted that discrimination plays an important role since some people argued that mushrooms are the “food of the poor.” As Burrola-Aguilar et al. [27] mentioned, in the case of fungi, many of the knowledge were lost because people migrated to national or international (mainly US) urban areas for better working conditions and the pursuit of economic improvements, resulting in trans-cultural and adoption of Western model over their culture and traditions [29].
Mushroom collection is commonly a family activity, in which people share and strengthen their family ties, and it is where children (from 5 to 10 years old) learn how to recognize edible and inedible mushrooms, and where mushrooms grow (main collection points). People have their techniques to recognize edible specimens from inedible ones, but it has been mentioned that some inedible species were similar to edible mushrooms. People commonly collect only red Russula species, which do not have a spicy taste, or Ramaria that have a mild flavor. Regarding the names of the mushrooms, most of them are similar to those reported elsewhere and are consistent with recent studies in Otomí areas [25,26,27,28,29].
Health Index (HI). People indicate that when they eat mushrooms, they cannot drink milk or alcohol, eat avocado, or consume medicine because they have side effects. Only Russula aff. lepida and Suillus granulatus were consumed with caution. The “skin hat” is commonly removed because it is considered as the main factor causing diarrhea or stomach pain. Xecomus illudens and Harrya chromapes are reported to have a sour taste but without consequences. Besides, only some people mentioned feeling healthier by eating mushrooms in general [22], and not only with the consumption of some species, they generally refer to assimilating minerals from the soil through eating mushrooms. It is important to not confuse these with the medicinal proprieties of used fungi, and finally, they think that mushrooms are better than meat or vegetables because they consider mushrooms as a natural product that does not have chemicals as Alonso-Aguilar et al. [23] reported.
Economic Index (EI). Amanita basii has the highest price ($60–$80 Mexican pesos per four basidiomata), but only a few people sell it. A 15 l bucket full of Fistulinella wolfeana was priced at $35. Other species, such as Lactarius indigo, Ramaria spp., Leccinum aff. aurantiacum (Bull.) Gray, Hypomyces lactifluorum, Boletus variipes, B. auripes, Agaricus campestris, Calvatia cyathiformis, Cantharellus cibarius, and Armillaria mellea (Vahl) P. Kumm. have a lower value, between $15 and $50 for about ten basidiomata. Calvatia cyathiformis is priced at $70, and A. campestris costs $50, but this can only be collected on plains at the beginning of the rainy season. To compare prices, at Acambay market (State of México), fungi prices range from $40 to $80 per 200 to 400 g for species like B. variipes and A. caesarea (Scop.) Pers. complex, while in the municipal market of Amealco (Querétaro), a plate of mushrooms, which contains about 100 g of C. cibarius and Ramaria spp. has a price of about $20 or 200 g for $35. Many respondents either have a store, work as laborers, have a piece of land to grow corn, or have relatives who send them money to help cover expenses, thus collecting mushrooms is not their main economic source. Only some people trade mushrooms for basic supplies like corn seeds, oil, beans, rise, etc. Until now, there is no consensus about this sub-index because it is in function of almost all the sub-indexes that compound the EMCSI and could be disregarded [23]. In this case, even with economic potential [22], people prefer to consume the mushrooms over selling them.
The information obtained in the three communities and the value of the indexes and total EMCSI are shown in Table 3. The three main mushrooms were L. indigo (63.24), A. basii (61.95), and F. wolfeana (61.23). It is probably because L. indigo and F. wolfeana are available after the rainy season, which gives them a high value, even over A. basii. Some people consume them for up to 1 year after they have been collected; they put dry basidiomata in hot water and then cook them. This contrasts with QI and PAI values, where A. basii had a higher value in the QI and a lower value in the PAI, compared to L. indigo and F. wolfeana. In many cases, before we start talking about mushrooms, people mention A. basii immediately, so we might consider these three species with similar ethnomycological importance values, and this matches with the results of other studies [22, 23], where A. caesarea complex are the most priced mushrooms, although it is possible to find other more valuable species in other places [12, 16, 28].
Uses
Edibility was the main use found for mushrooms. Almost all respondents mentioned that they consume fungi, only three people said they quitted eating them or using them for reasons discussed below. Regarding medicinal use, only three people mentioned Ustilago maydis as a remedy for burns and to combat vomiting. Mature basidiocarps are used by placing them directly on burn injuries, where informants argue a faster healing. This coincides with reports from other cultures that use U. maydis as a remedy for burns [28]. Other informants report that people use this species as a remedy when horses do not want to drink water, so they give them the mushroom in a solution of water with spores, and the horses drink water again. This might be the first veterinary report for mushrooms, and therefore, further research on this aspect is necessary.
Some informants mentioned the use of E. frostii to control diabetes. Basidiomes of Leccinum spp., which are not consumed, are used by some people as toys during harvest time, throwing these ones to others as a game. Mushrooms that they do not consume are considered poisonous, even if others eat them. A recent record of mushroom poisoning occurred in a community near Amealco, where four people confused the Omphalotus mexicanus Guzmán & V. Mora with a Lactarius indigo, and the symptoms consisted mainly of vomit and diarrhea; they were treated at the health center only with activated carbon and antihistamines, and people mentioned that one woman and her daughter died about 10 years ago due to the consumption of poisonous mushrooms; however, they do not know which species. According to Peña-Cañón and Enao-Mejíar [26], people only eat species they are sure to know.
People harvest mushrooms provided by the forest as part of the natural resources available during the rainy season. On the other hand, many of them used to grow vegetables a couple of months before the rainy season began, so they could get benefits from mushroom collection, by adding diversity and enrichment of the daily diet and helping them to save money. Mushroom recollection was restricted mainly to August and September, the months where we conducted the ethnographic work and where we found most of the species. All mushrooms have a utilitarian category [50]. We suspect in this particular study that they do not have a hierarchical category as Berlin [51] proposed for plants and animals because informants usually just named and used mushrooms related to their daily use, such as Russula spp. which is called “Hongo de Borrego (a)” (lamb mushroom), because when people take their animals out to the pasture, lambs eat these mushrooms. C. cibarius is called “Pericón” or “Santa María” due to the similar yellow color with Tagetes lucida Cav. Other example included L. indigo, which has names related with its bright blue color “pant mushroom,” because the blue color is a reminder of a pair of blue jeans. As mentioned, people only named mainly edible mushrooms and considered the remaining non-used as venomous. It is interesting how they recognize the good ones, and this knowledge is transmitted generationally mainly by women, being the principal characteristics color, smell, maturity, and in some cases, the taste (they avoid spicy and bitter flavors). Alonso-Aguilar et al. [23] found A. basii, among other mushrooms, is the most appreciated species. In the present work, we found F. wolfeana, L. indigo, Ramaria spp., and B. variipes (species close to B. pinophilus Pilát & Dermek) as having the highest values of EMCSI, and the species had highest sub-indexes values. These values are in function of the QI sub-index because not all the interviewed people mentioned other species with significant abundances, such as Russula aff. brevipes, E. frostii, Lyophyllum sp., G. dryophilus, A. novinupta, or H. crispa, which were mentioned by less than 20% of the interviewed people. In this case, those positions in the EMCSI value are relative to the mentioned above and could be modified along the time by the factors mentioned in KTI sub-index discussion.
Finally, we have noted that some people begin to get upset with the intervention of people who do not belong to their community; for this reason, it is important to consider as necessary a previous diagnose, and then get previous consent, considering and giving all the people the opportunity to participate and being interviewed, as observed by Garibay-Orijel et al. [22], and according to Ford [52], it is necessary to recognize them as authors of any work that involves traditional knowledge, not only on mushrooms. On the other hand, most of the people do not have any problem with sharing their knowledge, and in some cases, we developed a friendly relationship that persists even after the work has been finalized.
Cluster of similarities
The dendrogram of similarities (Fig. 2) with the standardized Euclidean distances (SED) linkage of 7.15 shows that the biggest group (A) is composed by L. indigo, Ramaria spp., F. wolfeana, A. basii, B. variipes, B. cf. speciosus, C. cyathiformis, U. maydis, C. cibarius, L. aff. aurantiacum, H. lactifluorum, A. mellea, and Clitocybe gibba (Pers.) P. Kumm., and includes B. auripes and C. cibarius. U. maydis has no EI value but has a high TSAI value because it is one of the most palatable mushrooms. In this group, the closer species were B. cf. speciosus and C. cyathiformis (with a linkage SED = 0.65). The second group (B) is formed by Retiboletus aff. griseus (Frost) Manfr., Leccinum sp., H. chromapes, X. illudens, Leccinum rugosiceps (Peck) Singer, A. novinupta, S. granulatus, R. aff. lepida, Boletus sp., R. aff. brevipes, and E. frostii, species that show medium to low QI values; and the third group (C) is composed of R. aff. cyanoxantha, L. marginatum, L. perlatum, Nolanea (Fr.) P. Kumm., Lyophyllum sp., G. dryophilus, and H. crispa, the last is the one with the lowest EMCSI value. This group had a linkage SED of 3.96.
Multidimensional scaling and principal components analysis
An analysis of the stress in the MDS suggested a 3D configuration (mean = 3.859 and P = 0.0196). According to the cluster shown in Fig. 2, mushrooms appear in three main groups A, B, and C (Fig. 3). In this case, we can see a slight difference in the species that conform all groups. The six main mushrooms (and at least the majority of the rest of the species that conform this group) are contained in group A, while the species from groups B and C appear mismatched. These results are supported by the PCA (Fig. 4). The first three principal components explain the 70.93% of the variance. PC1 variables were FUI (0.538), PAI (0.476), and QI (0.474; PC2 variables were TSAI (0.551) and KTI (0.489); and PC3 variables were HI (0.497) and MFFI (− 0.477). We only consider PC1 and PC2 because they are strongly related; frequency of use of spi is directly related to the abundance of spi, and this is influenced by the number of mentions of spi, as we can see in PCA. The last components, which conform PC3, have both positive and negative values, which makes sense due to only a few species that cause stomach ache, such as Suillus spp. or red spicy cap Russula spp., but these species are considerably abundant.
These results make sense if we consider the history behind those species; in all cases, people know them due to their families, which mean that these species have been used for almost three consecutive generations. The relation in PC2 variables is in function of the tradition of consuming the preferred species over the fewer accustomed ones by the main transmitters of knowledge; new collectors learn how to recognize all of them, but making emphasis on the preferred species. This contrasts with the PC1 components since the preference over a specific mushroom depends on its frequency of use and the abundance.
Figure 4 shows the similarities between species related, as a result of the values of every sub-index. This has a similar tendency to MDS analysis and PCA for sub-indexes (Fig. 5), wherein both cases, main species are affected by variables of the PC1 and PC2.
Alonso et al. [14] reported a similar tendency in their results, observing the same six main species we found in a similar environment, and as observed by Garibay-Orijel et al. [22], these mushrooms could be found on forest mainly composed of Quercus too, but with different values as we see in this survey. Although, it might be a tendency in temperate zones with their main species [16, 22, 23]. In this case, human communities are very close to the forest, so people can easily collect mushrooms and use them as a food source, which is the main use category. Agaricus campestris, C. cyathiformis, and U. maydis are out of the forest but have an important role, where the first two species are the first available in the season, and the last one depends on corn planting. Lactarius indigo, A. basii, and F. wolfeana are the main species found in this survey, among 33 different mushrooms. Although kids participate in mushroom harvesting, many of them do not like mushrooms. Bautista [29] refers the preference of new tendencies, so that means erosion in the ethnomycological knowledge; the situation also observed in the Hñähñu (Otomí) language. On the other hand, people refer that forest does not have the same shape they remember, and many of them mentioned that the amount of mushrooms has decreased because of environmental degradation and deforestation.