RESEARCH ARTICLE

Ethnobiology and Conservation 2019, 8:7 (21 June 2019) doi:10.15451/ec2019-06-8.07-1-31 ISSN 2238­4782 ethnobioconservation.com Knowledge and use of biocultural diversity by Nahua in the Huasteca region of Hidalgo, Mexico

Tania Vianney Gutiérrez­Santillán1, Ángel Moreno­Fuentes2, Arturo Sánchez­González2 and Gerardo Sánchez­Rojas2*

ABSTRACT

In the Huasteca region, high biological diversity and diverse ethnic groups converge. The implementation of metrics for biocultural diversity was developed based on metrics used in analyzes of biological diversity. We compared the results of the diversity known and used by two communities of Nahuatl origin established in two types of vegetation (Tropical Semi Evergreen Forest [TSEF] and Mountain Cloud Forest [MCF]). The fieldwork was carried out from January 2011 to December 2012; the ethnobiological information was collected combining the methods: percentual and snowball, additional applying as an ethnographic tool: multiple free lists and semi­structured interviews to 125 informants. The ethnobiological information was analyzed by adapting indexes used in the evaluation of biological diversity and multivariate methods. The informants identified 409 ethnospecies for both communities, although they only correspond to 383 biological species, the several taxonomic groups. The TSEF presents a greater richness of species­ethnospecies concerning the MCF. Eleven categories of use were identified, with the edible category being the most mentioned. In general, local people have extensive knowledge of the biological diversity present in their territory, and there are distinct differences in knowledge between communities established in different . However, there is much similarity in knowledge and use of , since both populations belong to the same cultural group. We believe that our results show the relevance of using the metrics used in the evaluation of biocultural diversity.

Keywords: Index of Biodiversity; Multitaxonomic;

1 Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas, Av. División del Golfo #356. Col. Libertad. C.P: 87020, Ciudad Victoria Tamaulipas, México.

2 Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Apartado Postal 1­69, Plaza Juárez, C.P. 42001, Pachuca Hidalgo, México.

* Corresponding author. E­mail address: TVGS ([email protected]), AMF ([email protected]), ASG ([email protected]), GSR ([email protected])

INTRODUCTION mostly populate greatest biodiversity areas, this correlation is conceptualized as A spatial co­occurrence among biological, biocultural diversity (Maffi 2001; 2005; 2007; ecological, environmental, geographical, Loh and Harmon 2005; Harmon and Loh linguistic and cultural components can be 2010; Stepp et al. 2004; 2005). This observed around the world; this co­ biocultural diversity establishes unique occurrence show that indigenous groups social­ecological relationships (Pretty et al. 1 Gutiérrez­Santillán et al. 2019. Knowledge and use of biocultural diversity by Nahua in the Huasteca region of Hidalgo, Mexico Ethnobio Conserv 8:7

2009); since it is recognized that each loss of both diversities (Sutherland 2003). indigenous group appropriates the The importance of maintaining the balance biodiversity present in their territories (Boege between nature­culture and how to sustain it 2008; Toledo 2010). is related to the proper development of Although biocultural diversity is future projects (Maffi and Woodley 2008), recognized, there are semantic and the use of natural resources as a way of conceptual gaps in the definition, additionally connecting with nature (Grasser et al. 2012), it has been seen that biological diversity and the conservation of biocultural diversity as a biocultural diversity are not entirely goal (Hong 2013) and even as a response to congruent in terms of the factors that the challenges faced by large cities (Elands generate them (Cardillo et al. 2015). A et al. 2018). concept of biocultural diversity should be Biocultural diversity should be used when based on more than merely the sum of its designing priorities in conservation (Dunn components. For this reason, we 2008), and social­ecological research should contextualize biocultural diversity as “the be the link between human and natural variety of organisms that are known, named, aspects (Gavin et al. 2015; Saslis­ classified, organized, used, exploited, Lagoudakis and Clarke 2013); integrating domesticated and/or manipulated by the new biocultural perspective into different human societies; including the conservation biology (Gavin et al. 2015; social­ecological systems of which this Gorenflo et al. 2012; Huntington 2013; diversity forms a part at various Luque and Doode 2010; Saslis­Lagoudakis spatiotemporal scales (Gutiérrez­Santillan and Clarke 2013; Wolverton et al. 2014). 2018). This is supported by successful conservation This conceptualization requires us to programs that integrate traditional define the units that make up biocultural knowledge and local practices (Huntington diversity, which are called ethnospecies. An 2013; Maffi and Dilts 2014). ethnospecies corresponds to a biological Mexico is one of the countries with high species and its cultural identity. biological diversity (Neyra­González and Indispensable attributes of an ethnospecies Durand­Smith 1998), as well as cultural are the combination of the taxa itself diversity (De Ávila 2008), which makes it one (species or genus but not any higher of the most propitious countries for category) with the cultural identity associated ethnobiological research, from different with the traditional unique name for that taxa approaches and themes, for example, the as the cognitive basis for the recognition of traditional classification (Berlin 1973; Berlin the organism by human groups (Hunn 2011). et al. 1973; Hunn 1998; 2008; Alcántara­ Assessing the richness and diversity Salinas et al. 2013), the evaluation of known and exploited by human groups, that cultural importance (Garibay­Orijel et al. is, biocultural diversity, helps us to 2007). ), the domestication of plants (Bye understand the degree of correlation with and Linares 1983), among many other biodiversity and thus to evaluate other examples. However, few studies associated phenomena; for example; comprehensively address the traditional understand the spatial congruence between knowledge of different taxonomic groups species richness and cultural evolution (Aldasoro­Maya 2012; Argueta­Villamar (Turvey and Pettorelli 2014) as well as the 2008; Cano 1988; Hunn 1998, 2008).

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Because in general ethnobiological works Considering that the Huasteca region is have been developed by defined rich in biodiversity and has the presence of subdisciplines (ethnobotany, ethnomycology, one of the most representative ethnic groups and ethnozoology). in Mexico the Nahuas, the work is The Huasteca is a region located in approached as a case study on conceptual central­eastern Mexico, where the territories and methodological aspects of cultural of several indigenous peoples converge. It is diversity. We proposed the use of the most characterized by high biological diversity current metrics for the analysis of biological (Olivier 2008; Ruvalcaba et al. 2004), biodiversity, to propose it as a new approach associated to many different geographic and to the measurement of biocultural diversity. environmental condition. Various The l study was designed with the following ethnobiological studies have been carried objectives: 1) to identify the ethnospecies of out in this region, focusing mainly on plants, fungi, and animals that the local ethnobotany of the Teneek (Alcorn 1981a; people know and use, in order to document 1981b; 1983; 1984), Nahuas (Andrade­Cetto their degree of knowledge about local 2009; Hernández 2003), Pames (Carbajal­ biodiversity; 2) to compare ethnospecies Esquivel et al. 2012; Torres et al. 2015), richness between the different vegetation Tepehuas (Álvarez 2002; López­Villafranco types, in order to find out whether traditional and Aguilar­Contreras 2010) and Totonacos knowledge is similar within a given cultural (Cano 1988). A number of studies have group or whether it may differ between examined the importance of the social­ different ecosystems; 3) to analyze the ecological relationship in terms of ethnospecies detected in the study by magical/religious aspects (Montoya 1968; means of diversity indexes as an evaluation Gallardo­Arias 2004; Piotrowska 2013a; metric for use in biocultural diversity studies; 2013b), traditional medicine (Andrade­Cetto 4) to evaluate the degree of correlation 2009) and the use of edible fungi (Bautista­ between taxonomic species and Nava 2007; Isidoro­Reséndiz 2011). ethnospecies, in order to find the degree of The few ethnozoological studies in the culturally recognized biodiversity; and 5) to region have documented knowledge, identify use categories, in order to find the perception, classification and, zootherapy. association between taxonomic groups and The vertebrate groups studied were fish use categories. (Montaño et al. 2010; González et al. 2010), We expected to contribute to the subject reptiles (Penguilly et al. 2010) and birds of biocultural diversity by establishing (Jaimes et al. 2014). Additionally, research in ethnospecies as social­ecological units of the Huasteca region has integrated study and their evaluation by using the most ethnobiological data for multiple taxonomic recent biodiversity metrics (Moreno et al. groups; for example, in Hidalgo (Gutiérrez­ 2017); The study was carried out in two Santillán 2013; Hernández and Bautista Nahua communities established in different 2011), in Puebla (López del Toro et al. types of vegetation in the Huasteca region in 2009), in San Luis Potosí (Alonso­Castro et the state of Hidalgo, Mexico. al. 2011) and Veracruz (Cano 1988), which has contributed to recognition of the biocultural diversity of the region.

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MATERIAL AND METHODS 98°43'26.58" – 98°43'13.90" W; 140 masl; vegetation type TSEF, annual temperature: Study area 18°C to 25°C, annual precipitation: 1600–1900 mm; with a populations of 380 The Huasteca is a region located in inhabitants (INEGI 2010). In this community, central­eastern Mexico that includes portions the main activity is agriculture, to lesser of the states of Hidalgo, Puebla, Querétaro, extent livestock and fishing as a recreational San Luis Potosí, Veracruz and Tamaulipas. activity. Some informants mentioned working The majority of the inhabitants of the in the citrus groves near the community; Huasteca region are mestizos, but a number Figure 1); b) Tlamamala, in the municipality of native peoples share the territory; of Huazalingo (20°58'15.27" – 20°58'0.64" N Nahuas, Huastecos, Pames, Otomíes, and 98°32'40.45" – 98°32'21.34", 960 masl, Tepehuas and Totonacos (Olivier 2008). vegetation type MCF, annual temperature: The present study involves Nahuas, as 13°C to 21°C, annual precipitation they are one of the most numerous 1500–2800 mm; with a population of 750 indigenous peoples and among the most inhabitants (INEGI 2010; Figure 1). The widely distributed in Mexico. In the main activity is family farming, coffee harvest Huasteca, Nahuas live in more than 50 (coffee under shade) and livestock. Some of municipalities (county equivalents) in the the informants mentioned working in the states of Hidalgo, San Luis Potosí, and nearby city of Huejutla de Reyes, Hidalgo Veracruz (INALI 2008). In the state of (approximately 40 km), and even in other Hidalgo, they live in 13 municipalities in the cities of the country. northeast as well as a small group in the southwest (Báez et al. 2012). The Huasteca Fieldwork part of Hidalgo state mainly contains two types of vegetation; tropical semi­evergreen Before fieldwork commenced, the study forest (TSEF) and montane cloud forest proposal was submitted to local authorities (MCF), the TSEF covering more area than and approved by a community assembly the MCF (Puig 1991). In addition, there are (International Society of Ethnobiology 2006; extensive areas of farmland, both crop and http://ethnobiology.net/code­of­ethics/). At livestock. The main crops are corn, coffee, each interview, consent was obtained from beans, sugar cane and oranges (Barthas the informant, including consent for 1996). photography and participant observation The study areas were selected using the (Albuquerque et al. 2014). The field research criteria 1) ethnic identity, 2) more than 80% was carried out during a two­year period indigenous speakers, and 3) low from January 2011 to December 2012, with disturbance of the vegetative cover. This a total of 20 visits to each of the two approach allows a selection of study sites locations. associated conditions of research interest Ethnobiological data were obtained by and not a priori selection assigned by the combining the ethnographic percentage investigator (Gutiérrez­Santillan et al. method (10% of the population; Bernard 2019a). Two communities were selected: a) 2006) and the snowball technique (Brewer El Barco, in the municipality of Lolotla 1995; 2002; Trotter et al. 2001). The (21°10'45.33" – 21°10'32.89" N, combination of both methods allowed us to

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Figure 1. Location of study sites. The red zone on the left represents the Huasteca portion of the state of Hidalgo, Mexico. The triangle shows the location of El Barco (TSEF = tropical semi­evergreen forest, 140 masl) and the star shows the location of Tlamamala (MCF = montane cloud forest, 960 masl). work with an ethnographic sample 62% men, with ages between 20 and 84 determined by chance, having informants in years, and 88% are speakers of the general and not only expert informants. indigenous language. During the development of the interviews in Ethnographic tools were also used by many of the cases, the same informant was combining: multiple free listings (Brewer interviewed several times. Also, it should be 1995; 2002) and semi­structured interviews noted that no additional ethnographic data (Bernard 2006; Albuquerque et al. 2014). were obtained; only sex, age and yes, his First, informants were asked about plants, mother tongue was Nahuatl. fungi, and animals are known in the area A total, 125 interview combinations were (multiple free listing in Spanish and Nahuatl); applied; a) 50 informants in the town of El Later using the semi­structured interview, the Barco of whom 50% were women and 50% use of the referred ethnospecies was asked. men, with age between 21 and 72 years and The interview data organized in databases, 94% are speakers of the indigenous for a) plants, b) and c fungi) animals, is language. B) 75 informants in the locality of organized by last taxonomic group (fish, Tlamamala of which 38% were women and amphibians/reptiles, birds and mammals).

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Each database consisted of several sets of association of the species (identified by us) information: a) information the informant concerning published regional taxonomic (name, gender, age, indigenous language lists. speakers), b) taxonomic data (order, family, Species were identified to the lowest genus, species), c) nomenclature traditional possible taxonomic level, based on the (name in Nahuatl and Spanish) and d) respective literature for the group; fungi category of use. (Bautista­Nava 2007; Isidoro­Reséndiz 2011), plants (Andrade­Cetto 2009; Luna et Collection, processing and al. 1994; Pennington and Sarukhán 2005; identification of ethnobiological Pérez­Escandón et al. 2003; Puig 1991; material Villavicencio 2005; Villaseñor 2016), crustaceans (Álvarez et al. 2012), mollusks The biological material was processed (Correa­Sandoval 2003), millipedes (Bueno and identified according to the taxonomic 2012) and vertebrates (fish: González et al. group in general; they had a) collections of 2010; Miller 2009; amphibians and reptiles: fungi and plant specimens were collected in Ramírez­Bautista et al. 2014; birds: Howell the field during the trips with the inhabitants and Webb 1995; Peterson and Chalif 2000; to their daily activities (participative Martínez­Morales 2007; Martínez­Morales et observation; Bernard 2006). The collections al. 2007; and mammals: Ceballos and Oliva were processed and dehydrated adequately, 2005). later in the laboratory they were identified In addition, lists of species reported for with the use of taxonomic keys. Fungal the respective taxonomic groups in the specimens are deposited in the collection Huasteca Hidalguense were used (Ramírez­ ethnomycology "Dr. Teófilo Herrera Suárez” Bautista et al. 2017). In the MCF, 336 at the Center for Biological Research, the species of plants have been recorded (Luna Autonomous University of the State of et al. 1994), 181 bird species (Martínez­ Hidalgo, Mexico. The deposit of the plants Morales 2007), 34 mammal species was not possible in an official collection (Mejenes­López 2008; Mejenes­López et al. because you do not have an herbarium of 2010), 73 amphibian and reptile species ethnobotany. (Ramírez­Bautista et al. 2014), and 22 For different groups of animals fieldwork species of fish (González­Rodríguez et al. was based primarily on: b) animals or parts 2010). For the TSEF, 274 species of plants of animals donated by the informants; c) have been recorded (Puig 1991; photographs of animals or parts of animals; Villavicencio 2005; Villaseñor 2016), 173 d) visual stimuli – pictures based on the bird species (Martínez­Morales et al. 2007), design of posters of species already 35 mammal species (Mejenes­López 2008; reported in the region (Bernard 2006; Mejenes­López et al. 2010), 32 amphibian Albuquerque et al. 2014), and e) field and reptile species (Ramírez­Bautista et al. guides, e.g., birding guides (Albuquerque et 2014) and 28 species of fish (González­ al. 2014). In general, for all taxonomic Rodríguez et al. 2010). groups, it has been made f) traditional The categories of use were established nomenclature associated (documented by through the use reported by informant (emic us) with bibliographic ethnobiological categories for region) additionally other information for the region; and g) the proposals in the literature were consulted

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(Farfán et al. 2007; Lira et al. 2009; Monroy­ considering each interviewee as a sampling Vilchis et al. 2008). Eleven categories were unit. An assumption of these nonparametric identified: ceremonial, fuel, edible, estimators is that the probability of capture – construction, timber, pets, medicinal, here the probability that an ethnospecies is ornamental, commercial/sale, agricultural mentioned – must remain constant use and other (which contained any other throughout the period of ethnographic uses which were mentioned only once in the sampling. interviews). The analysis of biocultural diversity was calculated based on the diversity formula Data analysis proposed by Jost (2006), which is known as a zero­order and first­order measure of The inventory of biocultural diversity was diversity (Hill 1973), using the formula: measured by means of indexes adapted from metrics used to analyze biological diversity. To determine whether the number of selected informants was sufficient to obtain a complete inventory of known and exploited diversity (frequency of mention, where pi is the abundance of species i FM), an accumulation curve was plotted divided by the total sum of the abundances using the non­parametric first­order Chao of the S (species), and the exponent q is the index (Chao1), calculated by means of the order of diversity. The order of diversity (q) is Estimates 8.0 program (Corwell et al. 2004). influenced by the relative abundance of the The Chao1 estimator is a method that uses species in the index; that is, the abundance data and is based on the number predominance of common species or of rare of species that occur only once or in one species. In the present case, the relative sample and the number of species that abundance values in the ecological occur exactly twice or in two samples inventories are replaced by the values (Escalante 2003). obtained for the FM of the reported In this case, the abundance data of the ethnospecies. species in a sample was replaced by FM Zero­order (0D) and first­order (1D) data; that is, the number of times a species i diversity values were calculated. Zero­order is mentioned in a sample (Pineda and Verdú diversity (0D) is based on the number of 2013). An approximation of the expected incidences of the species in the sample, number of ethnospecies was calculated, to which is equivalent to species richness, or in estimate whether the number of interviewees our case ethnospecies richness. In first­ (sampling effort) was sufficient for a order diversity (1D), all the species in a complete inventory. Nonparametric sample are aggregated with a value exactly estimators have their statistical basis in proportional to their relative abundance, techniques for estimating the number of without overvaluing the rare or common classes from samples and species (Hill 1973; Jost 2006; Moreno et al. capture–recapture techniques (Chao and 2011; Moreno et al. 2017). First­order Lee 1992; Jiménez­Valverde 2003). In the diversity (1D) can be interpreted as the present case, this corresponds to number of effective species, these being informants–mentioned ethnospecies, understood as units corresponding to the

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numbers of species with the abundances RESULTS that would theoretically coexist in a community with maximum equality (Moreno Analysis of Biocultural Diversity et al. 2017). Using this index facilitates comparing the numbers of species between A total of 408 ethnospecies that integrate communities and quantifying the differences the biocultural diversity recognized by the between them (Hill 1973; Jost 2006; Moreno Nahuas of the Huasteca region in the state et al. 2011). of Hidalgo were recorded. These correspond To compare the sites in terms of to 383 species distributed in 343 genera ethnospecies composition, the Sørensen belonging to 160 families (Supplementary similarity index (I ) was used. The degree of s Material). The biological groups recorded association between the species recorded in overall were plants (59%), birds (16%), the literature for the region (independent mammals (9%), fish (8%), amphibians and variable) and the ethnospecies reported in reptiles (5%), fungi (3%), and invertebrates this study (response variable) was tested by (molluscs, crustaceans and millipedes >1%). linear correlation using the Past 3.20 The biological group with the most recorded program (Hammer et al. 2001). taxonomic families was plants (58%), In order to describe the association followed by birds (16%) and mammals (9%) between use categories and biological (Table 1). In addition, 342 ethnospecies were groups, a correspondence analysis (CA) was mentioned in some use category; 304 carried out in the Statistica program species used in the TSEF and 290 species (StatSoft 2004). A data matrix was created, used in the MCF, a difference of 14. where the variables correspond to biological The ethnospecies accumulation curves groups and the cases to use categories. The for the TSEF showed that 82% of the 2 chi­square statistic (X ) and the percentage expected ethnospecies were represented of variation explained between the first and (Chao1 = 291), and for the MCF, 79% were second dimensions were calculated.

Table 1. Species–ethnospecies data for biological groups listed by inhabitants of two Nahua communities in the state of Hidalgo, Mexico. There was a strong relationship overall between the species and their cultural counterparts (ethnospecies); however, in the case of invertebrates, taxonomic identification was only made to the level of gender and family. TSEF = tropical semi­ evergreen, MCF = montane cloud forest.

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represented (Chao1 = 275). In both cases, different vegetation types. The Sørensen the actual ethnographic sampling effort similarity between the TSEF and the MCF (number of interviews) is located in the was 84%, indicating that a large percentage asymptote of the curve, which suggests that of ethnospecies are shared between the two the inventory of known and used biodiversity sites. In addition, a positive correlation was was very few interviews short of a complete found between the number of species inventory (Figure 2). reported in the literature for the different For the TSEF, zero­order diversity (0D) taxonomic groups and the number of was 355 ethnospecies (invertebrates 2, fish ethnospecies documented in the present 24, amphibians and reptiles 22, birds 57, study (r= 0.8424, p= 0.0037). This indicates mammals 31, fungi 12 and plants 207) and that most species have their cultural first­order diversity (1D) was 234.2 counterpart and that much of the knowledge ethnospecies (invertebrates 1.9, fish 21.5, about biodiversity is shared, independently amphibians and reptiles 19.9, birds 44.7, of vegetation type, a phenomenon mammals 23.7, fungi 9.9 and plants 136.7). associated with the cultural origin of the For the MCF, the 0D was 308 ethnospecies human group and the fact that both (invertebrates 2, fish 8, amphibians and communities are in the same geographical reptiles 13, birds 44, mammals 34, fungi 8 region. and plants 199) and 1D was 202.3 ethnospecies (invertebrates 1.8, fish 6, Use Trends amphibians and reptiles 8.6, birds 31, mammals 23.5, fungi 5.8 and plants 131). A total of 11 use categories were The observed difference between the TSEF identified for both communities. The and the MCF was 47 ethnospecies for 0D categories containing the highest number of and 31.95 ethnospecies for 1D (Figure 3). ethnospecies are commercial trade or sale We found a similar composition of known (28.7%), edible uses (17.5%) and medicinal and used ethnospecies in the two Nahua uses (14.1%); followed by the categories communities even though they are in with moderate values: ornamental (11.1%),

Figure 2. Accumulation ethnospecies curve based on the number of interviews and the non­ parametric Chao first­order accumulation function (Chao1). On the x­axis, the number of informants is shown by community, while the y­axis shows the cumulative number of mentioned species (FM). The bars at each point represent the 95% confidence interval. TSEF = tropical semi­evergreen, MCF = montane cloud forest.

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Figure 3. Diversity values of order zero (0D) and first order (1D) by vegetation type. To graph the values, the Shannon index was used in both levels of diversity. The data were the number of ethnospecies by biological group for zero­order diversity and the inverse of the Shannon index for first­order diversity. This procedure enabled the confidence intervals to be obtained. TSEF = tropical semi­evergreen, MCF = montane cloud forest. fuel (6.3%) and pets (5.3%). The categories We can observe in the graph (Figure 4) with the lowest values are ceremonial and that certain categories of use are exclusive construction with 4.5% each, timber (2.0%) of certain biological groups. For example, and agricultural use (1.8%). Four of the the categories of agricultural uses, fuel, categories (fuel, construction, timber, construction, and wood are exclusive to the agricultural use) only contained plant plants; while the pet category with birds, species, and the pet category was exclusive mammals and reptiles. In turn, birds and to animals, mainly birds and mammals mammals are more related to ornamental (Table 2). use and as pets, while reptiles with The correspondence analysis (CA) ceremonial uses. Some generic categories showed the association between biological are more associated with vertebrates than groups and anthropocentric categories, with plants (e.g., ornamental and including ethnospecies that are used in ceremonial), or, for example, the edible different ways in the two communities. There category (which should be generic) has a is a significant relationship between more significant relationship for fungi and biological group and use category (x2= fish; this is due to the fact that the 537.35, df= 50, p <0.05). The two ethnospecies that form these two biological dimensions explain 81% of the variation in groups generally only fulfill alimentary the data. In the first dimension, plants functions (Figure 4). The association of the contribute the most to the variance biological groups and the categories of use, (eigenvalue= −0.4621), followed by birds in this case, is given by the frequency of (eigenvalue= 0.2648) and mammals mention of each one of the ethnospecies for (eigenvalue= 0.1520). In the second each one of the categories; so, the dimension, the main contributions to the relationship shown in the chart (Figure 4) is variance are from fish (eigenvalue= specific for these two study communities. −0.1816), fungi (eigenvalue= −0.0570) and amphibians and reptiles (eigenvalue= 0.0330).

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Table 2. Relationship between number of ethnospecies mentioned and categories of use. Plants are the group with greatest diversity of categories, invertebrates and fish are the group with the least.

Legend: Relationship between number of ethnospecies mentioned and categories of use. Plants are the group with greatest diversity of categories, invertebrates and fish are the group with the least.

Figure 4. The correspondence analysis shows the association between the biological groups; mammals, birds, reptiles, fish, fungi and plants, with respect to the use categories: I= construction, II= timber, III= agricultural use, IV= fuel, V= sale or commercial trade, VI= others, VII= ceremonial, VIII= ornamental, IX= medicinal, X= pets, and XI= edible. In some cases, a specific relationship is observed between biological groups and certain categories; for example, fish and fungi are associated with the edible category because fungi are normally only harvested for food, and fish can only be sold sometimes, so their main use is as food. In contrast, mammals, birds and reptiles are mostly related to ceremonial, medicinal, ornamental and pet uses, while plants are associated with uses such as timber, agriculture, construction, fuel and commercial use. 11 Gutiérrez­Santillán et al. 2019. Knowledge and use of biocultural diversity by Nahua in the Huasteca region of Hidalgo, Mexico Ethnobio Conserv 8:7

DISCUSSION reasons such as lack of availability of time, funding, access to communities, or lack of Biocultural diversity of the Nahua transdisciplinarity, among others. It is more common to find multitaxonomic research The Nahuas of the Huasteca region in addressing two or three biological groups Hidalgo state have extensive knowledge (Nabhan et al. 1982; Caballero and Mapes about the biodiversity in their environment. In 1985; Farfán et al. 2007). this study, 408 ethnospecies were reported. On the other hand, regarding the They are associated with 383 species knowledge and use of biocultural diversity, a belonging to a variety of biological groups high similarity is determined even though the (invertebrates, amphibians and reptiles, fish, communities are established in two different birds, mammals, fungi and plants). This is a types of vegetation (TSEF and MCF). The higher number of ethnospecies than were similitude may be given because they share found by other comparable ethnobiological common species, which are generally widely studies (Caballero and Mapes 1985; Farfán distributed or introduced. It also suggests et al. 2007; Nabhan et al. 1982). Other that this phenomenon is associated with the studies have generally not addressed all cultural memory or bio­cultural patrimony of three main ethnobiological subdisciplines; both communities, as it belongs to the same ethnomycology, ethnobotany and indigenous group (Olivier 2008), as well as ethnozoology. Our research is a contribution geographic proximity (see map). So, when from a comprehensive ethnobiology studying two types of dominant vegetation in perspective, combining the three the Huasteca region (Puig 1999), it is likely subdisciplines integrating various biological that the social­ecological relationships for groups and evaluating social­ecological the Nahuas are similar. biodiversity knowledge held by a specific The biocultural diversity reported here indigenous group. In addition, this study indicates a high degree of recognition and contributes to the analysis of biocultural use of the natural environment in diversity by treating ethnospecies as units of communities where the traditional language analysis, as has been done in and many of the customs are still preserved. (Moreno 2011; Moreno et al. 2017) and This is confirmed by the significant positive shows how metrics used in the analysis of correlation between the number of biological diversity can be adapted to the ethnospecies and the number of species analysis of biocultural diversity. reported in the literature for the various Comprehensive ethnobiology research taxonomic groups (Ramírez­Bautista et al. has been previously addressed by Toledo et 2017). al. (1983) who documented 410 species for Conceptual contribution the Pu'rhépechas, Hunn (2008) who recorded a total of 1,379 species (fungi, We propose that Biocultural diversity as: plants, invertebrates and vertebrates) known “the variety of organisms that are known, and used by the Zapotecs, and Aldasoro­ named, classified, organized, used, Maya (2012) who reported 264 species exploited, domesticated and/or manipulated known and used by the the Tlahuica. by different human societies; including the However, there are few such ethnobiology social­ecological systems of which this studies using a comprehensive approach, for

12 Gutiérrez­Santillán et al. 2019. Knowledge and use of biocultural diversity by Nahua in the Huasteca region of Hidalgo, Mexico Ethnobio Conserv 8:7

diversity forms a part at various referring to the ethnospecies, which must be spatiotemporal scales (Gutiérrez­Santillan integrated by the taxonomic identity of the 2018). But this concept also must be species plus their corresponding culture; this referred to the correlation between its criterion should apply regardless whether the biological, ecological, environmental, investigation has a qualitative or quantitative geographical, cultural and linguistic approach. In addition, the establishment of components; include a regional or global ethnospecies as units of analysis, as has spatial scale (Maffi 2005; 2007; Loh and been done in ecology (Moreno et al. 2011; Harmon 2005; Harmon and Loh 2010; Stepp Moreno et al. 2017) favors the adaptation of et al. 2004; 2005; Turvey and Pettorelli current metrics used in the analysis of 2014). However, in sensu stricto has been biological diversity to the analysis of seen that biological diversity and biocultural biocultural diversity. diversity are not entirely congruent in terms The identity of the social­ecological units of the factors that generate them (Cardillo et is critical to begin to understand biocultural al. 2015). diversity from a more local and analogous However, the design of a conceptual view to biodiversity. Our study allows us to framework in the metric of cultural diversity observe another pattern more like those of analogous to that of biological diversity will biological diversity, such as the recognition not only allow us to understand it, but also to of common species, as well as rare species confirm that its identification and evaluation (Turner et al. 2011). As examples of common are adequate (Maclaurin and Sterelny 2008). species we have the coyote/coyochichi Currently, the existence of biocultural (Canis latrans), the pigeons/singuilotl diversity as a real and inherent property of (Claravis pretiosa, Leptotila verreauxi, the social­ecological relationship is not Geotrygon albifacies), the fungus orejita­de­ discussed, however, semantic, conceptual viejita/cuapetachiquinte (Auricularia auricula, and analytical gaps are detected; for which A. delicata, A. fuscosuccinea), and trees different approaches can be useful to such as guava (Psidium guajava) and generate new research perspectives as in framboyán/ framboyánxuchitl (Delonix regia). ecology (Moreno et al. 2011). And as rare species we have the One of the fundamental bases for the anguila/coatlmichi (Anguilla rostrata), the conceptual development of biocultural jaguar/tecuani (Panthera onca) and, the diversity is the establishment of real and perro­de­agua/atlchich (Lontra longicaudis), identifiable social­ecological units or entities, these recently reported species for the state as for example in ecology, that operational of Hidalgo (Aguilar­López et al. 2015; taxonomic units have been used (Krell Morales­García and Acosta­Rosales 2015). 2004). Although ethnobiology has sought to Or tree species that are very scarce in the develop research on the knowledge and use surrounding forests, but culturally highly of biodiversity, some of the previous studies valued as the palo­escrito (Dalbergia palo­ do not discriminate between species and escrito) or the palo­varón/tlacacuahuitl ethnospecies, or do not consider this (Ulmus mexicana). Even the documentation criterion as a rule in ethnobiological of a locally extinct species was obtained: the research; taking both as an independent mono/chango (Ateles geoffroyi), which is record or identifiable entity. We consider it estimated to have been extirpated from essential to establish the units of analysis, northeastern Mexico (Ceballos and Oliva

13 Gutiérrez­Santillán et al. 2019. Knowledge and use of biocultural diversity by Nahua in the Huasteca region of Hidalgo, Mexico Ethnobio Conserv 8:7

2005). effort is enough using accumulation curves Biocultural diversity is part of the memory (Alves et al. 2016). The curves showed that or biocultural heritage of indigenous peoples, the number of interviews was enough for the their documentation, analysis and inventory. This suggests that when the evaluation; it can be appreciated by percentage ethnographic method, which biologists of conservation, by documenting generally implies sampling 10% of the traditional knowledge and practices historical inhabitants of a population (Bernard 2006) is and currently conducted on biodiversity, applied in combination with the snowball helping to understand changes in local method (Trotter et al. 2001), it is possible to biodiversity and designing appropriate obtain a robust inventory of ethnobiological conservation strategies (Brook and information. In addition, selecting informants McLachlan 2008, Saslis­Lagoudakis and using the snowball method enables a Clarke 2012). In addition, under the random sample to be drawn (Trotter et al. perspectives projected in this research, we 2001). In addition, the combination of seek to open a way for conceptualization ethnographic tools (multiple free lists and and the establishment of methodologies that semi­structured interviews) also allow an help to understand biocultural diversity from adequate collection of information. the low level to more complex analyzes, These metrics can be used to corroborate such as, for example, macro­ethnobiological the completeness of the ethnobiological (Gutierrez­Santillán et al. 2019b), the data, since the accumulation curves and evolutionary ethnobiology (Albuquerque y estimates of chosen species (non­ Ferreira­Junior 2017), the niche construction parametric) are good indicators of the quality theory and ethnobiology (Albuquerque et al. of the sample (Albino­García et al. 2011; 2018); and the development of the social­ Benz et al. 2000; Hopkins and Stepp 2012; ecological theory of maximization Lozada et al. 2006; Pineda and Verdú 2013), (Albuquerque et al. 2019). in our case indicating proper ethnographic sampling. The use of new metrics for the In the accumulation curves, frequency of analysis and evaluation of biocultural mention is used, considering each informant diversity as a sampling unit, and the mentions of ethnospecies represent their cultural The comprehensive analysis of biocultural importance, not their abundance in nature. In diversity (multitaxonomic and quantitative) ethnographic sampling there are generates a clearer picture of social­ ethnospecies that are constantly mentioned, ecological knowledge. To do so, it is or common, and ethnospecies that are essential to evaluate biocultural diversity mentioned only occasionally or rarely. using metrics, which give greater robustness However, it is important to assess in which to the results and allow for comparisons, as cases to apply the accumulation curve or has been done in ecology (Moreno et al. not, since the curve may be indicating that 2017). our inventory is close to the optimum; that is, It is, of course, important that the increasing the sampling number maintains theoretical assumptions required for the the asymptote constant (Alves et al. 2016; chosen metrics be met. In this case, we Moroy­Vilchis et al. 2008); but other evaluate whether the ethnographic sampling methodological aspects must be adhered to,

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such as ensuring random and homogeneous which we consider could cause bias. sampling. We suggest that the suitability of For the implementation of these and other biodiversity metrics should be evaluated for metrics, it is essential to keep in mind that use in ethnobiological studies, in order to the methods used in the analysis of determine whether an ethnographic sample biological diversity are constantly being behaves in a similar way to an ecological updated (Moreno et al. 2011; 2017), making sample. The relevance of other indexes it necessary to evaluate their usefulness in should be considered as well; not only those ethnobiological or biocultural diversity that are based on incidence but also those studies. For example, the zero­order (0D) that take abundance values into account. and first­order diversity index (1D) are in We consider that using ethnobiological or current use (Hill 1973; Jost 2006). The social­ecological units (taxonomic species + advantage of using these indices is that the cultural assignment) and making results are comparable within a study and comparisons between the degree of with other studies in the same region biological diversity and the diversity of whether intra­ or inter­ethnically; and across ethnospecies are sufficient reason to apply time spans to evaluate cultural changes in more refined forms of analysis to evaluate knowledge or uses; that is, to evaluate local biocultural diversity. However, it is essential knowledge at different space and time to ensure the quality of the methodological scales (Gutiérrez­Santillán et al. 2019b). design such that it involves proper collection In this study we use only the 0D and 1D of sufficient data, to avoid a subjective diversity indices, because the zero­order interpretation. diversity data corresponds to species richness, in our case ethnospecies richness, Trends of use while first­order diversity includes all species with a weight precisely proportional to their One of the most important characteristics abundance in the community (Hill 1973; Jost of biocultural diversity is its use by human 2006; Moreno et al. 2011). In ethnographic groups. Studies in other regions of Mexico sampling, all species reported by the have documented various use categories for inhabitants correspond to a site, and they different taxonomic groups (Lira et al. 2009; have the same representation in the sample Monroy­Vilchis et al. 2008). In this study, 11 regardless of their frequency of mention, so categories, which contribute to satisfying a this proportion is maintained. For this index, wide range of human needs, were identified. second­order diversity (2D) is also Different indigenous groups use species in calculated, but its application is not different ways for different purposes, which recommended for the present case, because reflects the importance of nature in this measure is based on the dominance of contemporary societies (Alonso­Castro et al. the species present in a sample (Jost 2006; 2011; Carbajal­Esquivel et al. 2012; Toledo Moreno et al. 2011; 2017). In ethnobiological 1994). data we have ethnospecies that are In addition to the application of represented with a high frequency of appropriate metrics, the use of multivariate mention, which may be biased towards statistical methods provides a broader view some cultural or even economic preference of the social­ecological relationships in the that strongly influences its frequent mention, study area. In this case, implementing CA

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enabled a graphical association to be made main ethnobiological subdisciplines: between use categories and the various ethnobotany, ethnomycology and taxonomic groups. Several authors have ethnozoology (Figure 5). It is suggested that used these methods, finding structural the conceptualization of biocultural diversity relationships between the study groups; e.g., be extended beyond its cultural and between taxonomic families and habitat biological components. We propose that types (Molares and Ladio 2009), species biocultural diversity be considered as “the management types (Parra et al. 2012), variety of organisms that are known, named, species (Zamudio and Hilgert 2012) and classified, organized, used, exploited, knowledge among several indigenous domesticated and/or manipulated by groups (Núñez­García et al. 2012). We different human societies”; including the found that certain biological groups are social­ecological systems of which this associated with specific categories, as a diversity forms a part at various characteristic of the biological group and its spatiotemporal scales (Gutiérrez­Santillán use. 2019b). It is composed essentially of CONCLUSIONS ethnospecies, which consist of a taxonomic entity (species) together with its cultural The Nahuas of the Huasteca region in the counterpart (traditional name). When the state of Hidalgo have extensive knowledge basic units of biocultural diversity are and make widespread use of the biodiversity defined, they can be analyzed using the new in their territories. This study has shown that metrics used for the analysis of biological each of the vegetation types contributes diversity, enabling a better assessment of particular characteristics in terms of social­ biocultural diversity and more robust data to ecological relationships at the cultural level, be generated, which can be compared on a phenomenon associated with the presence the intra­ or interethnic level, between of unique species of the tropical semi­ regions, ecosystems, or other divisions. In evergreen forest and the montane cloud addition, this approach can be used to forest. However, since the two study generate and provide sociocultural data for communities belong to the same indigenous the implementation of conservation group, are located in the same geographical strategies under a biocultural approach. region and are in contact with the same widely distributed and introduced species, ACKNOWLEDGEMENTS there are strong similarities in their knowledge and use of these species. In Thanks are expressed to the residents of addition, it was found that each of the the study communities who kindly supported biological groups contributes in a particular this research and contributed their invaluable way and in some cases exclusively in their knowledge, and to the UAEH for its support respective use categories, especially in the of AMF, ASG and GSR so that this research case of plants and animals. could be carried out. TVGS received a This study contributes to a scholarship from CONACyT comprehensive view of the multitaxonomic (389096/254575). analysis of biodiversity known and used by a indigenous group, by combining the three

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Figure 5. A) Pet boar (Tayassu tajacu, MCF); B) Striped (lowland) paca meat (Cuniculus paca, TSEF); C) Child with preserved margay (Leopardus weidii, MCF); D) Pet red­billed pigeon (Patagioenas flavirostris, TSEF); E) Informant with preserved emerald toucanet (Aulacorhynchus prasinus, MCF); F) Child fisherman (TSEF); G) crayfish (Procambarus sp., TSEF); H) cosol, river crayfish trap (TSEF); I) Cross decorated with cycad leaves (Zamia herrerae, MCF); J) Itztacnanacatl fungus on papatla leaf (Pleurotus albidus, Heliconia collinsiana; MCF); K) yam and squash (Ipomoea batatas, Cucurbita maxima; TSEF); L) two species of marigold (cempoal) in ceremony for festival of Our Lady of Guadalupe (Dec. 12) (Tagetes coronopifolia, Tagetes erecta; TSEF). TSEF = tropical semi­evergreen, MCF = montane cloud forest.

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Received: 01 February 2019 Accepted: 28 May 2019 Published: 21 June 2019

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Supplementary Material

List of biocultural diversity for two communities of the Huasteca, Hidalguense; the type of vegetation is tropical semi­evergreen forest (TSEF) and montane cloud forest (MCF). The table contains the following data: family, gender and species, local name in spanish and nahuatl, vegetation type (TSEF / MCF) and category of use and utilization (ceremonial= I, fuel= II, edible= III, IV= construction, V= timber, VI= pet, VII= medicinal, VIII= ornamental, IX= others, X= agricultural use, XI= trade).

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