Forest Policy and Economics 73 (2016) 239–250

Contents lists available at ScienceDirect

Forest Policy and Economics

journal homepage: www.elsevier.com/locate/forpol

A local knowledge-based approach to predict anthropic harvesting

pressure zones of wild edible mushrooms as a tool for forest conservation
in Central Mexico
Sergio Franco-Maass a, Cristina Burrola-Aguilar b,⁎, Yolanda Arana-Gabriel b, Luis Antonio García-Almaraz a
a
Instituto de Ciencias Agropecuarias y Rurales, Universidad Autónoma del Estado de México, Instituto Literario 100, col. Centro, C.P. 50000 Toluca, Estado de México, Mexico
b
Centro de Investigación en Recursos Bióticos, Facultad de Ciencias, Universidad Autónoma del Estado de México, Km 14.5, carretera Toluca-Atlacomulco, C.P. 50200 Toluca, Estado de México,
Mexico

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to develop a model to estimate human pressure exercised through the process of har-
Received 18 May 2016 vesting mushrooms on the high mountain forest ecosystems of Central Mexico. To predict human pressure, we
Received in revised form 21 September 2016 applied a local knowledge-based model to a Geographic Information Systems and Multi-Criteria Evaluation
Accepted 27 September 2016
(GIS-MCE) approach. The study area was Nevado de Toluca, which is located in a mountainous forest ecosystem
Available online xxxx
of the Trans-Mexican Volcanic Belt. To construct the model, we used cartography data (land cover map, digital
Keywords:
elevation model [DEM], distribution of villages, roads and sidewalks) and local knowledge regarding mushroom
Ethnomycology harvesting (questionnaires, semi-structured interviews, field trips with mushroom harvesters). The level of pres-
GIS sure model was based on the application of the Weighted Linear Combination (WLC). Thus, harvesters were que-
Abies religiosa ried regarding the importance of the main criteria cited in the literature and whether they considered looking for
Multi-Criteria Evaluation the best harvesting sites. With the information generated, a multi-criteria image was obtained that expressed the
Policy potential harvesting pressure. The model was validated with real data from field trips. The location of harvesting
sites was then compared with the level of pressure obtained with the GIS analysis model. The model demonstrat-
ed that proximity to fir (Abies religiosa) forests exerted a greater influence on the value of the obtained pressure
level; moreover, this type of vegetation is preferred by the local people for harvesting mushrooms. The final
human pressure map confirmed that the model closely reflected the behavior of the mushroom harvesters in
the studied region, and it was applied considering the 23 villages within the protected region of Nevado de To-
luca. The information obtained can be used to locate areas with increased harvesting pressure, to establish poten-
tial sites for mushroom production, to propose a special program that includes management policies with
successive harvesting schemes, or to define priority areas for monitoring and conserving this type of non-
wood forest products (NWFPs).
© 2016 Elsevier B.V. All rights reserved.

1. Introduction (Rodríguez-Muñoz et al., 2012). This activity represents a real alterna-

Worldwide, the consumption of mushrooms has increased, of which
marketing is a popular activity for rural communities to promote new
revenue (Boa, 2004; Cai et al., 2011). After China, Mexico ranks second
in the number of wild mushrooms traditionally consumed. There are
371 mushroom species which are considered as NWFPs (Garibay-
Orijel and Ruan-Soto, 2014). They serve as food and have a high eco-
nomic importance for rural communities who live near forests
(Mariaca et al., 2001; Pérez-Moreno et al., 2008; Garibay-Orijel et al.,
2009). The harvest of mushrooms is a social activity (Montoya et al.,
2008) that is part of the bio-cultural heritage of the rural population
and involves a strong sense of family and community bonding
⁎ Corresponding author.
E-mail addresses: sfrancom@uaemex.mx (S. Franco-Maass), cba@uaemex.mx
(C. Burrola-Aguilar), agyarana@hotmail.com (Y. Arana-Gabriel).
tive for sustainable forest management and generates significant envi-
ronmental, economic and social benefits (Benítez-Badillo et al., 2013).
Some factors related to the harvest of mushrooms are the type of
vegetation, abundance, distribution, accessibility, cultural importance,
consumer preferences, assigned prices (Jarvis et al., 2004; Ruan-Soto
et al., 2009), distance between forests and the town where they are
marketed, demand, and income from sales (Montoya-Esquivel et al.,
2002, 2003; Garibay-Orijel et al., 2007; Burrola-Aguilar et al., 2012).
Local knowledge plays an important role in the selection of the harvest
sites and collection route. The collection process starts with knowledge
of the habitat of the fungi and their morphological characteristics. Peo-
ple use information transmitted by the elderly as well as their own ex-
perience, the phenology of species, environmental conditions (climate,
soil and micro-topographical conditions), and tree species that are asso-
ciated with the elevation of each gathering area, which influence the
presence of fungi (Mariaca et al., 2001; Montoya et al., 2014).

http://dx.doi.org/10.1016/j.forpol.2016.09.020
1389-9341/© 2016 Elsevier B.V. All rights reserved.
240 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250
On average, a mushroom gatherer walks in the forest for 4 h, be-
tween 8 and 20 km per day (Montoya et al., 2008), and includes more
than 120 fruiting bodies in various locations. According to the different
communities, collection patterns vary among harvesters and between
men and women. Men travel longer distances at higher elevation, but
they harvest fewer species and visit fewer collection sites. In contrast,
women exhibit better performance and more easily adopt appropriate
search strategies (Pacheco-Cobos et al., 2010).
Although harvesting is an important socio-economic activity, there
are no reliable data to determine whether that activity threatens the
mushroom populations. However, the effects of repeated harvesting
on the forest habitat are unknown (Arteaga and Moreno, 2006). The ex-
pansion of the commercial gathering in many parts of the world, has led
to reflect on the possible damage to the overexploitation of fungal re-
sources. In spite of this, it has been found in systematic studies and
long term, that constant and periodic harvesting not reduce the amount
collected or the richness of species of wild mushrooms (Egli et al., 2006).
In addition, the high value of wild mushrooms in the national and inter-
national markets has increased their collection from the temperate for-
ests of Mexico, transforming their use from a level of self-consumption
and local sales to commercialization on a larger scale. This expansion
has generated a habitat disturbance, resulting in land degradation. For
example, the removal of other organisms that interact with fungi, or dis-
ruption of the mushroom life cycle conducive a decrease the abundance
and distribution of the populations of fungi (Alvarado-Castillo and
Benítez, 2009).
According to Jasso-Arriaga et al. (2016), who carried out research on
traditional knowledge and vulnerability of edible mushrooms in the
Nevado de Toluca, they found that some harvesters who possess tradi-
tional ecological knowledge, argue that most of the habitats of mush-
rooms have disappeared mainly by activities such as irrational felling
of trees, trampling, grazing and lack of moisture and organic matter in
the forest. These are human activities that have contributed to the de-
cline of 36 species of edible mushrooms in the region.
Therefore, it is necessary to implement sustainable development
strategies, including knowledge of biology, ecology and productivity of
Fig. 1. Villages and land cover in the protected area of Nevado de Toluca.
wild edible mushrooms of cultural or economic importance to the peo-
ple of the region (Ortega-Martínez and Martínez-Peña, 2008). For ex-
ample, mushroom harvesters in Oaxaca, Mexico, have zoned their
communally owned land to prevent timber extraction or other land
uses from damaging mushroom collecting areas. They have also started
training harvesters to avoid litter removal, which has a negative impact
on production, and to recognize different quality grades (Belcher and
Schreckenberg, 2007).
The Geographic Information System (GIS) has been a very powerful
tool for the evaluation of NWFPs. Pilz and Molina (2002) proposed its
use to estimate the production of edible mushrooms across a watershed
or area of land. Yang et al. (2006) forecasted the habitat of matsutake
mushrooms using logistic regression and a GIS expert system with envi-
ronmental and stand parameters. Garibay-Orijel et al. (2009) proposed
the use of a GIS to improve mushroom harvesting by the local commu-
nities on a commercial scale. Mumcu and Zeki (2015) developed a GIS
program to create spatial distribution maps of Lactarius deliciosus and
L. salmonicolor to prepare multi-purpose forest management plans
that include NWFPs. The GIS-Multi-Criteria Evaluation (MCE) approach
has been very useful for forest conservation planning (Phua and
Minowa, 2005; Greene et al., 2010; Matsuura et al., 2014a) which ap-
plied MCE based on the analytic hierarchy process (AHP) and GIS to an-
alyze the spatial characteristics of the habitat distribution of fern
species, considering both natural and anthropogenic factors.
The integration of MCE with GIS involves the use of geographical
data, the definition of decision-maker's preferences and the selection
of a defined rule (Malczewski, 2004). The preferences usually depend
on the knowledge of technical experts. Considering that NWFP harvest
sites are generally influenced by both the ecological characteristics of
each species, and human harvesting behaviors (Matsuura et al.,
2014a), the knowledge of local forest harvesters can be very useful to
determine the criteria and preferences involved in identifying harvest-
ing sites (Matsuura et al., 2014b). Local expert knowledge adds value
to science by providing detailed insights into local and regional environ-
mental problems (Chalmers and Fabricius, 2007). It is important to con-
sider that local pickers have long-term experience locating the
 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250 241

Table 1 2. Materials and methods

Vegetation classes and dominant species in the study area.

Dominant 2.1. Study area

Class Subclassa species

Conifer forest Dense fir forest Abies religiosa The Nevado de Toluca region is a natural protected area located in
Open fir forest the central occident of the State of Mexico with altitudes ranging from
Dense fir-pine forest A. religiosa 3000 to 4600 m.a.s.l. (Fig. 1). The protected area occupies an area of
Pinus harwegii
51,000 ha and has temperate sub-humid weather. Rainfall occurs from
P. ayacahuite
Open fir-pine forest A. religiosa May to October, with an annual average of 800 mm and an average tem-
P. harwegii perature of 17.3 °C (Endara-Agramont et al., 2012). The region is cov-
Dense pine forest P. harwegii ered by temperate woods, pure stands, or with other species under
P. montezumae the canopy, mainly consisting of sacred fir (Abies religiosa) and pine
P. ayacahuite
P. psedotsuga
(Pinus spp.). There are also some small regions covered by alder (Alnus
Open pine forest P. harwegii acuminate) and oak (Quercus spp.) (Endara-Agramont et al., 2012). Sa-
Cedar plantation forest Cupressus cred fir is the most common species in the Trans-Mexican Volcanic
lusitanica Belt between an altitude of 2500 and 3500 m (Ferrusquía-Villafranca,
Deciduous Dense alder forest Alnus acuminata
2007); it is among the less studied dominant trees in Mexico and har-
broadleaved Open alder forest
forest Dense oak forest Quercus laurina bors the highest species density and fruit body productivity of wild ed-
Q. crassipes ible mushrooms among five different vegetation types in the
Q. crassifolia neotropical temperate forest region (Burrola-Aguilar et al., 2013). The
Q. rugosa Nevado de Toluca has recently been subjected to increasing distur-
Grassland and Grassland Calamagrostis
bances caused by the growing human population, which has converted
scrubland tolucensis
Festuca forests for crop agriculture and pastures. There are 23 villages inside the
tolucensis natural protected area that are threatening forest conservation, includ-
Muhlenbergia ing overexploitation of wild edible mushrooms. It is important to gener-
montana
ate detailed information to help develop forest conservation strategies
Shrubland Eryngium
monocephalum
for this region.
Cirsium
jorullense
Symphoricarpos 2.2. Data collection
sp.
Senecio
cinerarioides 2.2.1. Cartography
Others Settlement, bare land, rock, alpine pasture,
cropland, or water bodies. 2.2.1.1. Land cover map. Data were derived from a land use map (2009)
a
We consider as dense forests when trees cover more than 50% of the surface. Open generated by visual interpretation of digital images from the Spot 5 sat-
forests have between 25 and 50% of secondary tree occupation. ellite with reference to data of a land use map (2000) obtained from or-
thographic photos on a 1:20,000 scale, generated by the Institute of
Geography, Statistics and Cadastral Research and Information of the
appropriate areas for mushroom harvesting (Mumcu and Zeki, 2015). State of Mexico (IIIGECEM, for its acronym in Spanish) (Green et al.,
Yang et al. (2006) developed a GIS expert system that integrates local 1998; Regil et al., 2014). This allowed us to obtain a map with details
knowledge into a model to determine the distribution of matsutake in to 0.1 ha. The resulting map in vector format contains 125 categories
certain locations based on the available evidence. of land cover and was validated as recommended by Chuvieco (2002)
The protected Nevado de Toluca area is a representative region of with 196 plot samples to obtain an error probability of 95%, which sur-
high mountain forest ecosystems in Central Mexico. Edible mushrooms passes the minimum of 80% required for map validation. The map was
have been exploited in this region for several decades without any kind obtained in vector format using ArcGIS and contains the same land
of management. They are collected without control, and therefore their cover scheme recommended by the National Institute of Statistics and
potential use is unknown. In general, there is a lack of scientific and Geographic Information (INEGI, for its acronym in Spanish) (Franco et
technological knowledge concerning this resource, and thus there are al., 2006). To simplify the local behavior enquiry, the land use map
no alternatives for organizing and regulating mushroom collection was then generalized in a series of subclasses according the dominant
and use (Franco-Maass et al., 2012). species (Table 1). An important proportion of the surface is occupied
The objective of our research was to develop a model to estimate by a non-forest category (grasslands, agricultural lands, shrubs, naked
human pressure caused by mushroom collection in the high mountain soil, and anthropic intervention) (Regil et al., 2014).
forest ecosystems of Central Mexico. The development of strategies for
the conservation and use of edible mushrooms can be done with the
aid of this model. To predict human pressure, we applied a local knowl- 2.2.1.2. Topography. A digital elevation model (DEM) was generated
edge-based model to a GIS-MCE approach. The model was applied to using the Intercon algorithm of Idrisi Selva ver. 17.0 (Eastman, 2012),
the Nevado de Toluca region, but it can be applied to other mountainous based on digitized contour lines from IIIGECEM (20 m equidistant). To
forest ecosystems in the Trans-Mexican Volcanic Belt. validate the model, a series of 60 randomly distributed checkpoints
In the present study, we propose a potential area for management, was obtained in the field. A root mean square error (RMSE) of 4.0 m
an Abies religiosa forest, which is a type of dominant vegetation that ex- was obtained, which is consistent with the US geological survey stan-
hibits the greatest fungal species richness, as Agaricus subrutilescens, dards (Felicísimo, 1994).
Helvella crispa, H. lacunosa, Amanita calyptroderma, A. novinupta,
Lycoperdon perlatum, Lyophyllum shimeji, Floccularia aff. luteovirens,
Psathyrella spadicea, Laccaria trichodermophora, Tricholoma equestre, Bo- 2.2.1.3. Housing units, roads, and sidewalks. The distribution of villages,
letus edulis s.l., Suillus pseudobrevipes, Cantharellus subalbidus, Gomphus roads and sidewalks was obtained from the topographic maps
spp., Ramaria spp., Lactarius scrobiculatus, and Russula americana. 1:50,000 in ArcGIS vector format produced by INEGI.
242 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250

Table 2 2.2.2. Local knowledge of mushroom harvesting

Variables most frequently mentioned in the literature that affect presence and abundance Data collection was conducted during the harvesting season of 2009
of mushrooms and its relative importance for the harvesters.
(from May to October), corresponding to the rainy season in this region,
Relative importance for and consisted of three stages as follows:
Variable Description the harvesters
a) Application of 165 questionnaires in randomly selected housing
Vegetation class (Mueller Dense fir forest, open fir Very high
and Halling, 1995) forest, dense fir-pine
units of nine villages, representing 13.6% of the housing units in
forest, open fir-pine the protected area. The selection of the villages was based on three
forest, dense pine forest, fundamental criteria: the number of inhabitants; the prevailing eco-
open pine forest, cedar nomic activity and; its geographical location in relation to the for-
plantation, dense alder
ests. For example El Varal had only 51 inhabitants dedicated to
forest, open alder forest,
dense oak forest, cattle breeding and it was surrounded by dense fir forests. San
grassland, shrubland. Roman had 138 inhabitants engaged in agricultural production and
Slope (Mariaca et al., Considered as the High was surrounded by dense alder and oak forests. Raices had 664 in-
2001) difficulty of movement in habitants with a very diversified economy and was located next to
terms of the degree of
terrain inclination
the open pine forests. In this way we sought to achieve greater rep-
Proximity to the housing Path distance from the Medium resentation in the various types of villages. In each randomly select-
unit (Mariaca et al., house of the harvester to ed housing unit we interviewed only one member of the family (91
2001) the harvesting site were women and 47 were men). The questionnaires compiled infor-
Proximity to roads and Path distance from the Low
mation about how local people collect timber and non-timber re-
sidewalks (Mariaca et nearest road or sidewalk
al., 2001) to the harvesting site sources, and they allowed us to identify individuals who were
Undergrowth type The abundance of some Only relevant to some known locally as principal mushroom harvesters.
(Termorshuizen, 1993; mushrooms are species b) Semi-structured interviews of 13 people recognized as principal
Egli et al., 2006) associated with specific mushroom harvesters within their communities and who had in-
types of undergrowth that
are not considered in the
depth knowledge of regional edible mushrooms (Alexiades, 1996),
decision process by we call these people leader harvesters. The ages of the harvesters
harvesters varied from 32 to 65 years, and were six women and seven men.
Altitude (Salerni and Height from sea level Not relevant Our specific key questions were as follows:
Perini, 2004;
i. What, according to local experts, were the main criteria taken into
Villanueva-Jiménez et
al., 2006; Daza et al., account to define the harvesting routes?
2006; ii. What was the importance and order of priority of a series of
Zamora-Martínez et al., criteria found in the literature that exert an influence on the pres-
2013; Fierros et al., ence of wild edible mushrooms? (Table 2)
2000; Bonet et al.,
2008)
Aspect (Fierros et al., The direction of c) Field trips with the 13 leader harvesters, sometimes they were ac-
2000; Bonet et al., maximum downward companied by their children. These people were previously
2008) slope
interviewed to validate the model and characterize the collection
Age and structure of the Forest characteristics in
forest (Mueller and terms of age, composition
routes. We use the technique of participant observation to under-
Halling, 1995) and structure stand and explain the process of harvesting.
Disturbance degree The intensity of anthropic
(Mueller et al., 2004) interventions such as
logging, forest fires or
overgrazing 2.3. Construction of the model
Temperature (Salerni and Monthly average The harvesters consider
Perini, 2004; temperature these criteria as constant The level of pressure model is based on the application of the
Villanueva-Jiménez et during the rainy season Weighted Linear Combination (WLC), which is easy to implement,
al., 2006; Daza et al.,
2006;
easy to understand, and is intuitively appealing to decision-makers
Zamora-Martínez et al., (Malczewski, 2006):
2013; Martínez de
Aragón et al., 2007) Xn
Precipitation (Salerni and Average monthly rainfall P¼ j¼1
w j C ij ;
Perini, 2004;
Villanueva-Jiménez et
al., 2006; Daza et al., where P is the level of mushroom harvesting pressure, wj is the relative
2006; importance of criterion jð∑wi ¼ 1Þ and Cij is the value of the criterion j
Zamora-Martínez et al.,
2013; Martínez de
in the alternative i.
Aragón et al., 2007)
Acidity of soil (Salerni In terms of pH The harvesters are not
Table 3
and Perini, 2004; familiar with these
Factors in the Multi-Criteria Evaluation (MCE).
Villanueva-Jiménez et criteria, and thus it was
al., 2006; Daza et al., difficult for them to Factor Description
2006; establish a relative
Zamora-Martínez et al., importance Vegetation class/Villages Resistance from every pixel in terms of vegetation
2013) cost (Veg-Vil cost) classes to the nearest village
Evapotranspiration Expressed in millimeters Vegetation class/Roads cost Resistance from every pixel in terms of vegetation
(Martínez de Aragón et per unit time (Veg-Roads cost) classes to the nearest road or sidewalk
al., 2007) Slope/Villages cost Resistance from every pixel in terms of the slope to
Moisture Soil and environmental (Slope-Vil cost) the nearest village
(Zamora-Martínez et moisture Slope/Roads cost Resistance from every pixel in terms of the slope to
al., 2013) (Slope-Roads cost) the nearest road or sidewalk
 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250 243

Table 4 Decision preferences were generated from local knowledge, and the ob-
Friction values in the vegetation classes. jective was not to model the presence or abundance of the mushrooms
Relative Friction but to estimate human pressure according to the knowledge and prefer-
Vegetation class importance value ences of local harvesters.
Dense fir forest Extremely 1 We asked the local harvesters to establish the relative importance
high (from not relevant to very high) of the main criteria cited in the special-
Dense fir-pine forest Very high 4 ized literature and what they considered important in their search for
Dense pine forest High 6
the best harvesting sites (Table 2).
Dense alder forest Medium 10
Open fir forest Medium 12 According to our findings, the explanatory variables used by the
Open pine forest Medium 15 local harvesters were “vegetation classes; slope and; proximity to vil-
Open fir-pine forest Medium 17 lages and roadways and sidewalks”. They considered other criteria as ir-
Grassland and scrubland Low 50 relevant. Proximity to certain classes of vegetation, particularly forests
Dense oak forest Very low 70
Open alder forest Extremely low 80
of fir, was the most important criterion. Ease of access based on the
Cedar plantation Extremely low 85 lower slope was also considered important. Consequently, the model
Shrubland, grassland, alpine pasture, cropland, None 100 considers the theoretical walking difficulty using the villages and
settlements and bare land roads as the target and two friction value images (vegetation class and
slope) (Table 3). According to Eastman (2003) a cost surface implies
The WLC is one of the most often used decision strategies in GIS- the cost of moving through space. But it can also consider frictions and
MCDA (Boroushaki and Malczewski, 2008), and it can be implemented forces that impede or facilitate that movement. Taking into account an
into a GIS environment with overlay capabilities (Malczewski, 2004). image of a set of features (for example villages) and a surface that affect

Fig. 2. Cost of displacement according to the 4 factors.

244 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250

Table 5 The application of the Costgrow algorithm allowed us to obtain four

Pairwise comparison matrix of the factors. cost surfaces. Each of them represents the cost of travel from the villages
Veg-Vil Veg-Roads Slope-Vil Slope-Roads or roads in function of the friction exerted by the slope or vegetation. In
cost cost cost cost wij the resulting images the maximum cost represents the less appealing
Veg-Vil cost 1 0.5184 regions for the harvesters, therefore it was necessary to carry out a pro-
Veg-Roads 1/2 1 0.3035 cess to reverse these values. Finally the four factors had to be expressed
cost in a common scale before combination. We adopted the 0–255 byte
Slope-Vil cost 1/4 1/3 1 0.117
scale recommended by Eastman (2003). The higher value of the stan-
Slope-Roads 1/8 1/5 1/2 1 0.061
cost dardized scale (255) in a factor image corresponds to the higher attrac-
Consistency ratio: 0.01 tiveness for the harvester in that factor (Fig. 2).
To score the factors (wij), pairwise comparisons of the criteria and
the movement (for example slope) the resulting image expresses costs the eigenvalue technique were applied using the analytic hierarchy pro-
of movement in terms of distance. To generate the maps, we applied the cess (AHP) (Saaty, 1977). We asked the harvesters to rank the intensity
Costgrow algorithm using Idrisi Selva ver. 17.0 (Eastman, 2012). of importance of each class into nine grades, and then compared the
The slope friction image was obtained from the reclassification of the scores among classes. The construction of the final pairwise comparison
slope degree image to obtain an image with integer values between one matrix required to establish a dialogue between local harvesters to
(minimum slope) and 70 (maximum slope). The vegetation class fric- achieve a decision based on consensus (Table 5).
tion image was derived from the opinion of the 13 interviewed har- The Idrisi Selva weight algorithm allowed us to compute wij by calcu-
vesters. We asked the harvesters to assign a value in a 1 to 10 scale lating the principal eigenvector of the pairwise reciprocal comparison ma-
according to the perceived abundance of edible mushrooms in the 11 trix. The consistency ratio of the pairwise comparisons was 0.01, which
forest types. Fir forests received the highest score possible by consensus indicated that the matrix ratings were acceptable (Eastman, 2003).
(130). Cedar plantations were considered very unproductive and re- The weights could then be used with MCE to create a multi-criteria
ceived the minimum score (13). Scores were then inverted (the maxi- image expressing the potential harvesting pressure (Fig. 3).
mum value was the most appealing for the harvesters and therefore Based on the results of the GIS model, the potential pressure for harvest-
should represent the minimum difficulty of displacement). To assign ing sites was estimated within the study area. Note that -potential pressure-
the final value of friction of each forest type linear normalization was should be interpreted in terms of the human harvesting attractiveness
applied on a scale of 1 to 100 (Table 4). and not in terms of the diversity or abundance of edible mushrooms.

Fig. 3. Analysis model for the application of GIS to estimate the harvest pressure.
 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250 245

Table 6
Harvesting results in the nine villages.

Self-consumption Self-consumption/sell Sell Sell/self-consumption No harvest

Village Housing units Total housing units Total habitants Num. % Num. % Num. % Num. % Num. %

Agua Blanca 17 19 113 6 35.3 4 23.5 4 23.5 2 11.8 1 5.9

Buenavista 20 132 560 10 50.0 2 10.0 2 10.0 2 10.0 4 20.0
Contadero 36 494 2082 25 69.4 1 2.8 1 2.8 1 2.8 8 22.2
El Varal 6 13 51 4 66.7 1 16.7 0 0.0 1 16.7 0 0.0
La Peñuela 16 161 655 13 81.3 0 0.0 0 0.0 1 6.3 2 12.5
La Puerta 15 70 253 14 93.3 0 0.0 0 0.0 0 0.0 1 6.7
Loma Alta 16 139 530 12 75.0 2 12.5 0 0.0 0 0.0 2 12.5
Raíces 30 150 664 20 66.7 2 6.7 0 0.0 4 13.3 4 13.3
San Román 9 38 138 2 22.2 2 22.2 0 0.0 0 0.0 5 55.6
Total 165 1216 5046 106 64.2 14 8.5 7 4.2 11 6.7 27 16.4

2.4. Model validation
The model was validated using real data from 13 field trips. By re-
cording the GPS tracks followed by the local harvesters, it was possible
to locate 293 harvesting sites. In average the harvest sites cover an
area of 1000 m2 and their central positions were then compared with
the level of pressure obtained using the GIS analysis model.
Representative samples of edible mushroom were collected from
each harvesting site. The fruiting bodies were photographed, described
and dried according to Halling (1996). Taxonomic identification of
vouchers was based on macroscopic and microscopic characteristics
using specialized literature and keys reported by Burrola-Aguilar et al.
(2012). The vouchers were deposited in both the National Herbarium
of Mexico and the Research Center of Biotic Resources herbarium of
the Autonomous University of Mexico State.
3. Results
3.1. The survey
The application of 165 questionnaires allowed us to characterize
how people collect, consume and sell edible mushrooms. In 100% of
the housing units we could identify a person who answered the
survey. Twenty-seven (16%) said that no member of the family
harvests edible mushrooms. Despite the great diversity (77 species
reported by Franco-Maass et al., 2012), the local population knows
and consumes, on average, no more than six species, and only 18
families stated knowledge of 10 or more different edible mush-
rooms. Most of the families (64.2%) harvest mushrooms for self-
consumption; a few of them (8.5%) sell the surplus in regional mar-
kets (Table 6).
Most of the people harvested the mushrooms for self-consumption
(106 families harvested 5453.5 kg); 32 families harvested into three cat-
egories a) for sell, b) for self-consumption and sell, and c) for sell and self-
consumption; a total amount of 8128 kg (Table 6). On average, the fami-
lies make 5.3 collection trips per month in groups of three people (Table
7). During the rainy season of 2009, the evaluated families harvested
13,591 kg of edible mushrooms (Table 8). Despite being more people har-
vesting mushrooms for self-consumption, they harvest a lower amount of
mushrooms; in contrast to people harvesting in the three categories
which includes the sale of mushrooms as the main activity, or from the
sale of surplus mushrooms self-consumption. This demonstrates that
the greatest harvest pressure is given by the sale of mushrooms and
their demand in the market and not for self-consumption.
Of the 13 people interviewed, who have a rich knowledge of edible
mushroom distribution; men mainly carry out the harvest of edible
mushrooms in the Nevado de Toluca (Table 8). When alone, they
spend more than 6 h harvesting the most valued species. The collected
amount, however, is lower. It is important to highlight the role that chil-
dren play in harvesting mushrooms. Whereas only 20% of the harvest-
ing is performed exclusively by children, the proportion of children
accompanying the father or mother is significantly larger.
3.2. Application of the model
As expected, proximity to certain forest types exerted a greater influ-
ence on the obtained pressure level value (Fig. 4a). Dense fir forests
were preferred by local harvesters to search for edible mushrooms.
This finding is consistent with the results of Burrola-Aguilar et al.
(2013) in the sense that this kind of forest has greater diversity and pro-
ductivity compared with other coniferous forests in the surrounding re-
gion of Amanalco (State of Mexico).

Table 7
Amount of harvesting per family.

Average number of
Average persons Average months per harvesting trips per Average amount harvested Average amount harvested Families that harvest more
Village per harvesting trip year of harvesting month per family per season (kg) per family per week (kg) than 100 kg per season

1. Agua 2.9 3.6 9.5 182.0 12.8 7

Blanca
2. 3.3 3.0 4.5 114.4 9.5 3
Buenavista
3. Contadero 2.8 3.3 2.9 31.8 2.4 1
4. El Varal 3.7 3.3 7.3 94.0 7.1 2
5. La Peñuela 2.1 3.4 5.9 87.4 6.5 4
6. La Puerta 3.2 4.2 4.1 45.2 2.7 1
7. Loma Alta 3.1 4.9 5.9 78.1 4.0 6
8. Raíces 3.5 3.7 5.5 152.1 10.4 8
9. San 1.5 6.0 3.5 163.5 6.8 1
Román
Average 3.0 3.7 5.3 6.8
246 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250

Table 8
Characteristics of harvesting by family members, amount harvested, and time.

Family members Total harvesters Total amount per season (kg) Average per harvester per season (kg) Average collection trip time (h)

Father alone 18 1326 73.6 6.3

Father leads with family 65 5969 91.8 3.2
Mother leads with family 30 3642 121.4 3.4
Children alone 16 1835 114.7 2.4
Other relatives 9 819 91.0 3.2
Total 138 13,591

3.3. Validation of the model According to our prediction model, more than 19,400 ha of forest
could be under the highest levels of harvesting pressure, representing
The locations of the harvesting sites were compared with the level of 66% of the 29,300 ha covered by conifers in the protected area. The
pressure on the map (Table 9). The higher pressure level is expressed as main forest types under pressure are dense fir and open fir forests
the lower cost of travel in terms of distance, slope and land cover type. (more than 9700 ha) and dense fir-pine forests (4300 ha).
Each factor image was expressed in the 0–255 byte scale and was mul-
tiplied by its factor weight. Since the set of factor weights sum to one, the
3.5. Characterization of edible mushrooms
resulting image had zero as the minimum and 255 as the maximum. The
overlapping of the image with the 193 harvesting sites with the level of
Of the 77 taxa of edible wild mushrooms reported in the Nevado de
pressure image showed that all values obtained for the harvesting sites
Toluca, the highest cultural significance identified in the area was as fol-
were very high. None of the sites had a level pressure less than 230 and
lows: “clavitos” (Lyophyllum shimeji and Psathyrella spadicea),
more than 50% had values very close to the maximum possible.
“enchilados” (Lactarius c.f. sanguifluus and L. luculentus), “patas de pájaro”
This tendency was confirmed by analyses of the tracks followed by
(Ramaria abietina, R. aff. rubribrunnescens, R. aurantiisiccescens and R. aff.
the local harvesters (Table 10). The harvesters preferred fir forests; on
sanguinea), “orejas” (Lactarius scrobiculatus, Russula c.f. chloroides and
average, they travelled a distance of 6.7 km at altitudes of approximately
Hydnum sp.), “panzas” (Boletus cf. aereus and B. edulis), “gachupines”
3261.8 m.a.s.l. (in the development range of that type of forest). Al-
(Helvella lacunosa, H. crispa and H. compressa), “mazorcas” (Morchella
though they reached up to 50 degrees of slope, the mean value was
elata), “tejamaniles” (Clitocybe squamulosa and C. gibba), “calabacitas”
15.1 degrees. The main difference between men and women tracks
(Laccaria trichodermophora), “papitas” (Sarcosphaera sp.), “mantecos”
was that women tended to travel longer distances.
(Amanita novinupta) and “naranjos” (Cantharellus subalbidus).

3.4. Final human pressure map 4. Discussion

Once confirmed that the values obtained for the harvesting sites in the
pressure image were very high, the model was applied considering the 23
villages within the protected region of Nevado de Toluca (Fig. 4b). This
map can be used to define priority areas for the monitoring and conserva-
tion of NWFPs.
4.1. Harvesting of edible mushrooms
The harvesting process by people in Nevado de Toluca is similar at
other sites in Central Mexico. The activity starts early in the day and
the people tend to go to the most accessible places covered by fir forests.

Fig. 4. a) Potential harvesting pressure exerted by the nine villages selected to generate the model and b) Potential harvesting pressure exerted by the 23 villages in the protected area of
Nevado de Toluca.
 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250
People walk for long durations, lasting between 3 and 7 h on steep hills,
slippery floors and often in the rain. They usually follow known foot-
paths, but when they find a colony of mushrooms, they disperse
throughout the area (Mariaca et al., 2001). Unlike that reported by
Matsuura et al. (2014b) in the sense that local experienced harvesters
tend to be old men (with an age in years from the mid-60s to the
early 70s), in the Nevado de Toluca the age of harvesters varies from
32 to 65 years and almost half of them are women.
The harvesting of mushrooms in the study area tended to be led by
men, although women also played a role (Pérez-Moreno et al., 2008).
It was confirmed that harvesting has a strong family and community
spirit that involves the very important participation of the mother and
children (McLain and Jones, 2005; Montoya et al., 2008). When men
are harvesting mushrooms alone, they invested more travel time to har-
vest the most valued species; this behavior is equal to that in other sites
in Central Mexico (Montoya et al., 2008).
When the wife, children or other family members accompanied
the men, time was significantly reduced, and the amount harvested
was increased but became less selective. When the mothers led,
the time invested slightly increased, but the profits increased sig-
nificantly. These findings confirm those reported by Pacheco-
Cobos et al. (2010) in the sense that men tend to travel greater dis-
tances, representing a greater expenditure of energy (Ruan-Soto et
al., 2009). Women and children spend less time on collection,
resulting in higher profits and consistent with the notion that
women have more extensive knowledge of the taxonomy, biology,
and ecology of local mushrooms (Garibay-Orijel et al., 2012).
Unlike the findings of Matsuura et al. (2013) that female harvesters
generally use sites nearer to roads and settlements than male
harvesters, we found that, on average, women tended to travel
longer distances (8.3 km) in comparison to men (5.1 km).
Although harvesting is not very selective, the species with greater
cultural importance in the Nevado de Toluca are Lyophyllum shimeji
(“clavitos”), Psathyrella spadicea (“clavitos”), Lactarius spp.
(“enchilados”), Ramaria spp. (“patitas de pájaro”), Boletus spp.
(“cemitas”), and Helvella spp. (“gachupines”) (San Román, 2014). This
pattern differs from other regions in Mexico. In the State of Tlaxcala,
harvesters prefer Gomphus floccosus, Ramaria spp., and Boletus spp.
(Montoya-Esquivel et al., 2003). In the State of Oaxaca, Cantharellus
cibarius, Amanita caesarea and Ramaria spp. are preferred (Garibay-
Orijel et al., 2007). In the region of Amanalco, which is not very far
from Nevado de Toluca (Amanalco), the people mention Helvella crispa,
H. lacunosa, H. sulcata (“gachupines”), Amanita caesarea (“tecomates”),
and Lyophyllum decastes (“clavitos”) (Burrola-Aguilar et al., 2012).
Local harvesters in Nevado de Toluca prefer to harvest mushrooms
in dense fir forests. These data reflect the diversity of species, and fir for-
ests represent the region with the highest fungal diversity
(Villareal-Ruiz and Pérez-Moreno, 1989; Arteaga and Moreno, 2006;
Burrola-Aguilar et al., 2013). According to the harvesting track informa-
tion, harvesters remain within the altitude range of fir forests. In con-
trast, Montoya et al. (2008) have indicated that harvesters tend to go
further and further in the field as the season progresses and various
mushrooms appear. At the beginning of the season, their search is lim-
ited to the plains and the Pinus and Pinus-Alnus forests; later, they ex-
tend their search to the Abies forests located at higher altitudes (3600
m).
Local harvesters have demonstrated an understanding of edible
mushrooms' probable distributions in the regional forests. Local knowl-
edge can play a complementary role with expert and scientific knowl-
edge to define conservation strategies (Chalmers and Fabricius, 2007).
In addition, there are important social and economic factors to establish
the cultural scheme regarding knowledge of fungal resources (Ruan-
Soto et al., 2009). The most frequent and most abundant species are
not always the most culturally important (Pacheco-Cobos et al.,
2015); thus, their abundances and prices are related to cultural impor-
tance (Montoya et al., 2014).
247
4.2. Harvesting pressure model
In this study, we demonstrated a procedure to integrate local knowl-
edge into a GIS-MCE model that can be used to map the harvesting pres-
sure using land cover, elevation models and road networks. The maps
can then be used to define areas to monitor the collection of edible
mushrooms. This model may be considered a starting point for environ-
mental protection planning. It can be applied not only to the protected
area of Nevado de Toluca but also to temperate forests in central Mexico.
However, it must be applied within the framework of local harvester
consultation. It is important to recognize that local preferences can
vary according to the cultural, ethnic, or economic characteristics of
the local population (Phua and Minowa, 2005).
Few studies have considered the use of local knowledge in a GIS en-
vironment to analyze the spatial characteristics of the habitat distribu-
tion and harvesting sites of a variety of NWFPs. According to Yang et
al. (2006), incorporating local expert knowledge into a GIS expert sys-
tem can provide better-informed management decisions in terms of
the identification of mushroom habitats. Matsuura et al. (2014b) dem-
onstrated the possibility of using local knowledge to identify and char-
acterize the harvesting sites of edible ferns within a GIS-MCE
environment in Japan. Local harvesters demonstrated a great under-
standing of edible mushrooms and their probable distribution in the re-
gional forests (Chalmers and Fabricius, 2007).
According to Store and Jokimäki (2003), one of the advantages of
using GIS-MCE based approaches is the possibility of integrating empir-
ical models and expert knowledge. The same can be said when integrat-
ing local knowledge into the model.
The land cover criterion used in the present study is not only the
most important criterion for local harvesters but also the most cited in
the literature (De Miguel et al., 2014; Martínez de Aragón et al., 2007;
Mumcu and Zeki, 2015; Yang et al., 2006; Yang et al., 2012). As a part
of the local knowledge approach, GPS tracks followed by local har-
vesters were used to analyze the routes of mushroom collection and
to locate the harvesting sites. GPS tracks have been used as mapping
tool to estimate the distribution of NWFPs (Matsuura et al., 2014b).
During the development and application of the model, several issues
were encountered:
a) Local harvesters were not familiar with some of the criteria, such as
the soil acidity or evapotranspiration.
b) The integration of local knowledge, sometimes with different per-
spectives, into the GIS environment. It was a challenge to translate
the opinion of harvesters to score the factors.
c) Selection of the land cover classification. This process is important
because if it is too simplistic, then information can be lost (Store
and Jokimäki, 2003). In contrast, if the map is very complex, e.g.,
our source map with 125 land cover categories, it can be too difficult
to handle and understand by local harvesters. Consequently, it was
necessary to apply a process of generalization to obtain 10 different
forest categories, apart from shrubs and grasslands.
d) Weight assignment was a difficult task that was based on the objec-
tives of different local harvesters. Weights govern the degree to
which a criterion can compensate for another criterion
(Boroushaki and Malczewski, 2008). It is a case-specific process
that must be performed separately for each area (Store and
Jokimäki, 2003). Local harvesters found it difficult to establish their
preferences in a numerical manner for both the land cover catego-
ries and the decision rule between criteria. Integrating the different
weighting schemes in the local knowledge scope is a subject of inter-
est for further studies and also for other sites to be studied.
e) The sensitivity analysis (SA). There are various methodological ap-
proaches to SA that produce different outcomes (Ligmann-
Zielinska and Jankowski, 2008). The basic method used to examine
the sensitivity of weights involves the performance of different eval-
uations by varying the weighting scheme of the criteria to identify
248 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250

Table 9 studies must be conducted to evaluate the precise distribution and

Pressure level in the harvest sites (frequency groups).
Level of pressure Frequency
230–234.9 16
235–239.9 13
240–244.9 43
245–249.9 66
250–252.5 55
Total 193
changes in the resulting maps (Malczewski, 1999; Green et al.,
1998). The analysis revealed strong confidence in the solution indi-
cating no significant changes. This result was mainly due to the
proximity to certain types of forest exerting a definite influence on
the model. Thus, although there is a possibility of harvesting mush-
rooms from other forest categories, e.g., Flammulina mexicana grow-
ing mainly in open pine forests and shrubland, the local population is
generally not interested in specific species but in quantity.
From a practical perspective, our research is important because it
permits the development of a model for predicting the pressure exerted
by local harvesters. The pressure maps can be used to monitoring mush-
room conservation areas. From a theoretical perspective, we have con-
tributed to the development of methodologies that integrate local
knowledge into a GIS and MCE environment. No studies have focused
on evaluating the use of local knowledge to estimate the harvesting
pressure on edible mushrooms.
Despite its apparent simplicity, the model proved to be useful for
predicting potential harvesting sites with a high level of reliability.
This goal is important in countries such as Mexico, where there is no de-
tailed information about mushroom inventories or forest stand vari-
ables that could permit the application of more complex models
(Martínez-Peña et al., 2012; Mumcu and Zeki, 2015; Yang et al., 2006).
It is also important to consider that the model might be limited com-
pared with the actual distribution of edible mushrooms. Additional
abundance of the mushrooms in regions that are not attractive to
harvesters.
4.3. Conservation strategies
The model developed herein can be used to locate areas with in-
creased harvesting pressure; it may also be used to establish potential
mushroom production sites. These areas can be defined for each com-
munity and be subjected to a special management program with suc-
cessive harvesting schemes; during resting periods, no mushrooms
would be collected in a particular place for one or more seasons
(Gómez et al., 1999; Elith et al., 2006) to facilitate dispersion and
spore production. In addition, mushroom production can be monitored
by observing plots and the annual registration of collections (Gómez et
al., 1999). Alternatively, models can be established to predict the effects
of overexploitation of this resource (De Miguel et al., 2014).
The potential harvesting pressure map (Fig. 4) can be used to define
monitoring plots to determine the characteristics of the vegetation, eco-
logical availability, and species composition (Burrola-Aguilar et al.,
2012). Soil temperature and moisture are also important variables
(physiological responses to soil conditions) (Bonet et al., 2012). Soil
moisture and temperature conditions could contribute to the develop-
ment of predictive models of fungal fruiting to optimize the manage-
ment of harvesting edible mushrooms (Pinna et al., 2010). Another
variable to consider is the effect of exposure on the productivity of
fungi, which increases with an increasing slope (De Miguel et al., 2014).
Together with monitoring, it is possible to train harvesters regarding
the use of appropriate harvesting techniques. It is important to avoid in-
tense and frequent trampling in areas where fungal colonies are known
to be present; to pick manually to avoid damaging the mycelium; and to
avoid cutting, mistreating or stepping on fungi that are not known or
those that are small in size, broken or very mature (Gómez et al.,
1999). The implementation of reforestation programs for edible
ectomycorrhizal species of commercial interest to contribute to the es-
tablishment of fungal colonies at specific sites, will include species

Table 10
Main characteristics of the harvesting tracks.

Harvester
leader Altitude (m.a.s.l.) Slope (degrees) Dominant type of vegetation

Distance Percentage along the

Track Village Sex Age (km) Min. Max. Mean Min. Max. Mean In harvesting sites route

R1 Agua Male 50 5.8 3167.5 3266.6 3220.9 ± 0.0 30.8 11.7 ± 5.3 Dense fir forest 78.6
Blanca 26.9
R2 Agua Male 30 4.4 3220.0 3460.0 3300.9 ± 2.0 36.8 12.9 ± 7.0 Dense fir forest 62.9
Blanca 68.7
R3 Agua Female 35 6.8 3157.3 3296.6 3199.4 ± 0.0 35.2 8.3 ± 6.4 Dense fir forest 35.5a
Blanca 36.7
R4 La Peñuela Male 35 5.9 3020.0 3240.0 3153.1 ± 0.0 48.1 12.3 ± Dense pine forest 42.9a
49.1 11.2
R5 La Peñuela Female 40 7.4 2980.0 3226.6 3107.1 ± 0.0 48.1 16.2 ± Dense fir-pine forest 61.5
76.1 10.1
R6 La Peñuela Female 65 12.1 2946.6 3346.6 3123.7 ± 0.0 54.7 21.7 ± Dense fir forest 76.2
87.7 11.2
R7 Raíces Female 40 7.2 3340.0 3546.6 3432.9 ± 4.1 35.2 13.7 ± 6.2 Dense fir-pine forest & dense pine 71.4
52.0 forest
R8 Raíces Female 35 10.5 3354.5 3560.0 3463.0 ± 0.0 36.8 13.6 ± 7.3 Dense pine forest 70.4
61.5
R9 Contadero Male 32 2.9 2986.6 3175.0 3072.3 ± 0.0 29.2 11.8 ± 5.2 Dense fir forest 40.0a
63.4
R10 La Joya Male 40 4.8 3278.5 3425.7 3357.9 ± 0.0 45.0 18.8 ± Dense fir forest 69.0
37.4 11.1
R11 La Puerta Female 60 5.7 3130.5 3400.0 3259.5 ± 0.0 36.8 14.8 ± 7.0 Dense fir forest 81.2
68.2
R12 Loma Alta Male 65 2.4 3360.0 3500.0 3442.2 ± 0.0 48.2 22.2 ± Dense fir forest 82.0
34.5 10.8
R13 San Male 50 9.8 3034.2 3440.0 3271.4 ± 0.0 36.8 17.7 ± 8.8 Dense fir 48.2a
Román 114.0
a
Harvesters had to travel long distances along other types of land cover to reach the harvesting areas.
 S. Franco-Maass et al. / Forest Policy and Economics 73 (2016) 239–250
such as Laccaria spp., Suillus spp., Morchella spp., Lyophyllum spp., and
Boletus spp., as well as the creation of a gene bank of edible and medic-
inal species (Pilz et al., 2007; Pérez-Moreno et al., 2010).
However, if no action is taken to reverse the population decline of
wild edible mushrooms, then there is an imminent risk of exhausting
these resources by overexploitation, eventually resulting in undesirable
economic, social, and environmental effects. The lack of technical and
scientific guidance concerning the use of natural resources increases
the likelihood of overexploitation or extinction of more traditional spe-
cies and their habitats, resulting in their conversion for agricultural and/
or livestock activities, which do not always lead to social or economic
benefits (Arteaga and Moreno, 2006).
5. Conclusions
According to our findings, local harvesters do not conduct their ac-
tivities for particular target species; they search for the best environ-
mental conditions in terms of the productivity of any kind of edible
mushroom. Therefore, local knowledge of local mushroom populations
could help to determine the most likely harvesting sites of wild edible
mushrooms with reasonable accuracy.
Combining Multi-Criteria Evaluation (MCE) and Geographic Infor-
mation System (GIS) was very useful to characterize the level of pres-
sure of the territory as it allowed to incorporate the perception of the
local population about the geographical distribution of fungi. The results
supported the probability that the harvesters are harvesting edible
mushrooms and not the real abundance of the natural resource.
A better understanding of local population behavior is essential for
natural resource and forest landscape management. Fundamental stud-
ies are required to support the formulation of public policies for the con-
servation of NWFPs, such as the development of regional inventories
based on monitoring and geographical analyses of sites of increased
human pressure (Zamora-Martínez and Segundo, 2010).
Acknowledgements
The authors would like to thank the Institute for Agriculture and
Rural Sciences, Autonomous University of the State of Mexico for the lo-
gistic support. This study was carried out as part of the project “Charac-
terization of forest resources of Nevado de Toluca National Park, and
study of social dynamics that influence their decline”, financed by the
National Council of Science and Technology of Mexico (CONACyT) (CB
2006 CONACYT).
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