Journal of Environmental Management 279 (2021) 111819

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Journal of Environmental Management

journal homepage: http://www.elsevier.com/locate/jenvman

Research article

Timber and non-timber forest products in the northernmost Neotropical

rainforest: Ecological factors unravel their landscape distribution
Armando Navarrete-Segueda a, Jorge Cortés-Flores b, Guadalupe Cornejo-Tenorio a,
M. Lourdes González-Arqueros c, Mariana Torres-García a, Guillermo Ibarra-Manríquez a, *
a
Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua carretera a Pátzcuaro No. 8701. Col. San José de la
Huerta. C. P. 58190. Morelia, Michoacán, Mexico
b
Jardín Botánico, Instituto de Biología, Sede Tlaxcala, Universidad Nacional Autónoma de México, Ex Fábrica San Manuel S/N. Col. San Manuel. C. P., 90640, Santa
Cruz Tlaxcala, Tlaxcala, Mexico
c
CONACYT-Instituto de Investigaciones en Ciencias de la Tierra, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, C. P. 58060, Morelia,
Michoacán, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: The benefits provided by tropical rainforests are unevenly distributed throughout the landscape and are shaped
Biophysical factors by abiotic and biotic components that influence the spatial distribution and functional traits of the species
Functional traits involved. We tested whether environmental stratification of the rainforest in biophysical Landscape Units (LU),
Landscape ecology
defined by topography and soil, is related to the spatial distribution of diversity, abundance and productivity
Plant community diversity and structure
(standing biomass) of tree assemblages that provide potential forest products (PFP). Considering that different
Phylogenetic signal
PFP are associated with specific plant traits, we also tested whether a phylogenetic signal exists among the
species that comprise specific use categories. Non-metric multidimensional scaling ordinations and permuta­
tional analysis of variance were based on the frequency, abundance and productivity of 129 species, the PFP of
which were classified as fodder, food, fuelwood, medicinal, melliferous, ornamental, plywood and timber in 15
plots of 0.5 ha each. We constructed a phylogenetic tree of the studied species and analyzed the phylogenetic
signal strength (D-statistic) among them. The spatial distribution of diversity and abundance of useful species
changes among the LU. Specific PFP can be provided in contrasting habitat conditions, but generally not by the
same species. The PFP categories that presented a phylogenetic signal were associated with wood characteristics
(fuelwood and plywood) and the palatability of the leaves and reproductive structures (fodder). The Moraceae
family was significantly related to fodder and plywood, whereas Meliaceae, Myrtaceae and Sapotaceae were
mostly used for fuelwood. The medicinal species presented convergent traits distributed throughout the phy­
logeny. However, since our study included a broad variety of plant structures, it is possible that phylogenetic
dispersion can change if we consider the specific uses within each category. Our findings show that the as­
semblages of PFP suppliers can be clustered through biophysical units based on soil and topography, and specific
categories of PFP are often supplied by phylogenetically related species. This knowledge is fundamental in order
to incorporate the high diversity of tree species and their potential uses into productive reforestation and
agroforestry programs.

1. Introduction throughout the landscape. The potential harvesting and management of

The tropical rainforest (TRF) is a megadiverse ecosystem that de­
livers a wide variety of benefits to human well-being. These benefits
include both timber (TFP) and non-timber (NTFP; edible fruits, fuel­
wood, ornamental and medicinal plants) forest products (Belcher,
2003), which are provided by tree species that are unevenly distributed
these benefits represents a great challenge that has been widely dis­
cussed (Andersson et al., 2016; Guariguata et al., 2012). However, the
pressures on tropical forests as a result of Anthropocene activities
compel us to seek management options that allow for the persistence of
species diversity, as well as providing benefits to the landowners
(Michon et al., 2007). These alternatives require an ecological

* Corresponding author.
E-mail address: gibarra@iies.unam.mx (G. Ibarra-Manríquez).

https://doi.org/10.1016/j.jenvman.2020.111819
Received 19 June 2020; Received in revised form 5 December 2020; Accepted 6 December 2020
Available online 13 December 2020
0301-4797/© 2020 Elsevier Ltd. All rights reserved.
A. Navarrete-Segueda et al.
knowledge of useful species and their habitat requirements. In general,
however, these data are unavailable (Cornwell et al., 2019; Stroud and
Thompson, 2019).
Although the designation of TFP and NTFP generates artificial
categories for utilitarian (anthropic) purposes, the products that are
clustered in these categories are provided by species for which
distribution and functional traits respond to important ecological and
evolutionary processes (Gaoue et al., 2017). First, the capacity of the
forest to provide these potential forest products (PFP) is directly related
to the diversity and abundance of the species that are the source of these
products (Harrison et al., 2014; Navarrete-Segueda et al., 2017). Second,
according to the hypothesis of non-random plant selection (Moerman,
1979), while the selection criteria of useful species by people are highly
related to the particular traits of each tree species (e.g., high wood
density, production of edible fruits, and secondary metabolites), only
those that have specific traits of interest are likely to be used by humans.
From a phylogenetic perspective, the traits of interest can be the result of
phylogenetic relatedness among useful species at different taxonomic
levels, for example, taxa that belong to the same family or genus
(Ackerly, 2009; Gaoue et al., 2017). However, until now, studies
implementing phylogenetic analysis have focused mainly on medicinal
uses of plants (Rønsted et al., 2012; Yessoufou et al., 2015).
At landscape level, the tree community is structured based on spe­
cific habitat factors such as availability of water, soil nutrients or bio­
logical interactions (Baldeck et al., 2013a). The spatial variation of these
factors generates a mosaic of habitats that can act as a filter for the
establishment and persistence of species and for tree community as­
sembly (Keddy, 1992; Pulliam, 2000). It has been proposed that envi­
ronmental heterogeneity regulates spatial patterns of tree community
ecology (Stein et al., 2014) and productivity in tropical ecosystems (Ali
et al., 2019; Rodrigues et al., 2019). Topographic and edaphic factors
have been widely recognized as regulators of resource availability, as
well as drivers of habitat filtering and tree community assembly (Bal­
deck et al., 2013a, 2013b; John et al., 2007). Topographical features
have been widely used to delineate terrain units that are relatively ho­
mogeneous in terms of topography (e.g., slope, elevation, soil type) and
occur in a contextual position that is recognizable with respect to the
adjacent units. These units have discrete boundaries that coincide with
natural discontinuities (e.g., lithology, topography) and allow for nest­
ing processes that shape environmental components, such as soil prop­
erties and plant community assembly (Evans, 2012; MacMillan and
Shary, 2009). Characterization of the habitat based on landforms that
share topography, lithology and soils should therefore allow identifi­
cation of spatial differences in the diversity and density of useful trees, as
well as identification of the factors that regulate such attributes.
In Mexico, as across the Neotropics, deforestation and land use
change are a real threat to the megadiversity of the TRF (Gibbs et al.,
2010; Laurance et al., 2014). Management measures for maintaining or
increasing forest cover are crucial. The Mexican government has
implemented a program that seeks to encourage agroforestry production
systems that include both timber and non-timber species. A major goal is
to recover one million hectares of forest cover (DOF, 2019). The pro­
gram proposes the inclusion of an agroforestry system in productive
units according to the vocation of each region. However, the introduc­
tion of species, with no knowledge of the landscape diversity and
ecological factors that shape this, may jeopardize the success of such
goals, negatively affecting local biodiversity. Understanding the factors
that regulate the distribution of useful tree species and the possible
phylogenetic relationships among them therefore represents a solid base
for planning and managing TRF diversity and is also a topic of high
ecological and conservation importance.
One area in Mexico with high levels of TRF deforestation is the re­
gion of Los Tuxtlas in the state of Veracruz (Bonilla-Moheno and Aide,
2020). Although a list of useful species for the Los Tuxtlas Tropical
Biology Station is available (Ibarra-Manríquez et al., 1997a) and could
be useful for planning future restoration activities of this forest type, it
2
Journal of Environmental Management 279 (2021) 111819
does not include all the main PFP (e.g., medicinal use), nor the spatial
patterns of abundance and productivity of the species, which would
represent fundamental information for the design of adequate forest
management practices (Campbell et al., 1997; Fortini et al., 2006). This
reserve supports an old-growth forest that has been protected by the
National Autonomous University of Mexico from extractive activities
and it has one of the highest levels of conservation within the region. We
therefore selected this reserve to test whether habitat characterization,
based on soil and topographical attributes, would allow us to identify
differences in the composition, abundance and biomass of useful tree
species among habitats, as well as the factors that regulate these com­
munity parameters. Based on the assumption that each landscape unit
represents a portion of the habitat mosaic that shapes this Neotropical
landscape (Zinck et al., 2016; Zonneveld, 1989), we predicted that soil
and topography variation will determine differences in the abundance,
diversity and productivity of tree species (Evans, 2012; MacMillan and
Shary, 2009), including those that supply PFP.
Furthermore, considering that closely related species tend to exhibit
similarities in different traits, including morphological, life history and
ecological characteristics (Ackerly, 2009; Gaoue et al., 2017), we also
evaluated the phylogenetic signal in different PFP. Community phylo­
genetic analysis has been proposed as an efficient method for comparing
several ecological and evolutionary plant traits at different taxonomic
levels (Teixidor-Toneu et al., 2018). We expected that the phylogenetic
signal would allow us to determine associations among tree species that
supply specific PFP (Garnatje et al., 2017; Hawkins and Teixidor-Toneu,
2017).
2. Methods
2.1. Study area
We carried out the study in the reserve of the Los Tuxtlas Tropical
Biology Station in Veracruz state, Mexico (Fig. 1). The area is part of a
volcanic complex formed in the Neogene and middle Quaternary (<7
Mya), bordered by geological materials from the Holocene (~0.8 Ma)
(Nelson and Gonzalez-Caver, 1992). The climate in the region is tropical
wet with rainfall throughout the year (Af). The annual precipitation is
3928 mm, although there is a decrease in precipitation from March to
May, during which evapotranspiration exceeds precipitation. The study
area is covered by TRF (Bongers et al., 1988). The typical tree species
include Bursera simaruba (L.) Sarg., Cecropia obtusifolia Bertol.,
Damburneya ambigens (S.F. Blake) Trofimov, Dendropanax arboreus (L.)
Decne. & Planch., Guarea glabra Vahl, Poulsenia armata (Miq.) Standl.,
Pseudolmedia glabrata (Liebm.) C.C. Berg., and Pterocarpus rohrii Vahl
(Ibarra-Manríquez et al., 1997b). This 640 ha reserve, located within
the core zone of the biosphere reserve, is immersed in a biophysical
environment that extends beyond the administrative limits of the pro­
tection polygon (Fig. S1A). The reserve has protected this forest from
many detrimental human activities, such as pasture for cattle, logging
and fire for more than 50 years. As such, it is representative of
well-conserved TRF in the region (Fig. S1B).
2.2. Environmental heterogeneity and habitat characterization
We conducted a systematic integration of environmental factors
using the Landscape Units (LU) delimitation (Fig. 1). This was performed
by visual interpretation of the external characteristics of the landscape
forms (Zinck, 2016) using a 1:20,000 scale digital elevation model
(MDE) generated from the contour lines of INEGI (2010). We integrated
climate, geology, geomorphology and soil data for stratification of the
environmental mosaic and of potential habitats.
Five main geopedological LU were differentiated, four of which (LU1
to LU4) are associated with cinder cones (late Tertiary and early Qua­
ternary) that differ in inclination, elevation, microclimate (Table S1)
and soils, which were formed from volcanic ash. These units are (Fig. 1):
A. Navarrete-Segueda et al.
Fig. 1. Location of the study area: A) Relative to Mexican national territory and B) Relative to Veracruz state. C) Main landscape units within the Los Tuxtlas Tropical
Biology Station; plots locations are marked.
i) Piedmont (PD); ii) Low Elevation Slopes Strongly Inclined (LSSI,
10–24◦ slope and <350 m a.s.l.), iii) High Elevation Slopes Strongly
Inclined (HSSI, 10–24◦ slope and >400 m in elevation), iv) Steeply
Dissected Slopes (SDS, 22–35◦ slope range) and v) Lava flows (LF, a
landscape unit associated with volcanic events of the Holocene). The
selected LU represent 75% of the land-forms present on the reserve
surface (640 ha). In each LU, three 20 × 250 m (0.5 ha) plots were
established, covering a total sampled area of 7.5 ha. Estimated inter-site
distances ranged between 400 and 4550 m.
2.2.1. Soil sampling
One soil pit was dug in each plot for soil profile description of each
genetic horizon of the solum (A and B soil horizons) down to the soil
depth to which the plants roots can penetrate (rooting depth) without
major obstacles, for example, a continuous rock layer (Siebe et al.,
2006). We estimated and interpreted the available water retention ca­
pacity for plants (AWHC) for each horizon, according to AG-Bo­
denkunde (2005) and Siebe et al. (2006). The AWHC integrates soil
texture, organic matter content, bulk density, percentage of coarse
fragments and thickness of each horizon estimated in the field. In
addition to the AWHC, we selected the texture, rooting depth and per­
centage of coarse fragments as indicators of nutrient storage and soil
fertility (Bünemann et al., 2018).
2.2.2. Topography
To obtain the abiotic components related to relief, we parameterized
the topographic data pertaining to slope and elevation, based on a
digital elevation model (DEM), with a resolution of 20 m, obtained in
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Journal of Environmental Management 279 (2021) 111819
ArcMap 10.1 (ESRI®). Detailed analysis of the relief showed that some
LU were highly heterogeneous in terms of slope. Thus, although each
plot was integrated to its specific landscape unit, we added the standard
deviation values to incorporate this heterogeneity into the subsequent
analysis.
2.2.3. Tree sampling and characterization of PFP
In each 0.5 ha LU, we recorded all tree individuals with a diameter at
breast height (dbh) ≥ 10 cm in each plot; all individuals were identified
to the species level. We identified PFP reported for each recorded tree
species; the PFP were classified into the following categories (Table S2):
fodder, food, fuelwood, medicinal, melliferous, ornamental, plywood,
paper pulp and timber. For the timber use category, all forms of wood
extraction were considered because, despite the fact that some species
do not develop the wood density required for construction or furniture
production, they are highly appreciated for other uses, such as tool
handles, kitchen utensils or handicrafts. The aboveground biomass
(AGB) of species that provide PFP was estimated using allometric re­
lationships based on wood density (Chave et al., 2005). A detailed
description of this information can be found in the supplementary ma­
terials (Appendix 1).
2.2.4. Phylogeny
We constructed a phylogenetic tree of the study species using the V.
PhyloMaker package in R (R Core Team, 2018), which was derived from
a mega-tree that contains 74,533 vascular plant species and includes all
angiosperm plant families (Jin and Qian, 2019). The species not
included in the mega-tree were bound to the half point of the genus
A. Navarrete-Segueda et al. Journal of Environmental Management 279 (2021) 111819

branch, representing the branch between the genus root node and the
basal node, as recommended by Qian and Jin (2016). To calculate the
phylogenetic signal, each PFP was transformed into a binary character.
The D statistic (Fritz and Purvis, 2010) was implemented with the
‘phylo.d’ function in the “caper” package (Orme et al., 2013) in R. This
algorithm is based on the differences between sister clades of a given
phylogeny. While a clumped trait belongs to the same character state in
related species, an overdispersed trait does not. In this way, the sum of
the differences in the sister clades will be lower than in the clumped
traits. The D-statistic is equal to 1 where the binary traits have a random
phylogenetic distribution, and equal to 0 where the trait is clumped and
has evolved under the Brownian motion model. Values of D can fall
outside this range, indicating that phylogenetic patterns are extremely
clumped (<0) and phylogenetically overdispersed (>1) (Fritz and Pur­
vis, 2010). To visualize the different PFP along the phylogenetic tree, we
plotted the presence or absence of different plant uses on the tips using
the package ‘ggtree’ in R (Yu et al., 2018).
we included abundance in the measure of diversity (1D and 2D), we
found that LSSI was more diverse than HSSI and LF (F 4, 0 = 238.7, P =
0.001; F 4,10 = 223.0, P < 0.001, respectively) (Table S3). Likewise, it
was also observed that this unit, together with PD, had greater evenness
among the LU (F 4,10 = 0.0, P < 0.001) (Table S3, Fig. 1). Tree density
was significantly higher in SDS (F 4,10 = 129.9, P < 0.001), whereas PD
displayed the lower value (Table S3).
On average (±s.e.), a hectare of forest had 429 ± 29 trees, of which
348 ± 20 (81% of the total) provided at least one PFP, representing an
AGB of 322 ± 19.06 t ha− 1 and a species richness of 49 ± 2 species per
0.5 ha. Most species were used for medicinal purposes (89 species, 69%
of the total number of species providing PFP) followed by use for timber
and fuelwood (54 and 44 species, respectively). A large proportion of
timber species (83%) also supply NTFP (Table S2). Interestingly, the
number of species did not differ among LU for all use categories (Fig. 2).
In contrast, we did find a difference in tree density among LU. Tree

2.3. Data analysis

Using data of the number of individuals and species per PFP cate­
gory, we obtained mean (±s.e.) values of density and effective number
of species (0D, 1D and 2D), as indicated by Jost (2006). We applied
generalized linear models and performed multiple means comparisons
to assess differences in biotic and abiotic components, structure and
diversity of tree community among LU, using the ‘multcomp’ package in
R.
We constructed rank curves based on abundance and AGB to assess
changes in dominant tree species among LU (lumping data of the three
plots per unit). These curves were constructed following Magurran
(2013). Linear models were fitted for rank abundance and AGB curves
and differences between LU were tested using an analysis of covariance
(ANCOVA), considering rank (Rank; as numeric) as an explanatory
variable and Landscape Unit (LU; as categorical), as well as their
interaction (Rank: LU). Differences in slopes were evaluated among the
LU (Izsák, 2006).
The LU-related effects on tree community structure and diversity
were analyzed by means of a permutational multivariate analysis of
variance (PERMANOVA) (Anderson and Braak, 2003), using the
Bray-Curtis dissimilarity. This analysis is especially useful to the
partitioning of multivariate data in response to complex designs (e.g.,
LU) under ordinal or qualitative data (e.g., use category assigned to
species), in which the variables consist of abundance, frequency or
biomass (Anderson, 2017); P-values were obtained using 9999 permu­
tations. Finally, we performed a Nonmetric Multidimensional Scaling
(NMDS) analysis to examine the multivariate relationship among the
structures of the useful tree species based on presence, abundance and
productivity (i.e., AGB) data, with the environmental factors
(topography, microclimate and soils) of the LU. We implemented NMDS
with Bray-Curtis dissimilarities for abundance and AGB, and with the
Jaccard method for presence-absence data (Oksanen et al., 2019). Since
NMDS uses rank order information (Tong, 1992), this technique repre­
sents a highly flexible method with which to explore the proximities and
resemblances of the selected tree community parameters (Rabinowitz,
1975). We applied a minimum variance method to represent the ellipses
produced by clustering community parameters. The analyses were
conducted using the ‘vegan’ package in R.

3. Results
3.1. Diversity and abundance of useful tree species
A total of 179 tree species were recorded across the studied plots, of
which 72% (129 species) had PFP (Table S2). No significant differences
were found in species richness (0D) and biomass among LU (F 4, 0 = 9.7,
P = 0.092; F 4,10 = 58431.0, P = 0.5488, respectively). However, when
Fig. 2. A) Species richness, B) Assemblage density, and C) Aboveground
biomass of tree assemblages with potential forest products (PFP) in the Los
Tuxtlas Tropical Biology Station, Mexico. Ti (timber); Fo (food); Fw (fuelwood);
Fd (fodder); Me (medicinal); Mf (melliferous); Or (ornamental); and Pw
(plywood). Mean ± S.E. values (n = 3 per LU) for each structural attribute, LU,
and PFP are shown; bars with distinct lowercase letter within each PFP differ
significantly (P < 0.05).

4
A. Navarrete-Segueda et al.
density for the fodder category was significantly higher in LF than for all
other categories; this category of use presented the lowest tree density in
LSSI (F 4,10 = 102.7, P < 0.001). In turn, LF and SDS shared the highest
tree density values for the categories of food, plywood and timber (F 4,10
= 84.1, P < 0.001; F 4,10 = 30.9, P < 0.001; F 4,10 = 89.8, P < 0.001,
respectively). We found that trees of the fuelwood category had higher
AGB in LF and HSSI than in PD and LSSI (F 4,10 = 7054.2, P < 0.002),
following a pattern similar to the tree density among these units (Fig. 2).
Trees with medicinal, fuelwood and timber products exhibited the
highest density of individuals and overall AGB among the LU.
3.2. Spatial distribution of species composition and its effects on PFP
availability
Most of the species that provide PFP were registered in one category
only (56; 43.4%), while all of the other species had two to seven PFP
categories. The species with the highest number of PFP categories
recorded were Alchornea latifolia Sw. and Brosimum alicastrum Sw. with
seven uses each, followed by Bursera simaruba and Cecropia obtusifolia
with six PFP. Several species fell into 4 and 5 categories (Table S2).
Among the species with the highest number of potential uses, only
Dendropanax arboreus, C. obtusifolia and A. latifolia showed a wide
spatial distribution (recorded in 87, 67 and 53% of the plots, respec­
tively). Most of the species providing PFP (62%) had a narrow distri­
bution (≤40% of the plots).
We found significant differences between the LU curves with con­
trasting topography (Fig. 3; Table S4), since the HSSI curve differed from
the LSSI and PD curves (F1 = 12.9, P < 0.000 and F1 = 17.6, P < 0.001,
respectively). The rank abundance curves differed significantly between
LF and PD (F1 = 5.1, P = 0.025), while the LSSI and PD curves showed no
difference (F1 = 0.34, P = 0.562). In particular, the SDS curves did not
differ from those of HSSI (F1 = 2.31, P = 0.135) and LF (F1 = 0.33, P =
0.565) (Table S4). It was also found that the rank biomass curve of the
SDS differed significantly from those of HSSI (F1 = 35.29, P < 0.000) and
LF (F1 = 15.41, P < 0.000) (Fig. 3; Table S4). The rank-biomass curve of
LF differed from those of PD (F1 = 6.04, P = 0.015) and LSSI (F1 = 8.54,
P = 0.003).
3.3. Response of useful tree species to environmental factors
We noted distinct shifts in tree assemblages among LU. The species
Fig. 3. Species-rank curves based on species abundance and aboveground biomass for tree assemblages supplying Potential Forest Products (PFP) in the Los Tuxtlas
Tropical Biology Station. The top five species providing PFP are shown in each case. Curves correspond to each of the five study landscape units: High Elevation
Slopes Strongly Inclined (HSSI), Low Elevation Slopes Strongly Inclined (LSSI), Lava Flows (LF), Piedmont (PD) and Steeply Dissected Slopes (SDS).
5
Journal of Environmental Management 279 (2021) 111819
ordinations were consistent, grouping LF sites while separating them
from HSSI and SDS sites (Fig. 4). We found that 15% of the variation of
useful tree species presence was explained by relief elevation (F 1,14 =
2.31, P = 0.006) (Table S5). Soil rooting depth (F 1,14 = 1.89, P = 0.032)
and elevation (F 1,14 = 1.83, P = 0.041) both affected the species
abundance, accounting for 24% of variation. The soil and topography
variables included in the analysis did not a have significant effect on the
AGB of useful species (Table S5).
3.4. Phylogenetic signal of the PFP in the tree community
The tree species in the fodder and plywood categories of use showed
the highest phylogenetic signal values (i.e., these PFP were more similar
in the most phylogenetically related species), followed by those in the
fuelwood category. We detected no phylogenetic signal for the mellif­
erous, ornamental, medicinal, timber and food categories (Table 1;
Fig. S2).
4. Discussion
Here, we show that the systematic integration of biophysical com­
ponents through the delimitation of LU provides a spatially explicit
assessment of tree species assemblages providing potential forest prod­
ucts. It also allowed us to identify the components of environmental
heterogeneity that shape species diversity, abundance and biomass
throughout the landscape. Moreover, we show that specific PFP can be
provided in contrasting habitat conditions, although generally not by
the same species. The PFP categories that showed a phylogenetic signal
are associated with wood characteristics (fuelwood and plywood) or
palatability of the leaves and reproductive structures (fodder). In
contrast, medicinal use was a convergent trait distributed throughout
the community phylogeny.
Our results corroborate the findings of Quijas et al. (2010) regarding
the correlation between high TRF diversity and the number of species
with PFP. Although deforestation rate has diminished this TRF by ~90%
in Los Tuxtlas region (Bonilla-Moheno and Aide, 2020), the forest found
in the study area has high conservation value. In addition to biological
diversity, it has a higher tree species richness and density of individuals
with PFP per unit area than the TRF of the Lacandon forest, which is one
of the most diverse and best conserved in Mexico (Navarrete-Segueda
et al., 2017).
A. Navarrete-Segueda et al. Journal of Environmental Management 279 (2021) 111819

Fig. 4. NMDS ordinations for useful tree species in five landscape units. A) Presence. B) Abundance. C) Aboveground biomass.

biocultural diversity associated with the Los Tuxtlas TRF (Gaoue et al.,
Table 1
2017; Nortje and van Wyk, 2019).
Test for phylogenetic signal in potential forest products using the D-statistic in
the Los Tuxtlas Tropical Biology Station. Probabilities (P-values) indicate
whether the observed D-statistic differs significantly from 0 (Phylogenetic 4.1. Spatial variation of PFP
signal) and from 1 (random). Values of D > 1 indicate overdispersed phyloge­
netic patterns and <0 indicate extremely clumped phylogenetic patterns. Values As expected, the LU based on soil and topography allowed us to
in bold indicate the presence of a phylogenetic signal.
identify differences among tree assemblies that provide PFP in the Los
Potential Forest Products Estimated D P (D > 0) P (D < 1) Tuxtlas TRF. This variation was shaped by changes in species
Fodder ¡0.33 0.73 <0.001 composition and tree densities across the volcanic landscape. These
Food 0.54 0.01 0.003 results coincide with those of other studies showing that the availability
Fuelwood 0.15 0.25 <0.01 of PFP present an uneven distribution at the landscape level (Campbell
Medicinal 0.87 0.18
et al., 1997; Fortini et al., 2006; Navarrete-Segueda et al., 2017).
<0.001
Melliferous 1.07 0.006 0.57
Ornamental 0.93 0.01 0.34 However, we found that PFP landscape distribution can be related to
Plywood 0.20 0.30 <0.001 specific habitat mosaics, for instances, fodder tree density was higher in
Timber 0.76 0.05 0.15 LF, whereas medicinal trees were considerably more abundant in SDS.
It is interesting that SDS and LF share high tree densities in the food,
plywood and timber categories even though they present contrasting
The fact that more than half of the 179 tree species recorded had at
mosaics of soil and topography (Table S1). This result shows that PFP
least one PFP use supports Ibarra-Manríquez et al. (1997a) and studies in
can be found in contrasting habitat conditions, albeit provided by
other Neotropical and Pantropical forests (Dattagupta et al., 2014;
different species. For example, Croton schiedeanus and Pouteria durlandii
Navarrete-Segueda et al., 2017). Our results also confirm previous
can provide fuelwood and both species were registered in four LU (not in
studies that show that most timber species are also providers of other
LF), while B. alicastrum, which can provide the same resource, was not
NTFP (Herrero-Jáuregui et al., 2009, 2013; Navarrete-Segueda et al.,
found in HSSI and SDS. Therefore, redundancy in the supply of PFP can
2017). However, we found that medicinal use was the PFP category with
be attributed mainly to variation in species composition among the LU.
the highest number of species, in contrast to the study by Nav­
Another important factor is the difference in species responses to envi­
arrete-Segueda et al. (2017), in which this use category was found to be
ronmental habitat conditions, as in LF and SDS, where acquisition and
in second place, below the timber species. The large number of medic­
storage of soil resources, required for edible fruit production or standing
inal species registered was supported by previous studies carried out by
biomass accumulation (Laurance et al., 1999; Xia et al., 2020), can vary
Mendoza-Márquez (2000, 2004) and is an indicator of the great
among species (Asner et al., 2016; Wright et al., 2004).

6
A. Navarrete-Segueda et al.
The fact that no significant differences were found in richness among
LU can be explained by a high proportion of species that can supply two
or more products, which can act to blur the measurements of variation of
diversity (0D, 1D, and 2D) among LU (Navarrete-Segueda et al., 2017).
On the other hand, Cao and Hawkins (2019) indicate that the effective
number of species measurements may not improve the interpretation of
how species diversity responds to environmental conditions. Our results
confirm the effectiveness of rank abundance curves as an efficient in­
dicator of the structure of tree assemblages providing PFP, which can be
related to habitat environmental factors in TRF (Foster and Dunstan,
2010; Izsák and Pavoine, 2012; Magurran, 2013). This analysis provides
additional insight into the main useful species within the assemblage
providing PFP that would not be evident by changes in diversity mea­
surements alone.
The contemporary plant composition and distribution of the
Neotropical forests is strongly affected by pre-Columbian impact
(Watling et al., 2018) due to their role as important sites of ancient
human occupation (Caetano-Andrade et al., 2020). Whatever the legacy,
it is a fact that current TRF diversity is structured by species responses to
environmental filters (e.g., soil and topography variables) at multiple
scales (Denslow et al., 2019). Furthermore, the presence of pioneer
species in the LU such as Cecropia obtusifolia, Piper hispidum and Siparuna
thecaphora indicate the role of treefall gaps in species distribution across
the landscape (Popma et al., 1988). The ordination shows that the
presence, abundance and AGB of species providing PFP are distributed
heterogeneously across the landscape, as is also evidenced by the rank
species curves. These results show that the spatial distribution of the
PFP-providing tree species community was filtered by soil-topography
in LU. Although the selected variables had low predictive power, the
LU nest variation of the multiple biophysical factors (soils, topography,
parent material, and tree assemblages) affects the ecosystem processes
and properties that derive the species distributions and their abundances
(Chapin, 2003; Zinck et al., 2016; Zonneveld, 1989). Finally, the vol­
canic landscape environment of Los Tuxtlas shows similarities with
other Neotropical volcanic landscapes, in which the diversity and
structure of vegetation responds to soil-topography variation (Clark and
Clark, 2000; Denslow et al., 2019). Consequently, the distribution of the
species that provide the PFP would be expected to follow a similar
pattern.
4.2. Phylogenetic signal of the PFP in the tree community
We found that three of the eight PFP are shared between species that
are phylogenetically closer. It is important to point out that, even if the
PFP categorization is a human classification constructed from local
communities’ knowledge (Dattagupta et al., 2014; Ibarra-Manríquez
et al., 1997a), the plant uses are selected from physical or sensory
characteristics such as the shape, color, taste and smell of different
structures (Gaoue et al., 2017), which can be considered in ecological
studies as functional attributes. The PFP categories that showed a
phylogenetic signal are associated with morphological characteristics of
the tree trunks (fuelwood and plywood) and palatability of the leaves,
flowers, fruits and seeds (fodder). These structure-function relationships
represent a criterion for identifying useful species (Gaoue et al., 2017)
and are consistent with studies in which the morphological and chemical
characteristics of plant structures were shown to be closely related to the
evolutionary history of the species (Ackerly, 2009; Chave et al., 2009;
Rønsted et al., 2012).
Our results confirm the findings of Nortje and van Wyk (2019), who
indicated that plant families show different patterns of use depending on
the use category. In the Los Tuxtlas TRF, fodder and the plywood uses
are mainly related to Moraceae (Fig. 3, Table S2), which is characterized
by presenting palatable seeds and fruits, as well as a medium wood
density (Vázquez-Torres et al., 2010; Zanne et al., 2009). Similarly,
Meliaceae, Myrtaceae and Sapotaceae comprise the tree species most
used for fuelwood (Table S2). These families are characterized by a
7
Journal of Environmental Management 279 (2021) 111819
medium wood specific gravity (0.5–0.7 g/cm3; Chave et al., 2006),
which is considered optimal for fuelwood.
Like Yessoufou et al. (2015), we found that medicinal PFP are
convergent traits distributed throughout the phylogeny. This lack of
phylogenetic signal could be attributed to the fact that we classed all of
the possible medicinal uses into a single category. However, there is a
wide variety of pharmacological properties associated with numerous
metabolites and the plant structures that produce them (Ghorbanpour
et al., 2017). According to Mawalagedera et al. (2019) and Teix­
idor-Toneu et al. (2018), it would be expected that pharmacological
properties were the product of closely related plants. Therefore, it is
possible that phylogenetic pattern changes if we consider the specific
pharmacological applications (e.g., anti-inflammatory, laxative, anes­
thetic, antioxidant, antipyretic, etc.) within the medicinal category.
Finally, timber and food trees showed a pattern of phylogenetic
over-dispersion, indicating that the use of different species belonging to
different genera, families and orders. These findings must be interpreted
with some caution since the observed phylogenetic patterns can change
depending on the degree of knowledge of plants and their potential uses.
However, our results provide important information for the conserva­
tion of tree species, when we consider the position of clades on the
phylogeny and the intensity of species use.
4.3. Concluding remarks
The results of the present study show that the habitat mosaic that can
be related to the useful tree species assemblage is not randomly
distributed in this Neotropical rain forest, and that such variation can be
captured through soil-topography based l LU. We also demonstrated that
there are important PFP, such as fuelwood, fodder and timber, that show
a phylogenetically clumped pattern. The families identified are repre­
sented by species that are constrained to specific habitats, as well as
species of broad distribution and multiple PFP usage.
It is important to take into account the fact that we did not analyze
the anthropic factors that influence the success of management of the
forest tree species and their wide variety of products (Arnold and Pérez,
2001; Panayotou and Ashton, 1992), factors that can hinder the success
of TRF management practices (Andersson et al., 2016; Guariguata et al.,
2012; Herrero-Jáuregui et al., 2013). However, from an ecological and
phylogenetic perspective, our results indicate that tree species
management should consider the spatial landscape variation of the
selected species.
It has also been suggested that landscape management oriented to­
wards maintaining the multiple forest services and species richness
could be designed as tree-dominated mosaics, which can be imple­
mented on forest edges or in forest fragments immersed within inten­
sively produced agroecosystems (Michon et al., 2007; Arroyo-Rodríguez
et al., 2020; Knoke et al., 2020). Our study shows that, since the overall
distribution of sites in species ordinations fits the pattern of LU distri­
bution, these tree-dominated mosaics could be designed based on bio­
physical patterns, which are not aligned to any political or
administrative limits.
Credit author statement
Armando Navarrete-Segueda, Conceptualization, Methodology,
Formal analysis, Research, Data curation, Visualization, Writing –
original draft, Project administration. Jorge Cortés-Flores, Conceptual­
ization, Formal analysis, Writing – review & editing. Guadalupe
Cornejo-Tenorio, Data curation. Mariana Torres-García: Data curation.
Lourdes González-Arqueros: Methodology, Data curation. Guillermo
Ibarra-Manríquez: Conceptualization, Methodology, Data curation,
Writing – review & editing, Supervision, Project administration.
A. Navarrete-Segueda et al.
Declaration of competing interest
The authors declare no known competing financial interests or per­
sonal relationships that could have influenced the study reported in this
paper.
Acknowledgements
A.N.S thanks DGAPA-UNAM (Dirección General de Asuntos del
Personal Académico – Universidad Nacional Autónoma de México) for
the award of a postdoctoral fellowship grant. Santiago Sinaca-Colín,
Santiago Xolo and Armando Xolo, Iván Leonardo Ek-Rodríguez, Katia
Vianney Miranda-Gallegos and Estefanía Elizabeth Acosta-Pérez helped
with the fieldwork. The authors want to thank the staff of the Los Tuxtlas
Tropical Biology Station, especially Rosamond Coates, for all of the fa­
cilities provided during the fieldwork. The English translation was
reviewed by Rosamond Coates and Keith MacMillan. Finally, three re­
viewers provided useful comments that improved the manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.jenvman.2020.111819.
Funding sources
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
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