Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(4): 1189-1203, October-December 2021 (Published Nov. 17, 2021)
Tree structure and diversity of a Humid Mountain Forest in
the protected natural area La Martinica, Veracruz, Mexico
Rosa Lina López-Álvarez1; https://orcid.org/ 0000-0002-2543-0694
Mario Luna-Cavazos1*; https://orcid.org/0000-0003-1672-8154
Juan Ignacio Valdez-Hernández2; https://orcid.org/0000-0002-9488-2790
Edmundo García-Moya1; https://orcid.org/0000-0003-1100-8553
1. Posgrado en Botánica, Colegio de Postgraduados, Campus Montecillo, México; lopz.lina@gmail.com,
mluna@colpos.mx (*Correspondence), edmundo@colpos.mx
2. Posgrado en Ciencias Forestales, Colegio de Postgraduados, Campus Montecillo, México; ignaciov@colpos.mx
Received 04-V-2021. Corrected 08-X-2021. Accepted 04-XI-2021.
Introduction: The Humid Mountain Forest (HMF) has the highest number of plants per unit of surface, whose
vegetation grows under heterogeneous environmental conditions and possess a high floristic variation. HMF
conservation is important due to the biodiversity it harbors and the environmental services it provides.
Objective: This work evaluated the effect of the terrain aspect and density of the forest canopy on the structure
and tree diversity in La Martinica Protected Natural Area, Mexico.
Methods: Stratified sampling was performed in four terrain aspects and two canopy density conditions. Twenty
five sampling units of 20 x 25 m were considered, in which the normal diameter (ND), total height and the
largest and smallest diameters of the crown of the individuals with a ND ≥ 10 cm were registered. The diversity
was estimated by rarefaction curves and the structure was analyzed through the importance value index (IVI)
and the forest value index (FVI).
Results: 37 species belonging to 30 genera and 24 families were recorded. Greater diversity was observed in
the north terrain aspect and in the closed canopy. Tree species with the highest structural values were different
between terrain aspect and canopy types; Carpinus tropicalis presented the highest values in the zenithal terrain
aspect, Lippia myriocephala in the east and south terrain aspect, and Liquidambar styraciflua in the north. In
both canopy types Lippia myriocephala obtained the highest IVI values and FVI in the open canopy; Carpinus
tropicalis reached a higher FVI in the closed canopy.
Conclusions: Tree structure was different in the four terrain aspects and two canopy conditions studied. The
greatest difference in species composition and diversity was observed between the north and east terrain aspects;
the north presented the highest richness values, frequent and dominant species.
Key words: canopy opening; effective number of species; NMDS; terrain aspect; tree vegetation.
López-Álvarez, R. L., Luna-Cavazos, M., Valdez-Hernández, J.
I., & García-Moya, E. (2021). Tree structure and diversity
of a Humid Mountain Forest in the protected natural area
La Martinica, Veracruz, Mexico. Revista de Biología
Tropical, 69(4), 1189-1203. https://doi.org/10.15517/rbt.
The Humid Mountain Forest (HMF) is one
of the most important biomes in Mexico, has a
great richness of flora and endemic species, due
to the great variety of habitats and the restricted
to a small geographical area (Cruz-Cárdenas
et al., 2012; González-Espinosa et al., 2011);
its vegetation harbors the largest number of
species per unit area (Gual-Díaz & Rendón-
Correa, 2014; Gual-Díaz & Rendón-Correa,
2017; Villaseñor, 2010). At the national level,
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(4): 1189-1203, October-December 2021 (Published Nov. 17, 2021)
the humid mountain forest is one of the most
threatened ecosystems (González-Espinosa et
al., 2012; Toledo-Aceves et al., 2011), due
to its scarce distribution and the alterations
caused by global climate change, deforesta-
tion, the expansion of human communities to
mountainous areas where this forest persists,
and changes in land use due to conversion to
crop systems (Cayuela et al. 2006; González-
Espinosa, et al., 2011; Gual-Díaz & Rendón-
Correa, 2017).
The Humid Mountain Forest has also
been described as cloud forest and mountain
cloud forest (Rzedowski, 2006). It develops
between 800 and 3 000 m above sea level, in
the mountainous regions of Mexico, on the
slopes where the humid winds that come from
the sea affect, and generally between 1 000 and
3 000 m of altitude (Villaseñor, 2010) to the
windward of mountain massifs, where moisture
condenses and fogs form, as well as in ravines
and humid slopes (Challenger & Soberón,
2008; Rzedowski, 2006; Villaseñor, 2010). The
HMF is characterized by having a very dense
tree canopy, which limits the passage of light
to the lower strata (Challenger & Soberón,
2008; CONAFOR & COLPOS, 2014). Its
vegetation develops in very heterogeneous
climatic, altitudinal and edaphic conditions and
the orographic and local humidity conditions
that characterize it, originate a wide structural
variability in the form of various associations
that differ from each other in height, phenology
and dominant species (Gual-Díaz & Rendón-
Correa, 2014; Rzedowski, 2006). In addition,
HMF contains floristic elements of different
biogeographic affinity whose presence creates
a great opportunity to evaluate the relationships
among factors as climate, microenvironment,
changes in vegetation structure, and its floristic
composition (González-Espinosa et al., 2011;
Guerrero-Hernández et al., 2019).
Slopes facing north, in the northern hemi-
sphere, tend to be more humid, which benefits
different plant species; unlike south-facing
slopes which receive more solar radiation and
tend to be drier and warmer (Holland & Steyn
1975; Mata-González et al., 2002; Renaud et
al., 2011), thus the aspect is a factor that can
modify, at a local level, essential variables of
plant functions, such as the quantity and qual-
ity of incident radiation, temperature or frost
frequency (Torres et al., 2012). The foregoing
affected, for example, the presences of HMF
patches studied by Luna-Vega et al. (2007),
one oriented to the north and the other to the
southwest, in which these authors found differ-
ences in ecological attributes as the number of
individuals per ha, basal area (m2/ha), species
richness, crown cover and normal diameter.
It is important to mention that these ecologi-
cal attributes have a differential impact on the
structure and diversity of the HMF in different
environments. Williams-Linera et al. (2013) in
a study of the HMF (which they call Cloud For-
est) of central Veracruz, they mention that these
types of forests located at low altitudes are
less diverse, and more similar in composition,
unlike forests located at higher elevations, but
not found differences in the structure of vegeta-
tion in forests located at different altitudes.
Santana et al. (2014), analyzed the biodi-
versity and structure in fragments of the HMF
(described as Bosque Mesófilo de Montaña) of
Michoacán, México; the authors mention that
diversity, similarity, and structure demonstrate
significant heterogeneity in HMF fragments.
García-De la Cruz et al. (2013) mention, that
the alpha diversity of one of the studied sites
for a mountain cloud forest of Veracruz, Méxi-
co, was significantly higher than the other two
sites; similarly, the plant structure between sites
was different, which was attributed to the man-
agement history and natural disturbances that
favor the establishment and development of
different species. Luna-Vega et al. (2007) car-
ried out a structural analysis of two fragments
of mountain cloud forest of the Trans-Mexican
Volcanic Belt; the authors refer that the two
sites have densities of 740-1 720 individuals
per hectare, differ in basal area, and foliage
coverage. García-Franco et al. (2008) analyzed
the vegetation of the Mountain Cloud Forest in
three sites in the center of Veracruz, Mexico;
the authors mentioned that there were no sig-
nificant differences for basal area between
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(4): 1189-1203, October-December 2021 (Published Nov. 17, 2021)
sites; in addition, the greatest floristic differ-
ences were found between sites further away
from each other. Based on the aforementioned,
the close relationship that exists between the
ecological attributes mentioned above with the
structural characteristics and diversity of the
HMF can be observed. In the case of the HMF
located at west of Xalapa, Veracruz, Williams-
Linera et al. (2002) pointed out that the best
conserved forests are on very steep slopes, fac-
ing north, while the disturbed forests they are
located mainly to the south facing slopes.
The conservation of the HMF is important
for the biodiversity it encloses and for its con-
tribution to the maintenance of environmental
regulation services (CONAFOR & COLPOS,
2014; Manson, 2017; Williams-Linera, 2007).
Nevertheless, in the central region of Veracruz
this biome is fragmented. The edges of the
remnants experience changes in physical con-
ditions, such as variations in the microclimate
and, they are under pressure from the expan-
sion of urban settlements (Williams-Linera et
al., 2002; Williams-Linera, 2007).
Williams-Linera et al. (2002), report that
the Humid Mountain Forest of the central Vera-
cruz, Mexico, has been considerably reduced
since the 1960s due to the transformation of
the forest for pastures and crops, along with
urban growth. Deforestation processes con-
tinue in this area (Williams-Linera et al., 2007),
so the HMF is at risk. The PNA La Martinica
is located within the aforementioned area, so it
is subject to the same problems already men-
tioned. Among the various actions to reduce
the deterioration of the HMF, it has been pro-
posed to register the conditions and changes in
the environment necessary to prevent negative
impacts on the forest conservation; also, enrich
the knowledge of the identity and distribution
of the region’s biodiversity (Williams-Linera
et al., 2007). The HMF of the central region of
Veracruz is highly fragmented, La Martinica is
one of the few remnants that are under protec-
tion in order to be preserved, its importance
lies in its value as a reserve of biological diver-
sity and it is of great significance to maintain
environmental services such as the regulation of
water resources (Williams-Linera et al., 2007).
We consider that our study contributes to
the knowledge of the current state of the tree
vegetation in this important area of HMF in
the center of Veracruz state, with which we
can generate proposals for the conservation of
the tree diversity of this region. Based on the
above, the aim of this work was to evaluate the
influence of terrain aspect and canopy density
on the structure and diversity of tree vegetation
in the Humid Mountain Forest at the natural
protected area La Martinica, Banderilla, Vera-
cruz. We asked the following questions: (i) do
terrain aspect influence structure, diversity and
tree species composition? (ii) do canopy densi-
ty influence structure, diversity and tree species
composition? As hypotheses, we assumed that:
(i) structure, diversity and tree species compo-
sition is different between terrain aspects and
particularly north aspect has a positive influ-
ence on them (ii) closed canopies have a posi-
tive influence on structure, diversity and tree
species composition.
Study Area: The study area is locat-
ed in the Natural Protected Area (NPA) La
Martinica, Banderilla, Veracruz, Mexico (Fig.
1), between 19°35’01.3’’-19°35’27.9’ N &
96°56’52.7’’-96°57’30.4’ W. The site was a
private property where extensive cattle ranch-
ing was developed and was decreed as a state-
owned protected area in 2010. It has an area of
52.36 ha, of which near to 30.5 ha are covered
by forest vegetation (hillsides), and the rest are
remnants of induced grasslands which is par-
tially in restoration process (non-sloping area)
(Herrera-Beltrán, 2010; SEDESMA, 2006).
La Martinica has plateaus and slopes with
angles from 2 to 45°, the area belongs to the
Neovolcanic province and is distributed in
an altitudinal range between 1 570 and 1 620
m.a.s.l., andosol is the predominant soil type,
the average temperature is 18 °C with an oscil-
lation of 5 to 7 °C and the total annual precipi-
tation fluctuates between 1 500 and 2 000 mm
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(4): 1189-1203, October-December 2021 (Published Nov. 17, 2021)
(SEDESMA, 2006). The climate corresponds
to temperate C (fm) b (i’) with an ample cool
summer, abundant rain all year round and little
thermal oscillation (García, 2004). The vegeta-
tion corresponds to a humid mountain forest
and the most typical characteristic species, we
can find Liquidambar styraciflua L., Clethra
mexicana DC, Carpinus tropicalis (Donn. Sm.)
Lundell, Ostrya virginiana (Mill.) Koch, and
Quercus spp. L (Villaseñor, 2010).
Sampling and measuring variables: A
stratified sampling was carried out in four
terrain aspects (sampling unit): zenithal (Z),
east (E), north (N) and south (S). The forest
was classified based on canopy densities in:
closed canopy (C), areas with a smaller open-
ing (21.8 ± 0.79), and open canopy (O), where
the opening percentage was bigger (26.23 ±
0.82), a generalized linear model for a Gauss-
ian distribution was used to determine whether
canopy opening varied significantly between
sites, the test showed that there is a signifi-
cant difference P < 0.0001. The estimation of
the gaps in each sampling subunit was made
through photographs taken at 1.6 m from the
ground (250 in total) at approximately 10:00
in the morning, with a Nikon COOLPIX B500
camera. Images were analyzed with CobCal
software version 1.0 (Ferrari et al., 2006), to
estimate the opening percentage. This method
is based on colorimetry, and the coverage per-
centage is calculated. Positive colors (represent
the vegetative surface to be calculated) and
negative colors (representative of the surface to
be discarded from calculation) were assigned to
Fig. 1. Location of the study area and distribution of the sampling units in the Protected Natural Area “La Martinica”, in the
municipality of Banderilla, Veracruz, Mexico.
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(4): 1189-1203, October-December 2021 (Published Nov. 17, 2021)
the photograph. The West aspect was not con-
sidered because the open canopy condition was
poorly represented in that aspect.
The sampling method of Endara-Agra-
mont et al. (2012) was adapted to each terrain
aspect and canopy type. Six sampling units
(SU) of 20 x 25 (500 ) were arranged in each
aspect. Three SUs were located in each canopy
type (3 in Z-C and 3 in Z-O), with the excep-
tion of north aspect with closed canopy condi-
tion where four SUs were installed, because
it was the most extensive area, for a total of
25 SUs, equivalent to 1.25 ha. Each SU was
divided into 10 subunits 10 x 5 m (50 m2) in
which the trees were numerated to facilitate
counting. Normal diameter (ND) was recorded
at 1.3 m height from the ground. Total height
was estimated, and also upper and lower crown
diameters of every individual with a ND 10
cm were measured.
Some species were collected, and photo-
graphs taken for later taxonomic identification
with specific available literature, i.e. Barce-
na (1981), Fernández-Nava (1986), Ludlow-
Wiechers (1978), Nash & Nee (1984), Nee
(1981), and Pacheco (1983). The Angiosperm
Phylogeny Group classification was followed
(APG IV, 2016; Stevens, 2017). The nomen-
clature was verified by consulting the Mis-
souri Botanical Garden database (TROPICOS,
2018). Collected specimens were deposited in
the CHAPA herbarium of Colegio de Postgrad-
uados, Mexico.
Structure and diversity: The structure
analysis of tree species on each terrain aspect
and canopy type was based on the estimation
of the importance value index (IVI = relative
dominance + relative density + relative fre-
quency) (Curtis & McIntosh, 1951; Sánchez-
Gutiérrez et al., 2017) and the forest value
index (FVI = relative ND + relative height +
relative cover) (Corella-Justavino et al., 2001;
Ortega-Baranda et al., 2017).
The diversity between terrain aspects and
forest canopy types was compared in units
of effective number of tree species. The pro-
cedure proposed by Chao & Jost (2012) and
Chao et al. (2014) was used, by interpolation
and extrapolation of estimates from diversity
rarefaction curves qD (y-axis) as a function of
sampling coverage
(x-axis), where species richness (q = 0), expo-
nential of Shannon entropy (q = 1), and inverse
of the Simpson concentration (q = 2). There-
fore, 0D = number of species, 1D = effective
number of equally frequent species, and 2D =
effective number of dominant species. f1 is the
number of species of which only one individual
was registered during the sampling, f2 is the
number of species with two individuals, and
n is the total number of registered individuals
(Cultid-Medina & Escobar, 2019). Estimations
were done in R software using “iNEXT” pack-
age (Hsieh et al., 2020; R Core Team, 2019).
Statistical analyses: The effect of the
aspects and types of canopies over plant com-
position were evaluated by a permutational
multivariate analysis of variance (PERMANO-
VA) for a factorial arrangement 4 x 2. Also,
the similarity in species composition among
aspects and type of canopy was evaluated
through non-metric multidimensional scaling
(NMDS), which produces a ranking based on
a dissimilarity matrix. The analyses were based
on 999 permutations using the Bray-Curtis
distance as a measure of similarity, with the
transformation of the data to square root. These
analyses were conducted with R software using
“Vegan” package (Oksanen et al., 2019; R Core
Team, 2019).
The association among tree species and
terrain aspects was based on a correspondence
analysis. A frequency matrix of individuals
from each species in their respective aspect
was elaborated. This analysis was carried out
in R software using “CA” package (Nenadic &
Greenacre, 2007; R Core Team, 2019).
The effect of the aspect and type of canopy,
on the basal area m2 and tree density (ind. x 500
m2), was determined using a generalized linear
model (Crawley, 2012) with a 4 x 2 factorial
Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(4): 1189-1203, October-December 2021 (Published Nov. 17, 2021)
arrangement for a Gaussian error distribution
in the case of basal area and quasi-Poisson
for density. When significant differences were
found, they were contrasted in pairs by the
Holm adjustment method, analysis were done
with the program R using the ‘Phia’ package
(R Core Team, 2019; Rosario-Martinez, 2015).
Individuals of 779 trees were recorded
which belong to 37 species, distributed in 30
genera and 24 families. The tree species with
the highest structural values in La Martinica
were the same for both indices (IVI and FVI).
The five species being remarkable abundant
were: Lippia myriocephala (IVI = 17.2 %, FVI
= 16.9 %), Carpinus tropicalis (IVI = 12 %,
FVI = 12.3 %), Myrsine coriacea (IVI = 11.27
%, FVI = 10.74 %), Liquidambar styraciflua
(IVI = 9.14 %, FVI = 9.69 %), and Trema
micrantha (IVI = 8.24 %, 9.63 % FVI) (Appen-
dix 1). The most important species were differ-
ent among terrain aspects. C. tropicalis had the
highest values on Z aspect (IVI = 17.75 %, FVI
= 18.2 %), L. myriocephala on E (IVI = 25.36
%, FVI = 25 %) and S aspects (IVI = 21.11 %,
FVI = 19.4 %), and L. styraciflua on N aspect
(IVI = 18.37 %, 20.2 % = FVI) (Appendix 2).
By contrast, in both types of canopy L. myrio-
cephala had the highest IVI values: at O (22.9
%) and at C (11.84 %), and only FVI in the O
canopy type (22.9 %), due to the fact that C.
tropicalis had a highest FVI in C canopy areas
(12.1 %) (Appendix 3).
All the diversity expressions (0D, 1D and
2D) were significantly higher in the N aspect. In
fact, no significant differences were observed
Fig. 2. Rarefaction curves with 95 % CI, constructed based on the coverage of the trees registered according to terrain aspect.
In the upper part, the order of diversity is shown: 0D = number of species, 1D = effective number of equally frequent species,
and 2D = effective number of dominant species. Curves were extrapolated to the total abundance observed in the zenithal
exposure (N = 222 individuals).