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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.

ABSTRACT

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.

v69i4.46855

https://doi.org/10.15517/rbt.v69i4.46855

TERRESTRIAL ECOLOGY

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,

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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

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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.

MATERIALS AND METHODS

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

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(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.

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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

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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).

RESULTS

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).