Introduction

In Mexico, conifer and broadleaf forests occupy 15.4 % of the national territory; managed forests cover 7.3 million hectares, while protected forests cover 7.1 million hectares (^{SARH-SFF, 1994}). On the other hand, nearly 80 % of the forest areas are communal property, and 95 % of the forest exploitations originate mainly from native temperate forests (^{Masera et al., 2001}).

In the state of Chiapas, these forests cover 117 248 ha, and rain forests occupy 2175 948 ha (^{SARH-SFF, 1994}); therefore, the entity has the second place nationally for forest surface area and timber extraction from pine, cypress, sweetgum, holm oak, rosy trumpet, amate, cedar and mahogany trees. In addition, its vast forest cover confers it a great potential for CO₂ sequestration.

Forest ecosystems can capture significant amounts of Greenhouse Gases (GHG), particularly CO₂. For this reason, in recent decades there is considerable interest in increasing the carbon content of the vegetation through the preservation of forests, reforestation, the creation of forest farms and other land management methods. A great number of studies have demonstrated the ability of forest species to store carbon in their biomass (^{Pimienta et al., 2007}; ^{Alberto and Elvir, 2005}; ^{Roncal et al., 2008}; ^{Nájera and Hernández, 2009}).

Each year, these forest areas store significant amounts of biomass that contribute to reduce carbon levels in the atmosphere (^{Melillo et al., 1993}; ^{Dixon et al., 1994}), which acquire greater significance if we consider that the CO₂ content in the atmosphere has augmented since the industrial revolution, and estimations indicate that in the XXI^st century this tendency will increase further (^{Petit et al., 1999}; ^{Crowley, 2000}; ^{UNEP, 2001}). All this indicates that anthropic activities have caused disturbances that contribute to the deterioration of the ecosystems (^{Dhillon and Von Wuehlisch, 2013}).

Various studies performed in Mexico have proven the potential of forests to capture atmospheric carbon. ^{Masera et al. (2001)} created a model simulating carbon capture during the 2000-2030 period, which divided land use into forests, rain forests, arid zones and non-forest uses. These authors used two scenarios: the first, referred to as “baseline”, and the second, as “policies”. If the proposed options derived from their results were to be adopted, Mexico would be able to capture approximately 46 million tons of carbon during the 2000-2030 period. Part of this mitigation would be achieved as follows: a) by preventing deforestation, b) through sustainable management of the natural forests, and c) by restoring the degraded forest areas.

CO₂ is one of the main components of GHGs and is produced by human activities when fossil fuels are utilized to generate energy and to meet other demands of society. Deforestation processes, land-use changes and methane concentrations resulting from agricultural and stockbreeding activities also promote climate change (^{UNEP, 2001}).

The increase in GHG concentrations in the atmosphere has caused the “greenhouse effect” phenomenon, which has resulted in changes in the climatic scales of the Earth (^{IPCC, 2007}). The increase of CO₂ in the atmosphere produces extreme climatic events such as floods caused by hurricanes, which result in regrettable losses of human lives as well as economic losses (^{IPCC, 2005}).

According to ^{Alberto and Elvir (2005)}, carbon sequestration has been the object of study of forest research in various countries. ^{Montero and Kaninnen (2002)} point out that, in southern Costa Rica, the accumulation of aboveground biomasss and carbon sequestration in managed Terminalia amazonia (J. F. Gmel.) Exell plantations after 10 years was of 97.03 Mgha^{- 1} and 45.30 Mg ha^-1, respectively. In central Honduras, the accumulation of aboveground biomass was of 80.53 Mg ha-1 in natural Pinus oocarpa forests (Ramos, 2000). Carbon accumulation in the aboveground biomass of the pine forests of the La Majada ejido in Michoacán, Mexico, amounted to 28.85 Mg ha^-1 (Zamora, 2003), while in the conifer forests of Tancítaro, Michoacán, Mexico, the annual accumulation and capture of carbon in the aboveground biomass added up to 19.00 Mg ha-1 and 1.65 Mg ha-1, respectively (^{Fragoso, 2003}). Based on the potential contribution of the forests of Chiapas to the mitigation of the effects of climate change, the purpose of the present research was to estimate the production of biomass and the capture of carbon in pine, holm oak, Mexican weeping pine and oak forests in the forest areas of La Frailesca region, as well as to determine the relationship between the age of trees and biomass production.

Location

The research was carried out in Villacorzo municipality, in southeastern Chiapas, in forest areas of 1 ejidos of La Frailesca region (Table 1, Figure 1), located between the coordinates los 16°1’05” N and 93°16’03” W, at a mean altitude of 584 masl (^{CEIEG, 2011}).

Table 1 Distribution of the plots by ejidos and by selected forest species. 

Figure 1 Location of the ejidos where the plots were selected for research purposes in La Frailesca region of Chiapas, Mexico. Created by Red AC (Network of Studies for Rural Development). 

A subhumid warm climate with abundant summer rains prevails in the study area. The minimum annual precipitation is 1200 mm, and the maximum is 3 000 mm, distributed among 100 and 200 days a year. The soils are affected by silt erosion precipitated by the action of the wind and by river floods; its fertility is variable, with its agricultural use conditioned by its depth and stoniness (^{CEIEG, 2011}).

The localities have a vegetal cover that consists mainly of conifer forest secondary vegetation, montane cloud and holm oak forests, and deciduous, sub-deciduous and evergreen rainforests.

Plot selection and estimation of the accumulated biomass and carbon sequestration

Mensuration data were recorded for twenty-two 500 m² sampling plots (two in each ejido). This information was entered into a database which included data of 358 individuals of the following species: Pinus maximinoii H. E. Moore (pine), Quercus robur L. (oak), Quercus rugosa Neé (holm oak), and Pinus patula Schiede ex Schltdl. & et Cham. (Mexican weeping pine) (Table1). The age of the trees was determined using a Pressler drill, as well as based on information provided by the common land holders; the normalized diameter (ND) was measured with a diameter measuring tape, and the height (H) of the main stem, with a clinometer (^{Gómez-Castro et al., 2010}).

The stem volume (V) was calculated using the following equation:

V= π4 •H•DN2•CF 1

Where:

• H = Tree height

• SC = Shape coefficient of each species.

• ND = Normalized diameter

In order to estimate the stem biomass, the total volume was multiplied by the density of each of the species (Table 2) (^{González, 2008}). Once the values of the biomass were determined, the accumulated carbon was estimated by multiplying the biomass by 0.50, a value that represents the mean concentration of carbon for conifers (^{Hamburg, 2000}); a value cited in the Green House Gas Inventories of the forestry sector for Mexico (^{IPCC, 2005}).

Table 2 Biomass expansion factors (BEF), shape coefficients (SCs) and density of the studied species. 

The value of the biomass accumulation in the various parts of the tree was determined based on the biomass expansion factors (BEFs) and shape coefficients (SCs) published by ^{González (2008)} (Table 2), with the following expressions:

Stem biomass (SBM)

SBM=V·ρ 2

Where:

• SBM = Stem biomass

• V = Stem volume

• ρ= Wood density (Table 2)

Tree aboveground biomass (AGBM)

AGBM=SBM · BEF 3

Where:

• AGBM = Tree aboveground biomass

• SBM = Stem biomass

• BEF = Biomass expansion factor

Root biomass (RBM)

RBM=AGBM · 0.30 4

Where:

• RBM = Root biomass

• AGBM = Tree aboveground biomass

Results and Discussion

The histogram of tree age by species shows that the pine plots reflected a rather heterogeneous distribution, with 12 % of the trees aged 40-50 years (Figure 2), followed by 10 % of trees aged 90-100. The age of holm oaks ranged between 20 and 70 years, with 10 % of the individuals in an age interval of 30-50 years. The oak forests had 95 trees aged 20 to 40 years, while 18 % of the trees of Mexican weeping pine forests were aged 30-60 years (Figure 2).

A = Pine; B = Holm oak; C = Oak; D = Mexican weeping pine.

Figure 2 Frequency histograms of tree ages sampled by species in La Frailesca region of Chiapas, Mexico. 

The largest number of trees with ND values of 0.1-0.4 m were oaks, followed by pines and Mexican weeping pines (Figure 3). In every case, like for the tree age, the highest degree of heterogeneity was found in the pine plots, with ND values ranging between 0.13 and 1.02 m (Figure 3). The interval between maximums, minimums and NDs (Table 3) made it possible to determine that the species with the highest variability were pine, holm oak, oak and Mexican weeping pine, in this order (Table 3).

A = Pine; B = Holm oak; C = Oak; D = Mexican weeping pine.

Figure 3 Frequency histograms of the ND of the sampled trees by species in La Frailesca region, Chiapas, Mexico. 

Table 3 Intervals between the maximums, the minimums and the normalized diameters (NDs) of the studied species. 

Given the close relationship observed between the ND, the age of the trees and biomass accumulation and carbon capture in various forest species (^{Fonseca et al., 2008}; ^{Gómez- Castro et al., 2010}), it is possible to understand the capacity of these forests to capture carbon from the atmosphere, particularly if it can be proven that the accumulated biomass and the captured carbon increase with the age of the trees.

The relationship between the height and the ND of the species was adjusted to an exponential model (Figure 4) called allometric, previously cited by ^{Acosta et al. (2002)} and ^{Gómez-Castro et al. (2010)}. The highest determination coefficients (r²) were observed in pines and holm oaks, which also had the broadest interval between tree ages and NDs. For all the species, the mathematical adjustment produced a statistical significance of the model parameters, according to the Student’s t-test (Table 4), a fact that corroborates the selection of the exponential model to estimate tree heights through the normalized diameter, although it suggests the need to delve into the effect of the normalized diameter interval, for which the best estimates were obtained.

Table 4 Parameters and statistical significance of the model of mathematical fit between the height and the normalized diameter. 

t = Student’s t; p = Probability of error.

A = Pine; B = Holm oak; C = Oak; D = Mexican weeping pine.

Figure 4 Exponential regression models of adjustment between the height and the ND of the studied species of La Frailesca region of Chiapas, Mexico. 

For all species, the ratio of the total biomass of the tree (BMt) and the age was significantly fitted according to an exponential model (Figure 5, Table 5), with determination coefficients ranging between 0.56 and 0.85. Similar results were obtained by ^{Rodríguez et al. (2004)} for the allometric relationships between the biomass production and the age of the pine trees. This result corroborates the biomass and carbon estimation studies based on the ND and ratifies the relationship between tree age and the photosynthetic processes that trigger biomass and carbon accumulation (^{Pacheco et al., 2007}).

A = Pine; B = Holm oak; C = Oak; D = Mexican weeping pine.

Figure 5 Regression curves of fit between the total accumulated biomass (BMt) and the age of the trees of the various species. 

Table 5 Parameters and statistical significance of the model of mathematical fit between the biomass and the age of the trees. 

t = Student’s t; p = Probability of error.

According to ^{Fonseca et al. (2008)}, both the aboveground biomass and the root biomass increase with the age in secondary forests and forest plantations. ^{Hughes et al. (1999)} register an average biomass of 272.1 Mg ha^-1 at 16 years of age. ^{Corrales (1998)} registers a biomass of 162.1 Mg ha^-1 in secondary forests aged 15 years, and of 324.1 Mg ha^-1 in primary forests in humid and very humid climates in Costa Rica.

The trees that accumulated the largest amount of biomass in the stem and other aboveground parts and in the roots were pines, with values above 0.79, 1.37 and 0.42 Mg ha^-1, respectively (Figure 6). Oak trees accumulated the least biomass. ^{Monroy and Navar (2004)} cite similar results for Hevea brasiliensis (Willd.) ex A. Juss.) Müll. Arg., with values of 73.9 % stem biomass and 27.1 % branch biomass, both of which increased with the age of the trees.

The vertical lines in the columns represent the mean standard error.

Figure 6 Biomass accumulation in the stem, branches and roots of pine, oak, holm oak and Mexican weeping pine trees in communities of La Frailesca region of Chiapas, Mexico. 

As for the relationship between the carbon content and the accumulated biomass in the various components of the plant, the results suggest that the high rates registered in pine forests for both growth and aboveground carbon fixation may be due, as ^{Pacheco et al. (2007)} proved, to a good combination between the production of wood and cellulose compared to other species; this is helpful for the implementation of reforestation and CO₂ sequestration projects (^{Gamara, 2001}). However, other factors, such as the site and the tree mass, also determine biomass accumulation and carbon capture. Furthermore, this author cites a direct relationship between the sequestered carbon and growth, in both the normal diameter (ND) and the total height of the trees (^{Ugalde, 1997}).

Analysis of the information from the various ejidos proved that the total biomass accumulated in pine trees was highest at “24 de Febrero” and “Juan Sabines” (Figure 7), with values above 8 and 6 Mg ha^-1, respectively. Therefore, these communities also had the highest values for carbon capture.

Figure 7 Biomass (A) and carbon (B) accumulation in Pinus maximinoii H. E. Moore forests of the Juan Sabines, Tierra Santa, La Unión and 24 de Febrero communities of La Frailesca region of Chiapas. 

Holm oak forests, which are prevalent in the “Bonanza” and “24 de Febrero” communities, accumulated up to 0.8 and 2.5 ha^-1Mg of total biomass, respectively (Figure 8), whereas the accumulated carbon was higher at “24 de Febrero”, with 390 Mg of C ha^-1, which proves the potential of this ejido for CO₂ capture and its contribution to the abatement of Greenhouse Gases (GHGs).

The vertical lines in the columns represent the mean standard error.

Figure 8 Biomass (A) and carbon (B) accumulation in Quercus rugosa Neé forests in the Juan Sabines, Tierra Santa, La Unión and 24 de Febrero communities of La Frailesca region of Chiapas, Mexico. 

The total biomass accumulation in oak trees was 0.79 to 1.12 Mg ha^-1, the highest record in the forest areas of the “La Libertad” ejido, followed by “Monterrey” (Figure 9). The lowest value was found at “Patria Chica”. As for carbon capture, in all the ejidos it was above 50 Mgha^-1; the highest was obtained in the forests of the “La Libertad” ejido, with 82 Mg of C ha^-1 (Figure 9).

The vertical lines in the columns represent the mean standard error.

Figure 9 Biomass (A) and carbon (B) accumulation in Quercus robur L. forests of the Juan Sabines, Tierra Santa, La Unión and 24 de Febrero communities of La Frailesca region of Chiapas, Mexico. 

For the clear trunks of Pinus cooperi C. E. Blanco in Durango, Mexico, ^{Pimienta et al. (2007)} estimated an average value of accumulated carbon of 51.12 Mg ha^-1, a higher value than estimated by ^{Domínguez et al. (2007)} for the mixed Pinus teocote Schiede ex Schltdl. & Cham. and Pinus pseudostrobus Lindl. forests in southern Nuevo León, Mexico, which was 45.18 Mg ha^-1. Studies of biomass and fixed carbon quantification in 269 felled and harvested trees belonging to 12 species in temperate rainforests of the central-southern region of Chile estimated the biomass and the carbon accumulated in the roots, undergrowth, necromass and dead leaves. Carbon accumulation in the sites of the pre-Andes mountains was 662.06 Mg ha^-1, i.e., higher than in the Cordillera de la Costa (Coast Mountain Range), where it was 423.83 Mg ha^-1.

The total biomass accumulated by Mexican weeping pines (Pinus oocarpa Schiede) ranged between 1.57 and 2.51 Mg ha^-1 (Figure 10). This species occurred only in the “La Frailesca” and “Nuevo Refugio” ejidos; the forests of the latter contributed a larger amount to this accumulation. The highest values for accumulated carbon 212 Mg of C ha^-1, were found in the forests of “Nuevo Refugio”, while the “La Frailesca” ejido accumulated only 132 Mg ha^-1.

The vertical lines in the columns represent the mean standard error.

Figure 10 Biomass (left) and carbon (right) accumulation in Pinus oocarpa Schiede forests of the La Frailesca and Nuevo Refugio in La Frailesca region of Chiapas, Mexico. 

As for the accumulation of biomass per tree components (Figures 6, 7, 8, 9 and 10), in all the taxa and localities, the highest accumulation occurred in the aboveground biomass, as indicated by ^{Gower et al. (1993)}, who proved that approximately 75 % of the biomass of a tree is accumulated in the aboveground parts, while only 25 % is accumulated in the roots.

Comparison between biomass accumulation and carbon capture by species showed that Pinus spp. and Quercus spp. had the highest values, while Quercus robur had the lowest (Table 6). This agrees with the findings of ^{González (2008)}, who, after comparing three tree species, determined that P. maximinoi had the highest biomass accumulation, followed by Quercus spp. In regard to carbon, pine and holm oak had a capture potential of 380.13 to 173.852 Mg of C ha^-1 (Table 6).

Table 6 Accumulated biomass and carbon in pine, holm oak, oak and Mexican weeping pine forests of La Frailesca region, Chiapas. 

Different letters in the superscripts (^a, ^b and ^c) indicate significant statistical differences of p≤ 0.05.

Conclusions

Biomass accumulation was adjusted to an exponential model with the age of the trees of the four evaluated species. The forests of the “24 de Febrero” ejido registered the highest growth, based on their height and stem diameter, as well as on the accumulated biomass, rendering this ejido one of the localities with the highest potential for carbon capture of all the studied sites.

Pine, holm oak, oak and Mexican weeping pine trees of the communities of Frailesca region in Chiapas, Mexico, accumulate between 0.459 and 2.606 Mg ha^-1 of vegetal biomass; therefore, they are considered to have a high potential for carbón capture. Pine tres reached a value of 380.13 Mg^-1 ha^-1 of C; due to its high degree of development, this species has the highest capture potential of all.

Conflict of interests

The authors declare no conflict of interest.

Contribution by author

Luis Alfredo Rodríguez Larramendi: coordination and integration of the article and analysis of field data; Francisco Guevara Hernández: coordination of the research team, as well as of field work, logistics, and of the project which supported the actual paper and review of great part of it; Luis Reyes Muro: help in field work and in the makind and analysis of results; Jesús Ovando Cruz: maps and help in the information of the institutions involved in the actual paper; José Nahed Toral: contribution with the focus and theoretical and methodological concept to prepare this paper; Miguel Prado López: information about natural protected areas and review of previous versions of the manuscript; Rady Alejandra Campos Saldaña: help in field work, in methodology and review of the previous versions of the document.