Introduction
Plant biomass is formed by all the organic components within an ecosystem (Litton et al., 2007) and is important as a
source of energy, as well as in the storage of carbon (C) and nitrogen (N)
(Peichl et al., 2012; Schuler et al., 2017). The capacity of a
forest to capture atmospheric carbon tends to decrease with the increase in the
age of the trees. It is known that at early or intermediate ages the rate of
carbon capture is higher (López-Reyes et al.,
2016). In addition, it is related to the rate of accumulation of
aboveground and root biomass that forests have with the net growth of trees that
are capable of sequestering more CO2 than they emit through
respiration. The rate of carbon capture is directly proportional to said growth
(Casiano-Domínguez et al., 2018).
-
Litton et al., 2007
Carbon allocation in forest ecosystems
Global Change Biology, 2007
-
Peichl et al., 2012
Above-and belowground ecosystem biomass, carbon and nitrogen
allocation in recently afforested grassland and adjacent intensively managed
grassland
Plant and Soil, 2012
-
Schuler et al., 2017
Biomass estimates of small diameter planted and natural-origin
loblolly pines show major departures from the national biomass estimator
equations
Forest Science, 2017
-
López-Reyes et al.,
2016
Carbono almacenado en la biomasa aérea de plantaciones de hule
(Hevea brasiliensis Müell. Arg.) de diferentes edades
Madera y Bosques, 2016
-
Casiano-Domínguez et al., 2018
El Carbono de la biomasa aérea medido en cronosecuencias: primera
estimación en México
Madera y Bosques, 2018
Natural Protected Areas (NPA) are intended to conserve, protect and recover
natural resources (González et al., 2014;
Íñiguez et al., 2014). Such is the case of El Chico National
Park, which is a provider of important environmental services for the
mountainous region of central Mexico and is home to one of the most important
relics of Abies religiosa (Kunth) Schltdl. & Cham. (fir)
(Comisión Nacional de Áreas Naturales
Protegidas [Conanp], 2005). This species develops in humid conditions
(precipitation greater than 1 000 mm) and in low temperatures (average
temperature of 7 to 12 °C), so the increase in the temperature on the planet
causes effects, which are manifested in modifications at the molecular,
morphological and physiological level that are reflected in negative alterations
in its early stages of development (Romahn-Hernández et al., 2020).
-
González et al., 2014
Las áreas naturales protegidas de México
Investigación y Ciencia de la Universidad Autónoma de
Aguascalientes, 2014
-
Comisión Nacional de Áreas Naturales
Protegidas [Conanp], 2005
Programa de conservación y manejo Parque Nacional El Chico, 2005
-
Romahn-Hernández et al., 2020
Rango altitudinal: factor de vigor forestal y determinante en la
regeneración natural del oyamel
Revista Entreciencias: Diálogos en la Sociedad del Conocimiento, 2020
The initial development of the temperate forest is known as the sapling stage,
which includes trees up to approximately 1.5 m tall and with an average base
diameter of less than 5 cm (Aguilar, 2018;
Hutchinson, 1993; Ronquillo-Gorgúa et al., 2022). In most
temperate climate NPAs, the sapling stage is established during the first rainy
period, after gaps are generated in the canopy that allow solar radiation to
enter the forest floor (Lara-González et al.,
2009). Generally, there are densities of up to 6 100 seedlings
ha-1 in western exposures (Rodríguez-Laguna et al., 2015) that are reduced over time due to
competition for abiotic and biotic factors that thus achieve a gradual
accumulation of biomass in the aboveground and root parts of the tree (Bar-On et al., 2018; Ronquillo-Gorgúa et al., 2022).
-
Aguilar, 2018
Estructura y diversidad de la vegetación arbórea de un bosque de
galería en el estado de Puebla
Revista Mexicana de Ciencias Forestales, 2018
-
Hutchinson, 1993
Puntos de partida y muestreo diagnóstico para la silvicultura de bosques
naturales del trópico húmedo, 1993
-
Ronquillo-Gorgúa et al., 2022
Carbon storage during the development stages of Pinus patula
Schiede ex Schltdl. & Cham. in the Sierra Alta of
Hidalgo
Revista Chapingo Serie Ciencias Forestales y del Ambiente, 2022
-
Lara-González et al.,
2009
Regeneration of Abies religiosa in canopy gaps versus understory,
Cofre de Perote National Park, México
Agrociencia, 2009
-
Rodríguez-Laguna et al., 2015
Regeneración natural post-incendio de Abies religiosa (H. B. K.)
Schl. et Cham, en el Parque Nacional “El Chico” Hidalgo
Revista Iberoamericana de Ciencias, 2015
-
Bar-On et al., 2018
The biomass distribution on Earth
Proceedings of the National Academy of Sciences, 2018
-
Ronquillo-Gorgúa et al., 2022
Carbon storage during the development stages of Pinus patula
Schiede ex Schltdl. & Cham. in the Sierra Alta of
Hidalgo
Revista Chapingo Serie Ciencias Forestales y del Ambiente, 2022
Studies focused on estimating the accumulation of aboveground biomass in forests
(Albers et al., 2019; Oliveira et al., 2018; Pham et al., 2019; Razo et al., 2015), do not consider root biomass (Adame et al., 2017; Addo-Danso et al., 2016; Sochacki et al., 2017). Recent research suggests the need to know
point estimates by component of the total forest biomass on a large scale (Bar-On et al., 2018; Djomo et al., 2011; Fu et
al., 2017).
-
Albers et al., 2019
Data and non-linear models for the estimation of biomass growth
and carbon fixation in managed forests
Data in Brief, 2019
-
Oliveira et al., 2018
Above-and below-ground carbon accumulation and biomass allocation
in poplar short rotation plantations under Mediterranean
conditions
Forest Ecology and Management, 2018
-
Pham et al., 2019
Integrating Sentinel-1A SAR data and GIS to estimate aboveground
biomass and carbon accumulation for tropical forest types in Thuan Chau
district, Vietnam
Remote Sensing Applications: Society and Environment, 2019
-
Razo et al., 2015
Coeficientes de Carbono para arbustos y herbáceas del bosque de
oyamel del Parque Nacional El Chico
Revista Mexicana de Ciencias Forestales, 2015
-
Adame et al., 2017
Mangrove root biomass and the uncertainty of belowground carbon
estimations
Forest Ecology and Management, 2017
-
Addo-Danso et al., 2016
Methods for estimating root biomass and production in forest and
woodland ecosystem carbon studies: A review
Forest Ecology and Management, 2016
-
Sochacki et al., 2017
Accuracy of tree root biomass sampling methodologies for carbon
mitigation projects
Ecological Engineering, 2017
-
Bar-On et al., 2018
The biomass distribution on Earth
Proceedings of the National Academy of Sciences, 2018
-
Djomo et al., 2011
Estimations of total ecosystem carbon pools distribution and
carbon biomass current annual increment of a moist tropical
forest
Forest Ecology and Management, 2011
-
Fu et
al., 2017
Individual tree biomass models to estimate forest biomass for
large spatial regions developed using four pine species in
China
Forest Science, 2017
The machinery, tools and time to extract adult trees with roots is almost
impossible, but the interest in providing information on the root component of
young trees allows for complementary information to reach the total biomass
stored in the forest. Fragoso-López et al.
(2017) estimated the aboveground biomass component through geographic
information systems; likewise, the biomass stored on the soil surface, known as
necromass (Cortés-Blobaum et al., 2019),
is known, so it is necessary to incorporate a part of the root component in this
ecosystem. Therefore, the objective of the present research was to estimate the
total biomass accumulation capacity (aboveground-root) in A.
religiosa trees at the sapling stage in El Chico
National Park, Hidalgo state, Mexico.
-
Fragoso-López et al.
(2017)
Carbon sequestration in protected areas: A case study of an Abies
religiosa (H. B. K.) Schlecht. et Cham forest
Forests, 2017
-
Cortés-Blobaum et al., 2019
Patrones culturales de uso de leña en la primera área protegida
de Latinoamérica, El Chico, México
Revista Iberoamericana de Ciencias, 2019
Materials and Methods
Study area
The study was carried out in the NPA El Chico National Park,
located at the western end of the Sierra de Pachuca,
Hidalgo state, in the Transversal Neovolcanic Axis
(Figure 1). It is located between
20°10’10’’ to 20°13’25’’ North and 98°41’50’’ to 98°46’02’’ West, with an
area of 2 739 ha, and altitudes between 2 600 and 3 050 m (Conanp,
2005).
Figure 1
Geographic location of El Chico National
Park, Hidalgo state, Mexico.
The climate is temperate-subhumid with summer rains (C(m)(w)b(i0)gw) and mean
annual temperature between 12 and 18 °C. The predominant soils are humic
Cambisol, dystric Regosol and medium-textured humic Andosol (Conanp, 2005).
The largest percentage of vegetation cover (67 %) belongs to the A.
religiosa forest (Fragoso-López
et al., 2017); other important tree species are:
Quercus spp., Pseudotsuga macrolepis
Flous, Taxus globosa Schltdl. and Pinus
spp. (Conanp, 2005).
-
Fragoso-López
et al., 2017
Carbon sequestration in protected areas: A case study of an Abies
religiosa (H. B. K.) Schlecht. et Cham forest
Forests, 2017
Tree density in the sapling stage
To determine density, four 100 m2 (10×10 m) plots were established
in fir regeneration areas; from which the complete saplings with roots were
extracted.
Tree selection for aboveground-root biomass analysis
Travels were conducted within El Chico National Park to
identify spaces (clearings) within the forest that were large enough for
natural fir regeneration. A total of 52 A. religiosa trees
at sapling stage were selected, with average heights of 6-150 cm (Ronquillo-Gorgúa et al., 2022), free of
mechanical damage, far from roads or gaps with compacted soil, and were
completely extracted from the root.
-
Ronquillo-Gorgúa et al., 2022
Carbon storage during the development stages of Pinus patula
Schiede ex Schltdl. & Cham. in the Sierra Alta of
Hidalgo
Revista Chapingo Serie Ciencias Forestales y del Ambiente, 2022
Organic matter was removed from each tree using a rake, then sufficient water
was gradually added around the base of the specimen in order to soften the
soil and remove it the next day, taking care not to damage the root. A
high-pressure water backpack sprayer was used and the direction and depth of
each root was followed (one at a time) until the complete extraction of the
root system was ensured. A wooden support in the form of a square was
implemented, fixed to the ground, which helped to keep the tree in a
vertical position; in the middle part of the trunk they were tied with
plastic ropes during the entire extraction process, until the root system
was completely free.
Evaluated variables
The total height (cm) from the soil surface to the apex of each tree was
measured with a model FCN-3M Truper® tape measure; the base
diameter (cm), with a model 14388 Truper® digital vernier with
millimetric precision; age was determined by the number of whorls in each
individual, since these are produced at a rate of one whorl per year in
Abies (Lara-González et
al., 2009). The complete root system of each specimen was washed
and left to air dry in the shade for approximately two hours (Fonseca et al., 2009) and the fresh
weight of the entire tree (g) was taken in the field with a model BE16001
Biobase® scale. Subsequently, the aerial and root parts were
separated to weigh each component and were placed each in paper bags
previously labeled with the sample number and were placed in a model LW-201C
GRIEVE® drying oven at 80 °C until reaching constant weight.
With this, the average dry weight (g) of each component was calculated and
multiplied by the number of fir plants per hectare.
-
Lara-González et
al., 2009
Regeneration of Abies religiosa in canopy gaps versus understory,
Cofre de Perote National Park, México
Agrociencia, 2009
-
Fonseca et al., 2009
Modelos para estimar la biomasa de especies nativas en
plantaciones y bosques secundarios en la zona Caribe de Costa
Rica
Bosque, 2009
In a first analysis, the variance of the dry weight of the root was
determined with the following formula:
t = Standardized value of the error at 5 %, which is
equivalent to 1.96
σ
2
= Variance of the attribute to be evaluated
d = Confidence interval for the quality measured (Zar, 2010).
-
Zar, 2010
Biostatistical analysis, 2010
Data analysis
With the information from the 52 trees included in the sample, a cluster
analysis was performed based on the variables height, dry weight of the
whole tree, dry weight of the root and percentage of root biomass, using the
Ward method based on Euclidean distances; for this, the Statistica v.10
program was used (StatSoft Inc.,
2011). The dry root biomass was contrasted using a t-test for
unbalanced samples, before a normality test. For this analysis, the Past
program was used (Hammer et al.,
2001). And the rest of the attributes were contrasted with parametric
or non-parametric paired tests according to the type of data.
-
StatSoft Inc.,
2011
STATISTICA (data analysis software system), 2011
-
Hammer et al.,
2001
PAST: Paleontological statistics software package for education
and data analysis
Palaeontologia electrónica, 2001
Results and Discussion
The cluster analysis indicated the formation of two groups that are mainly
distinguished by smaller size (initial sapling) with a height range of 6 to 65
cm, 0.07 to 0.9 cm base diameter and age of 1 to 8 years, and another of larger
size (developed sapling) with a height range of 68 to 150 cm, 0.9 to 2.1 cm base
diameter and age of 8 to 12 years. The root biomass data are normally
distributed (Anderson-Darling, 0.4669 and 0.3743; p>0.05)
with 38 individuals of initial sapling and 14 of developed sapling; on the other
hand, no significant differences were found between groups of saplings
(t=1.7468; p=0.09), while for height:
t=5.47 and p=0.0001, dry weight of the
aerial part: t=5.435 and p=0.0001, and dry
weight of the root: t=5.482 and p=0.0001.
The organization of two groups is possibly due to the age of the specimens and
the differences in the formed and accumulated biomass (Figure 2), in addition to the changes in the formation of
roots at early ages, so it is not possible to assume a linear increase
throughout the life of the plant.
Figure 2
Grouping by morphological attributes in Abies
religiosa (Kunth) Schltdl. & Cham. plants at the
sapling stage in El Chico National Park,
Hidalgo state, Mexico.
Some works mention that the proportion of aboveground biomass-root biomass are
interdependent, which highlights the importance of the functional balance of
both parts (van Noordwijk & Willigen,
1987). However, the growth rate of both elements differs depending on
soil water content, biophysical processes, changes in leaf elongation rate,
plant stress, crowding and competition, among others (Krizek et al., 1985; Macklon et al., 1994).
-
van Noordwijk & Willigen,
1987
Agricultural concepts of roots: from morphogenetic to functional
equilibrium between root and shoot growth
Netherlands Journal of Agricultural Science, 1987
-
Krizek et al., 1985
Comparative effects of soil moisture stress and restricted root
zone volume on morphogenetic and physiological responses of soybean [Glycine
max (L.) Merr.]
Journal of Experimental Botany, 1985
-
Macklon et al., 1994
Soil P resources, plant growth and rooting characteristics in
nutrient poor upland grasslands
Plant and Soil, 1994
Biomass by component
The results for dry biomass by component indicate that the trees in the
initial sapling group have 72.6 % of aboveground biomass and 27.4 % of root
biomass (Figure 3), while in the
developed sapling group, 75.8 % corresponds to aboveground biomass and 24.2
% to root biomass (Figure 4). It is
convenient to consider this rate of change to estimate the amount of Carbon
in regeneration areas, especially when the space has a greater abundance of
young plants. Previous studies have shown that there is a significant
increase of up to five percentage points in root production in restrictive
soils (Guerra et al., 2005), which
could modify the results obtained if they were compared under conditions
with lower soil nutritional quality.
-
Guerra et al., 2005
Análisis de la biomasa de raíces en diferentes tipos de bosques.
Avances en la evaluación de Pinus radiata en Chile
Bosque, 2005
Figure 3
Aboveground and root biomass in initial sapling trees (6 to
65 cm tall).
Figure 4
Aboveground and root biomass in trees with developed saplings
(68 to 150 cm tall).
Several authors estimate that 20 to 40 % of forest biomass is composed of
roots (Brunner & Godbold, 2007;
Finér et al., 2011; Sochacki et al., 2017); however, this
biomass changes according to the species, the climate and the
characteristics of the ecosystem in which they grow.
-
Brunner & Godbold, 2007
Tree roots in a changing world
Journal of Forest Research, 2007
-
Finér et al., 2011
Factors causing variation in fine root biomass in forest
ecosystems
Forest Ecology and Management, 2011
-
Sochacki et al., 2017
Accuracy of tree root biomass sampling methodologies for carbon
mitigation projects
Ecological Engineering, 2017
Accumulated biomass potential
An average regeneration density of 3 925 trees ha-1 at the sapling
stage was estimated, but this result could be overestimated since the
sampling sites were located in clear spaces in the canopy where
environmental conditions allowed the establishment of A.
religiosa regeneration; however, under the canopy of adult
trees the density was low due to the low solar radiation that reaches the
forest floor and the plants do not regularly establish themselves (Lara-González et al., 2009).
Contrasting data by Hernández et al.
(2022) with the percentage of dead seedlings under a partially
closed canopy was 79 % (n=803), while under light gaps it
was 70.1 % (n=384). And regarding the percentage of live
seedlings under a partially closed canopy it was 17.9 %
(n=182), while in light gaps it was 28.1 %
(n=154).
-
Lara-González et al., 2009
Regeneration of Abies religiosa in canopy gaps versus understory,
Cofre de Perote National Park, México
Agrociencia, 2009
-
Hernández et al.
(2022)
Nicho de regeneración de Abies religiosa (Kunth) Schltdl. &
Cham. en el Monte Tláloc, Parque Nacional Iztaccíhuatl-Popocatépetl,
México
Botanical Sciences, 2022
On the other hand, the potential of total biomass (aboveground and root)
stored in A. religiosa at the sapling stage was 103.6 kg
ha-1 (Figure 5). It is
worth noting that the aboveground part-root ratio calculated was 3:1, that
is, 3 parts correspond to aboveground biomass and one part to root biomass.
This contributes to maintaining organic Carbon (OC) under the soil by
inducing its stability through the mineralization process that occurs over
time. Xia et al. (2022) mention that
the lignin contained in the wood of the roots is a recalcitrant component
that stabilizes the OC in the soil for decades, and fir forests have a high
lignin content as do pine forests (Avendaño
et al., 2009; Leifeld &
Kögel-Knabner, 2005).
-
Xia et al. (2022)
Characterizing natural variability of lignin abundance and
composition in fine roots across temperate trees: a comparison of analytical
methods
New Phytologist, 2022
-
Avendaño
et al., 2009
Estimación de biomasa y Carbono en un bosque de Abies
religiosa
Revista Fitotecnia Mexicana, 2009
-
Leifeld &
Kögel-Knabner, 2005
Soil organic matter fractions as early indicators for carbon
stock changes under different land-use?
Geoderma, 2005
Figure 5
Potential storage of aboveground and root biomass per hectare
of fir trees at the sapling stage in El Chico
National Park, Hidalgo state, Mexico.
Root competition is greater when they grow with other root structures, so
this is a factor that influences their conformation, extension and
distribution in the soil and sometimes tends to reduce their depth, design
and density (Bolte & Villanueva,
2006; Curt & Prévosto,
2003; Rewald & Leuschner,
2009). In this way, the percentage of root biomass during the
growth of Abies religiosa in El Chico
National Park could be reduced.
-
Bolte & Villanueva,
2006
Interspecific competition impacts on the morphology and
distribution of fine roots in European beech (Fagus sylvatica L.) and Norway
spruce (Picea abies (L.) Karst.)
European Journal of Forest Research, 2006
-
Curt & Prévosto,
2003
Root biomass and rooting profile of naturally regenerated beech
in mid-elevation Scots pine woodlands
Plant Ecology, 2003
-
Rewald & Leuschner,
2009
Belowground competition in a broad-leaved temperate mixed forest:
pattern analysis and experiments in a four-species stand
European Journal of Forest Research, 2009
Conclusions
Abies religiosa forests at the sapling stage have the potential
to accumulate aboveground-root biomass in a 3:1 ratio in canopy gaps where
conditions allow the establishment of natural regeneration. Small plants aged 1
to 8 years on average store more root biomass in percentage than larger plants
aged 8 to 12 years at the same sapling stage. The ratio of root biomass to
aboveground biomass at the sapling stage changes with age in Abies
religiosa trees.
Acknowledgements
The authors wish to express their gratitude to the National Council of
Humanities, Sciences and Technologies (Conahcyt), for the
financial scholarship granted to the first author, which allowed this research
to be carried out.
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