The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures

Abstract

Based on previous reports, our study aimed to obtain the first estimate on the contribution of termite mounds to CH4 emissions in Brazilian Cerrado pastures. We estimated that termite mounds occupy an area larger than 200,000 ha in degraded pastures, an important loss of grazing area considering the current scenario of land-use change of pastures to other crops in Brazil. Moreover, mound-building termites in degraded pastures may be responsible for CH4 emissions greater than 11 Mt CO2 eq. yr−1, which would notably affect the greenhouse gases (GHG) balance of grass-fed cattle production in Brazil. In this sense, it is urgent to conduct field-scale studies about the CH4 emissions by mound-building termites in pastures and its contribution to the C footprint of Brazilian beef.

Full text

Brazilian Journal of Animal Science
e-ISSN 1806-9290
www.rbz.org.br
R. Bras. Zootec., 50:e20200185, 2021
https://doi.org/10.37496/rbz5020200185
Forage crops
Full-length research article
The neglected contribution of
mound-building termites on CH4
emissions in Brazilian pastures
ABSTRACT     
on the contribution of termite mounds to CH4 emissions in Brazilian Cerrado pastures.
We estimated that termite mounds occupy an area larger than 200,000 ha in degraded
pastures, an important loss of grazing area considering the current scenario of land-use
change of pastures to other crops in Brazil. Moreover, mound-building termites in
degraded pastures may be responsible for CH4 emissions greater than 11 Mt CO2 eq. yr,
which would notably affect the greenhouse gases (GHG) balance of grass-fed cattle
  
CH4 emissions by mound-building termites in pastures and its contribution to the C
footprint of Brazilian beef.
Keywords: biogenic CH4, Brazilian Cerrado, greenhouse gases, pasture degradation
1. Introduction
Global average methane (CH4) concentrations in atmosphere reached ~1875 parts per billion at the
end of 2019, more than 2.5 times that of preindustrial levels (Dlugokencky, 2020). Unfortunately, CH4
presents a potential greenhouse effect 25 times higher than CO2 on a timespan of 100 years. Currently,
more than 580 Tg yr of CH4 are released into the atmosphere, with more than 70% of this value
originating from biogenic sources (Saunois et al., 2020). Among the biogenic sources of CH4, importance
must be given to ruminants, waterlogged areas, peatlands, and termites (Saunois et al., 2020). Although
the less attention recently received, termites had been associated with about 15% of the entire CH4
emitted globally (Rasmussen and Khalil, 1983).
Nowadays, Brazil is the second biggest beef exporter and has the second largest herd in the world, only
surpassed by India. Most livestock production is grass-fed, extensive, and spread across the Cerrado
biome. Cerrado occupies an area of 204.7 million ha in central Brazil. Pastures are the main land use in
this biome, occupying more than 54 million ha (Sano et al., 2008). It is estimated that 60% of Cerrado
pastures are degraded in some level (Andrade et al., 2014). Generally, degraded pastures exhibit low
plant and animal productivity, reduced soil cover, soil erosion and compaction, and invasion of weeds.
Despite the contentious relationship between termite infestation and pasture degradation (Lima et al.,
Dener Márcio da Silva Oliveira1*, Eloá Moura Araújo2, Elizio
Ferreira Frade Junior3, Laisa Gouveia Pimentel1, Carlos Eduardo
Pellegrino Cerri4
1 Instituto Federal Goiano, Laboratório Multiusuário de Ciências Naturais, Posse, GO, Brasil.
2 Universidade Federal do Paraná, Departamento de Solos e Engenharia Agrícola, Curitiba,
PR, Brasil.
3 Universidade Federal do Acre, Laboratório de Fertilidade do Solo e Nutrição de Plantas,
Rio Branco, AC, Brasil.
4 Universidade de São Paulo, Escola Superior de Agricultura “Luiz de Queiroz”,
Departamento de Ciência do Solo, Piracicaba, SP, Brasil.
*Corresponding author:
dener.oliveira@ifgoiano.edu.br
Received: August 14, 2020
Accepted: November 5, 2020
How to cite: Oliveira, D. M. S.; Araújo, E. M.;
Frade Junior, E. F.; Pimentel, L. G. and Cerri,
C. E. P. 2021. The neglected contribution of
mound-building termites on CH4 emissions
in Brazilian pastures. Revista Brasileira de
Zootecnia 50:e20200185.
https://doi.org/10.37496/rbz5020200185
Copyright: This is an open access article
distributed under the terms of the
Creative Commons Attribution License
(http://creativecommons.org/licenses/by/4.0/),
which permits unrestricted use, distribution,
and reproduction in any medium, provided the
original work is properly cited.

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
2
2011), a high infestation of mound-building termites is certainly an indicator of pasture degradation
(e.g., Spain and Gualdrón, 1988; Santos et al., 2007; Miranda et al., 2012).
Enteric fermentation is the main source of CH4 in Brazil, being responsible for the emission of 246 million
Gg CO2 eq yr (MCTI, 2014), whilst one of the main sources of N2O emissions is the deposition of urine
      
of greenhouse gases (GHG) from pastures. However, is possible that C inventories have neglected
the role of an important component in CH4 emissions from pastures: mound-building termites. The
        2 (intermediate in the fermentation
process), which permits reduced cofactors to be re-oxidized, increasing the fermentation of cellulosic
material (Grieco et al., 2013). However, this process is responsible for CH4 production, the main negative
outcome of termite-microbe symbiosis. Studies carried out in Africa (Brümmer et al., 2009) and Oceania
Savana (Jamali et al., 2011a) highlighted the notable contribution of mound-building termites in CH4
emissions of these areas. In Brazil, oddly enough, there is no published study about the CH4 emissions
by mound-building termites from Cerrado pastures.
Pasture recovery and deforestation reduction are goals reinforced in the Brazilian intended
Nationally Determined Contribution (iNDC) set during the United Nations Conference on Climate
Change (iNDC Brazil, 2015). The Brazilian government has ambitious goals for the next years:
reduce GHG emissions by 37% by 2025 and 43% by 2030, compared with 2005. To do so, one of
the commitments of the Brazilian iNDC is to strengthen the Low Carbon Emission in Agriculture
Program (ABC Program; Brasil, 2012) as the main strategy for sustainable agriculture development,
including restoration of additional 15 million ha of degraded pastures by 2030. Pasture recovery

C footprint of Brazilian beef (Silva et al., 2016). However, the magnitude of this mitigation could be
greater if an important source of GHG in degraded pastures were accounted in inventories: mound-
building termites.
   
mound-building termites in CH4
we aimed to identify Cerrado pastures under different degradation levels, estimate the average
infestation by mound-building termites associated with each degradation level, calculate the loss of
grazing area due to mound termite infestation, and estimate CH4 emissions by termites in degraded
pastures of Brazilian Cerrado.
2. Material and Methods
After a comprehensive literature review and using all available data from previous studies, our
research estimated CH4 emissions by termites in pastures from Brazilian Cerrado. In each stage,
a compilation, analysis, and extrapolation using all the available data were carried out. Initially,
it was assumed that 60% of Cerrado pastures are degraded (Andrade et al., 2014). Then, from the
few studies regarding this topic, the pasture area under different degradation levels was estimated
(low to moderate, high, and very high). As observed in studies used in our assessment, the model

of the degradation process in pastures. In this model, the occurrence of termite mounds is one of
the indicators for highest degradation levels. Thus, infestation by mound-building termites and its
associated CH4     
high degradation levels.
Split pastures by different degradation levels was very useful, considering that termite infestation is
quite variable among areas. In this way, it was possible to associate a level of infestation by termites
with a level of pasture degradation, as also proposed by Santos et al. (2007) and Miranda et al. (2012).
The level of infestation by mound-building termites was estimated using different studies carried out
across Brazilian Cerrado (Figure 1). Based on the approach proposed by Spain and Gualdrón (1988),
we assumed infestations of 70 and 200 mounds ha as the bottom limit associated to high and very

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
3
high levels of pasture degradation, respectively. To calculate the area occupied by termite mounds,
seven studies were used, all carried out in Brazilian Cerrado (Figure 1). Moreover, it was assumed that
88% of termite mounds are active, according to Lima et al. (2015), Senci and Junqueira et al. (2013),
Lima et al. (2011), and Cunha and Morais (2010).
Studies carried out in other countries were used to estimate CH4 emissions by termites. The total lack

savanna areas with termite mounds of Termitideae family, conditions that most closely mimicked those
in Brazilian Cerrado. Although the relation between termite population weight and CH4 emissions is
widely used, estimates considering the CH4 emissions per area of mound are assumed more realistic
(Brümmer et al., 2009; Jamali et al., 2011a). In this respect, we opted for studies with measurements
by a unit of area.
3. Results
We estimated that 13.8±3.2 million ha of pastures in Brazilian Cerrado are low to moderately
degraded, whilst 15.4±2.8 and 3.0±1.6 million ha are in high and very high degradation levels,
respectively (Table 1). Thus, at least 50% of the degraded pastures are in advanced degradation
stages. Levels of infestation by mound-building termites notably vary in degraded pastures of
Brazilian Cerrado (Table 2). We assumed a bottom limit of 70 mounds haassociated with a high
degradation level, estimating an infestation of 145.1±48.3 mounds ha. For degraded pastures in
the very high level, a minimum number of 200 mounds hawas assumed, with a mean infestation
of 398.7±107.3 mounds ha (Table 2). The mean basal area of termite mounds in Brazilian Cerrado
pastures is 0.59±0.33 m2 (Table 3). Thus, we estimated that in a high degradation level, termite
mounds represent 0.9% of the total area, whilst in very high degradation level, they occupy 2.4% of
the pasture area. Consequently, termite mounds could occupy 204,000 ha in severely degraded
pastures from Brazilian Cerrado.
Figure 1 - Pastures in Brazilian Cerrado (adapted from Andrade et al., 2014) and locations of the studies available
in literature and used in each step of this assessment.
Degraded pastures
Non-degraded pastures
Degradation levels
Termites infestation
Area of mounds

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
4
Mean annual CH4 emissions by mound-building termites are 0.311±0.17 kg m (Table 4). Using the
previously mentioned results, we estimated that termites in degraded Cerrado pastures could emit
0.56 Tg CH4 yr, 0.364±0.022 Tg CH4 yr from pastures in a high level and 0.195±0.028 Tg CH4 yr from
pastures in a very high degradation level (Figure 2). The CH4 emissions by mound-building termites
in degraded pastures from Cerrado could represent 3% of the GHG emissions of Brazilian agriculture
(Figure 3), surpassing 11 Mt CO2 eq. yr.
Table 1 - Degradation levels in Cerrado pastures
Reference Origin Degradation level (%)
Low to moderate High Very high
Moreira and Assad (2000) DF 54 39 7
Nascimento et al. (2006) MG 37 56 6
Miranda et al. (2012) MS 37 48 15
Mean 42.7±9.8 47.7±8.5 9.3±4.9
Cerrado (million ha)113.8±3.2 15.4±2.8 3.0±1.6
MS - Mato Grosso do Sul State; DF - Distrito Federal; MG - Minas Gerais State.
1 Considering an area of 54 million ha of pasture in Cerrado, of which 60% are degraded (Andrade et al., 2014).
Table 2 - Levels of infestation by mound-building termites in Cerrado pastures in different degradation levels
Reference Origin Mounds ha
High degradation
Valério (1995) Mato Grosso do Sul 200
Czepak et al. (2003) Goiás 73
Valério et al. (2006) Mato Grosso do Sul 170
Cunha and Morais (2010) Goiás 182
Cunha (2011) Goiás 196
Lima et al. (2011) Mato Grosso do Sul 128.5
Senci and Junqueira (2013) São Paulo 113
Lima et al. (2015) Mato Grosso do Sul 98
Mean 145.1±48.3
Very high degradation
Valério et al. (2006) Mato Grosso do Sul 287
Oliveira et al. (2011) Goiás 408
Oliveira et al. (2011) Goiás 501
Mean 398.7±107.3
Table 3 - Mean basal area of termite mounds in Cerrado pastures
Reference Origin Area (m²)
Valério (1995) Mato Grosso do Sul 0.50
Czepak et al. (2003) Goiás 0.53
Cunha and Morais (2010) Goiás 0.96
Cunha (2011) Goiás 1.05
Benito et al. (2007) Distrito Federal 0.23
Oliveira et al. (2011) Goiás 0.16
Lima et al. (2015) Mato Grosso do Sul 0.71
Mean 0.59±0.33

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The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
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5
4. Discussion
It was estimated that 46-63% of the degraded pastures in Brazilian Cerrado may be in a high or
very high degradation level (Table 1). Pastures occupy 54 million ha in Cerrado (Sano et al., 2008),
where approximately 60% is degraded (Andrade et al., 2014). Our assessment corroborates studies of
Miranda et al. (2012) and Nascimento et al. (2006), both concluding that about 65% of the evaluated
pastures was moderate to highly degraded. Moreover, Moreira and Assad (2000) highlighted that
at least 45% of the Brazilian Cerrado pastures were in advanced degradation stages. The severe
Table 4 - Mean annual emissions of CH4 by mound-building termites
Reference1Origin CH4 (kg m yr)
Khalil et al. (1990) Australia 0.639
Brümmer et al. (2009) Burkina Faso 0.246
Brümmer et al. (2009) Burkina Faso 0.345
Jamali et al. (2011a) Australia 0.423
Jamali et al. (2011b) Australia 0.159
Jamali et al. (2011b) Australia 0.236
Jamali et al. (2011b) Australia 0.130
Mean 0.311±0.17
1 Values obtained under savanna conditions in termite mounds of the Termitideae family.
Currently, 60% of the pastures in Cerrado are degraded (1). We divided this area in different degradation levels (2) and estimated the average
incidence of termite mounds for each one of these levels (3). Posteriorly, we estimated the average area occupied by each termite mound and
used this value to calculate the total area occupied by termite mounds in degraded Cerrado pastures (4). Finally, using the available estimates
of CH4 emissions by mound-building termites in savanna regions and the total area occupied by termite mounds estimated in this research,
we estimated the CH4 emissions by mound-building termites in degraded Cerrado pastures.
Figure 2 - Step-by-step of the estimation of CH4 emissions by mound-building termites in degraded pastures of
Brazilian Cerrado.
step 1
step 2
step 3
step 4
step 5
Brazilian Cerrado Area: 204.7 Mha
Pasture land use: 54.01 Mha
32.4 Mha of degraded pastures
High
15.44±2.8 Mha
Very high
3.02±1.6 Mha
0.56 Tg CH4 yr−1
145.1±48.3
mounds ha−1
132,638±7,892 ha 71,281±10,163 ha
0.364±0.022
Tg CH4 yr−1
0.195±0.028
Tg CH4 yr−1
0.59±0.33 m2 mounds−1
0.311±0.17 kg CH4 m−2 yr−1
398.7±107.3
mounds ha−1

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The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
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degradation scenario observed in most pastures brought out concerns about the sustainability of
livestock production in Brazilian Cerrado, besides reiterating the importance of national policies to
improve pasture conditions, such as the ABC Program.
                
and soil. Currently, there is no agreement in relation to the trustworthiness and feasibility of these
indicators, as well as the closeness of the association between them and the degradation process.
Mound-building termites are consumers of dead grass residues. Thus, in pastures approaching the
   
Furthermore, there is a large incidence of termites in soils undergoing advanced degradation
stages (Oliveira et al., 2012). Boddey et al. (2004) suggested that at least 50% of Brazilian pastures
were in advanced degradation stages, with low grass yield and soil cover, invaded by weeds, and
in many cases densely occupied by termite mounds. In addition, in degraded Cerrado pastures,
the mound-building termite population is usually high (Lima et al., 2015). According to Cunha
and Morais (2010), the density increment of termite mounds in pastures could occur due to the
homogeneity of the environment and less competitors/predators. Finally, the conversion of
native vegetation to pastures, coupled with pasture aging and degradation, can create a favorable
environment to drastically increase the population of some termite species in Brazilian Cerrado
(Carrijo et al., 2009). Thus, despite the contentious relationship between termite infestation and
pasture degradation (Lima et al., 2011), all this evidence supports that termite infestation is a
reliable indicator of pasture degradation in Brazilian Cerrado.
Severely degraded pastures in Brazilian Cerrado are densely infested by mound-building termites,
which we estimate to have 145.1±48.3 and 398.7±107.3 mounds ha under high and very high
degradation levels, respectively. Estimating the infestation level and number of mound-building
termites in Cerrado pastures, Oliveira et al. (2011) evaluated areas of 5 ha and found between 195
and 672 mounds ha. Lima et al. (2015) and Cunha (2011) observed lower values, 68-127 and
196 mounds ha, respectively. Finally, in a study carried out in 133 municipalities across Brazilian
Cerrado, Czepak et al. (2003) obtained a mean of 73 mounds ha, with a minimum of 3 mounds ha
and values reaching a maximum of 500 mounds ha. The notable variability of infestation levels
Scenario A represents values currently accounted (MCTI, 2014), whilst scenario B also includes the emissions by mound-building termites in
degraded pastures of Brazilian Cerrado estimated in this study.
Figure 3 - Greenhouse gas emissions from Brazilian agriculture by sources (Mt CO2 eq.).
1%
1%
2% 2%
5%
5%
36%
35%
56%
54%
Scenario A Scenario B
3%
Enteric fermentation
Agricultural soils
Waste management
Rice cultivation
Burning of residues
Enteric fermentation
Agricultural soils
Waste management
Rice cultivation
Burning of residues
Termites in pastures

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
7
observed in these studies emphasize that the use of a general mean disregarding the degradation level
would jeopardize the reliability of our assessment.
             
(Table 3). In a widespread assessment, Czepac et al. (2003) observed an average basal area of
0.53 m2. However, Cunha (2011) concluded that the mean basal area of termite mound was 1.05 m2.
More recently, Lima et al. (2015) published a value of 0.71 m2 for basal area of the termite mounds in
  
are not well established. However, in more mature pastures, which commonly are in a more advanced
degradation stage, termite mounds are usually older and have a larger basal area. Accordingly, as well
as with the infestation level, the basal area of the termite mound may be used as an indicator of pasture
degradation in further assessments.
Besides CH4 emissions, impacts associated with the presence of termites in pastures range from the
fact that the mounds could be shelters for venomous animals to damage associated with grazing
area losses. However, several studies have reported that infestation by mound-building termites does

0.1% (Lima et al., 2011) to 2.06% (Cunha, 2011) of the total grazing area. Considering the estimates
from Table 3, termites are associated with grazing area losses of 132,628±7,892 ha under a high
degradation level and 71,281±10,163 ha in pastures under a very high degradation level. Therefore,
termite mounds could occupy an area larger than 200,000 ha in degraded pastures of Brazilian
Cerrado, a remarkable loss that deserves more attention. In addition, in a scenario of land-use change
of pastures to other crops, such as sugarcane and soybean (Lapola et al., 2014), any loss of grazing
area must be considered.
Emissions of CH4 by mound-building termites are determined by the balance between CH4 production
and CH4 oxidation after release. Considering that there is no evidence that the intestines of these
insects contain microbes that oxidize CH4 (methanotroph), the CH4 produced is directly released to
the environment. However, the microbes present in the material that makes up the termite mound can
act as a CH4 sink, by the oxidation of this GHG (Brümmer et al., 2009; Nauer et al., 2018). Thus, CH4
emissions could be greater if these methanotrophic organisms were not present in termite mounds,
although the dynamics of this process, as well as the community responsible for the phenomenon, are
not yet fully known (Chiri et al., 2020). In this way, estimates that consider the balance of CH4
at the surface of the termite mounds assessed by chambers (e.g., studies of Table 4) are much more

(Brümmer et al., 2009; Jamali et al., 2011a).
Termite species from the Cornitermes genus are the main responsible for the construction of epigeal
mounds in Brazilian pastures, occupying 94% of the termite mounds in Cerrado (Valério et al.,
2006). The predominant species of mound-building termites are Cornitermes cumulans, C. bequaerti,
C. silvestrii, and Syntermes Holmgren, all included in the Termitidea family. In Brazil, studies have
estimated CH4 emissions by termites after deforestation in Amazonia (e.g., Martius et al., 1993). In
these cases, termites are usually from other genera, consume the remaining biomass after burning,
and do not build mounds. In this sense, using data from other savanna regions to estimate the CH4
emissions of mound-building termites in Cerrado pastures, within the options available, is the most
feasible and realistic approach.
We estimated annual CH4 emissions of 0.311±0.17 kg m by mound-building termites in other savanna
regions (Table 4). The amplitude of termite CH4 emissions are still debatable, and few estimates were
carried out on national or biome scales. From the previous results mentioned, we estimated that
termites present in degraded Cerrado pastures could emit 0.56 Tg CH4 yr (Figure 2). Because the
             
assessment of CH4 emissions by termites in degraded pastures of Brazilian Cerrado are comparable
with those from the African (0.9 Tg CH4 yr; Brümmer et al., 2009) and Australian (1.1 Tg CH4 yr;
Jamali et al., 2011b) savannas.

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
8
The inclusion of CH4 emissions by mound-building termites could impact GHG emissions by agriculture
in Brazil (Figure 3). Disregarding emissions associated with deforestation and land-use change,
Brazilian agriculture was responsible for the direct emission of 441 Mt CO2 eq. in 2012 (MCTI, 2014).
However, this calculation did not consider the CH4 emissions by mound-building termites in degraded
pastures, which in our assessment is associated to emissions greater than 11 Mt CO2 eq. yr. When
scenario A (without termite emission) is compared with scenario B (including termite emissions), it is
possible to notice that GHG emissions by termites exceed those from rice cropping and residue burning
in Brazil (Figure 3).
We are sure that the lack of experimental data and all assumptions through our calculations jeopardize
 
about CH4 emissions are prone to bias, since GHG emissions are known to be highly dependent on
environmental constraints. In this sense, despite the limitations discussed above, the data presented
in our research aim to show the likely direction and relative magnitudes of CH4 emissions by termites
in Brazilian pastures. Moreover, it is an indisputable evidence about the need for carrying out studies
regarding these emissions and their possible contribution to C footprint of Brazilian beef or even to
C savings in recovered pastures. The CH4 emissions could be greater or smaller than estimated here,
but this approximation would be a starting point for research development regarding the neglected
contribution of mound-building termites on CH4 emissions in Brazilian pastures.
5. Conclusions
The large population of mound-building termites generally observed in degraded pastures must not
be ignored. It is estimated that termite mounds occupy an area larger than 200,000 ha in Cerrado
pastures, an important grazing area loss considering the current scenario of land-use change of
pasture to other crops in Brazil. Additionally, based on previous reports, our estimates indicate that
the degradation of pastures is associated with the inclusion of a new component in the C balance
of these areas: termites. Mound-building termites in degraded pastures could be associated to CH4
emissions greater than 11 Mt CO2 eq. yr, which can notably affect the GHG balance of grass-fed cattle
     4 emissions by
mound-building termites and their contribution to C footprint of Brazilian beef or even to C savings
in recovered pastures.
The large and increasing role CH4 plays in climate change, in particular on a shorter timescale,
makes emission reductions imperative. Assuming the relationship between termite infestation and
pasture degradation, CH4 emissions by mound-building termites in Cerrado pastures are mitigatable.
In this sense, the restoration of additional 15 million ha of degraded pastures by 2030 suggested
in the Brazilian iNDC would have an additional C saving. Pasture recovery drastically reduce the
mound-building termite population and, therefore, the associated CH4 emissions. Better emission
inventories are mandatory to include the role of termites in GHG emissions of Cerrado pastures or
even to account for CH4 emissions mitigated by the reduction of mound-building termite population
in recovered pastures. In the near future, we believe that CH4 termite emissions mitigated by pasture
recovery may be accounted for Brazil to achieve the iNDC commitments.


Author Contributions
Conceptualization: D.M.S. Oliveira, E.M. Araújo and E.F. Frade Junior. Data curation: D.M.S. Oliveira,
E.M. Araújo, E.F. Frade Junior and L.G. Pimentel. Formal analysis: D.M.S. Oliveira. Funding acquisition:
C.E.P. Cerri. Methodology: D.M.S. Oliveira and E.M. Araújo. Supervision: C.E.P. Cerri. Validation:

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
9
D.M.S. Oliveira. Writing-original draft: D.M.S. Oliveira, E.M. Araújo, E.F. Frade Junior, L.G. Pimentel and
C.E.P. Cerri. Writing-review & editing: D.M.S. Oliveira.
Acknowledgments
The authors gratefully thank the Instituto Federal de Educação, Ciência e Tecnologia Goiano (IF Goiano)

References
Andrade, R. G.; Teixeira, A. H. C.; Leivas, J. F.; Bayma-Silva, G.; Nogueira, S. F.; Victoria, D. C.; Vicente, L. E. and
Bolfe, E. L. 2014. EMBRAPA: Sistema de Observação e Monitoramento da Agricultura no Brasil. Pastagens
degradadas no Cerrado – Cenário 3. Available at: <http://mapas.cnpm.embrapa.br/somabrasil/webgis.html>. Accessed
on: Apr. 18, 2020.
Benito, N. P.; Brossard, M.; Constantino, R. and Becquer, T. 2007. Densidade de ninhos epígeos de térmitas em
uma área de Cerrado, Planaltina, DF. In: Anais do VIII Congresso de Ecologia do Brasil. Sociedade de Ecologia do
Brasil, Caxambu. Available at: <http://www.seb-ecologia.org.br/revistas/indexar/anais/viiiceb/pdf/862.pdf>. Accessed
on: June 5, 2020.
Boddey, R. M.; Macedo, R.; Tarré, R. M.; Ferreira, E.; Oliveira, O. C.; Rezende, C. P.; Cantarutti, R. B.; Pereira, J. M.; Alves,
B. J. R. and Urquiaga, S. 2004. Nitrogen cycling in Brachiaria pastures: the key to understanding the process of pasture
decline. Agriculture Ecosystem and Environment 103:389-403. https://doi.org/10.1016/j.agee.2003.12.010
Brasil. Ministério da Agricultura, Pecuária e Abastecimento. 2012. Plano setorial de mitigação e de adaptação
às mudanças climáticas para a consolidação de uma economia de baixa emissão de carbono na agricultura.
MAPA, Brasília. Available at: <https://www.gov.br/agricultura/pt-br/assuntos/sustentabilidade/plano-abc/arquivo-
publicacoes-plano-abc/download.pdf>. Accessed on: Apr. 18, 2020.
Brümmer, C.; Papen, H.; Wassmann, R. and Brüggemann, N. 2009. Fluxes of CH4 and CO2 from soil and termite
mounds in south Sudanian savanna of Burkina Faso (West Africa). Global Biogeochemestry Cycles 23:1-13.
https://doi.org/10.1029/2008GB003237
Carrijo, T. F.; Brandão, D.; Oliveira, D. E.; Costa, D. A. and Santos, T. 2009. Effects of pasture implantation on the
termite (Isoptera) fauna in the Central Brazilian Savanna (Cerrado). Journal of Insect Conservation 13:575-81.
https://doi.org/10.1007/s10841-008-9205-y
Chiri, E.; Greening, C.; Lappan, R.; Waite, D. W.; Jirapanjawat, T.; Dong, X.; Arndt, S. K. and Nauer, P. A. 2020. Termite
mounds contain soil-derived methanotroph communities kinetically adapted to elevated methane concentrations. The
ISME Journal 14:2715-2731. https://doi.org/10.1038/s41396-020-0722-3
Cunha, H. F. 2011. Distribuição espacial de cupinzeiros epígeos de pastagem no município de Iporá-GO, Brasil.
EntomoBrasilis 4:45-48. https://doi.org/10.12741/ebrasilis.v4i2.116
Cunha, H. F. and Morais, P. P. A. M. 2010. Relação espécie-área em cupinzeiros de pastagem, Goiânia-GO, Brasil.
EntomoBrasilis 3:60-63. https://doi.org/10.12741/ebrasilis.v3i3.102
Czepak, C.; Araújo, E. A. and Fernandes, P. M. 2003. Ocorrência de espécies de cupins de montículo em pastagens no
estado de Goiás. Pesquisa Agropecuária Tropical 33:35-38.
Dlugokencky, E. 2020. Carbon Cycle Greenhouse Gases: Trends in CH4. Global Monitoring Laboratory, National
Oceanic and Atmospheric Administration. Available at: <www.esrl.noaa.gov/gmd/ccgg/trends_ch4/>. Accessed on:
May 18, 2020.
Grieco, M. A. B.; Cavalcante, J. J. V.; Cardoso, A. M.; Vieira, R. P.; Machado, E. A.; Clementino, M. M.; Medeiros, M. N.;
Albano, R. N.; Garcia, E. S.; Souza, W.; Constantino, R. and Martins, O. B. 2013. Microbial community diversity in the
gut of the South American termite Cornitermes cumulans (Isoptera: Termitidae). Microbial Ecology 65:197-204.
https://doi.org/10.1007/s00248-012-0119-6
iNDC Brazil. 2015. Intended nationally determined contribution towards achieving the objective of the United
Nations Framework Convention on Climate Change. Brazilian Ministry of Foreign Affairs, Brasília. Available at:
<http://www.itamaraty.gov.br/images/ed_desenvsust/BRAZIL-iNDC-english.pdf>. Accessed on: May 18, 2020.
Jamali, H.; Livesley, S. J.; Dawes, T. Z.; Cook, G. D.; Hutley, L. B. and Arndt, S. K. 2011a. Diurnal and seasonal variations in
CH4               
Meteorology 151:1471-1479. https://doi.org/10.1016/j.agrformet.2010.06.009
Jamali, H.; Livesley, S. J.; Dawes, T. Z.; Cook, G. D.; Hutley, L. B. and Arndt, S. K. 2011b. Termite mound emissions of CH4
and CO2 are primarily determined by seasonal changes in termite biomass and behavior. Oecologia 167:525-534.
https://doi.org/10.1007/s00442-011-1991-3

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
10
                     
trace gases: CH4, CO2, CHCL3, N2O, CO, H2, and light hydrocarbons. Journal of Geophysical Research: Atmospheres
95:3619-3634. https://doi.org/10.1029/JD095iD04p03619
Lapola, D. M.; Martinelli, L. A.; Peres, C. A.; Ometto, J. P. H. B.; Ferreira, M. E.; Nobre, C. A.; Aguiar, A. P. D.;
Bustamante, M. M. C.; Cardoso, M. F.; Costa, M. H.; Joly, C. A.; Leite, C. C.; Moutinho, P.; Sampaio, G.; Strassburg, B. B.
N. and Vieira, I. C. G. 2014. Pervasive transition of the Brazilian land-use system. Nature Climate Change 4:27-35.
https://doi.org/10.1038/nclimate2056
Lima, S. S.; Alves, B. J. R.; Aquino, A. M.; Mercante, F. M.; Pinheiro, E. F. M.; Sant’Anna, S. A. C.; Urquiaga, S. and Boddey,
R. M. 2011. Relação entre a presença de cupinzeiros e a degradação de pastagens. Pesquisa Agropecuária Brasileira
46:1699-1706. https://doi.org/10.1590/S0100-204X2011001200016
Lima, S. S.; Ceddia, M. B.; Zuchello, F.; Aquino, A. M.; Mercante, F. M.; Alves, B. J. R.; Urquiaga, S.; Martius, C. and
Boddey, R. M. 2015. Spatial variability and vitally of epigeous termite mounds in pastures of Mato Grosso do Sul,
Brazil. Revista Brasileira de Ciência do Solo 39:49-58. https://doi.org/10.1590/01000683rbcs20150326
Martius, C. R.; Wassmann, R.; Thein, U.; Bandeira, A.; Rennenberg, H.; Junk, W. and Seiler, W. 1993. Methane emission
from wood-feeding termites in Amazonia. Chemosphere 26:623-632. https://doi.org/10.1016/0045-6535(93)90448-E
MCTI - Ministério da Ciência, Tecnologia e Inovação. 2014. Estimativas anuais de emissões de gases de efeito estufa
no Brasil. MCTI, Brasília. Available at: <https://sirene.mctic.gov.br/portal/export/sites/sirene/backend/galeria/
arquivos/2018/10/11/Estimativas_2ed.pdf>. Accessed on: June 1, 2020.
Miranda, C. S.; Lima, D. L. and Paranhos Filho, A. C. 2012. Diagnóstico dos níveis de degradação das pastagens com o uso
geotecnologias. In: III Seminário de Gestão Ambiental na Agropecuária. Bento Gonçalves, RS.

    
m16c.sid.inpe.br/col/dpi.inpe.br/vagner/2000/07.04.15.16/doc/008.pdf>. Accessed on: June 1, 2020.
Nascimento, M. C.; Riva, R. D. D.; Chagas, C. S.; Oliveira, H.; Dias, L. E.; Fernandes Filho, E. I. and Soares, V. 2006.
                
Engenharia Agrícola e Ambiental 10:196-202. https://doi.org/10.1590/S1415-43662006000100029
Nauer, P. A.; Hutley, L. B. and Arndt, S. K. 2018. Termite mounds mitigate half of termite methane emissions.
Proceedings of the National Academy of Sciences 115:13306-13311. https://doi.org/10.1073/pnas.1809790115
                        
solo em virtude de construções termíticas no norte de Tocantis. Revista Engenharia na Agricultura 20:118-130.
https://doi.org/10.13083/reveng.v20i2.179
Oliveira, M. I. L.; Brunet, D.; Mitja, D.; Cardoso, W. S.; Benito, N. P.; Guimarães, M. F. and Brossard, M. 2011. Incidence
of epigeal nest-building termites in Brachiaria pastures in the Cerrado. Acta Scientiarum. Agronomy 33:181-185.
https://doi.org/10.4025/actasciagron.v33i1.7075
Rasmussen, R. A. and Khalil, M. A. K. 1983. Global production of methane by termites. Nature 301:700-702.
https://doi.org/10.1038/301700a0
Sano, E. E.; Rosa, R.; Brito, J. L. and Ferreira, L. G. 2008. Mapeamento semidetalhado do uso da terra do Bioma Cerrado.
Pesquisa Agropecuária Brasileira 43:153-156. https://doi.org/10.1590/S0100-204X2008000100020
Santos, R. S. M.; Oliveira, I. P.; Morais, R. F.; Urquiaga, S. C.; Boddey, R. M. and Alves, B. J. R. 2007. Componentes da
parte aérea e raízes de pastagens de Brachiaria spp. em diferentes idades após a reforma, como indicadores de
produtividade em ambiente de Cerrado. Pesquisa Agropecuária Tropical 37:119-124. https://www.revistas.ufg.br/
pat/article/view/1837
Saunois, M.; Stavert, A. R.; Poulter, B.; Bousquet, P.; Canadell, J. G.; Jackson, R. B.; Raymond, P. A.; Dlugokencky, E. J.;
Houweling, S.; Patra, P. K.; Ciais, P.; Arora, V. K.; Bastviken, D.; Bergamaschi, P.; Blake, D. R.; Brailsford, G.; Bruhwiler, L.;
Carlson, K. M.; Carrol, M.; Castaldi, S.; Chandra, N.; Crevoisier, C.; Crill, P. M.; Covey, K.; Curry, C. L.; Etiope, G.; Frankenberg,
C.; Gedney, N.; Hegglin, M. I.; Höglund-Isaksson, L.; Hugelius, G.; Ishizawa, M.; Ito, A.; Janssens-Maenhout, G.; Jensen, K.
M.; Joos, F.; Kleinen, T.; Krummel, P. B.; Langenfelds, R. L.; Laruelle, G. G.; Liu, L.; Machida, T.; Maksyutov, S.; McDonald, K.
C.; McNorton, J.; Miller, P. A.; Melton, J. R.; Morino, I.; Müller, J.; Murguia-Flores, F.; Naik, V.; Niwa, Y.; Noce, S.; O’Doherty,
S.; Parker, R. J.; Peng, C.; Peng, S.; Peters, G. P.; Prigent, C.; Prinn, R.; Ramonet, M.; Regnier, P.; Riley, W. J.; Rosentreter, J. A.;
Segers, A.; Simpson, I. J.; Shi, H.; Smith, S. J.; Steele, L. P.; Thornton, B. F.; Tian, H.; Tohjima, Y.; Tubiello, F. N.; Tsuruta, A.;
Viovy, N.; Voulgarakis, A.; Weber, T. S.; van Weele, M.; van der Werf, G. R.; Weiss, R. F.; Worthy, D.; Wunch, D.; Yin, Y.; Yoshida,
Y.; Zhang, W.; Zhang, Z.; Zhao, Y.; Zheng, B.; Zhu, Q.; Zhu, Q. and Zhuang, Q. 2020. The global methane budget 2000–2017.
Earth System Science Data 12:1561-1623. https://doi.org/10.5194/essd-12-1561-2020
       
Cornitermes              
       
Sic08/Resumo/2013820_10133_375705409_resahy.pdf>. Accessed on: June 5, 2020.

R. Bras. Zootec., 50:e20200185, 2021
The neglected contribution of mound-building termites on CH4 emissions in Brazilian pastures
Oliveira et al.
11
Silva, R. O.; Barioni, L. G.; Hall, J. A. J.; Matsuura, M. F.; Albertini, T. Z.; Fernandes, F. A. and Moran, D. 2016. Increasing
beef production could lower greenhouse gas emissions in Brazil if decoupled from deforestation. Nature Climate
Change 6:493-497. https://doi.org/10.1038/nclimate2916
Spain, J. M. and Gualdrón, R. 1988. Degradación y rehabilitación de pasturas. p.269-283. In: VI Reunión del Comité
Asesor de la Red Internacional de Evaluación de Pastos Tropicales. Centro Internacional de Agricultura Tropical, Cali.
Valério, J. R. 1995. Ocorrência, danos e controle de cupins de montículo em pastagens. p.52-57. In: V Reunião Sul-Brasileira
de Insetos de Solo. EMBRAPA-CPAO, Dourados. (EMBRAPA-CPAO. Documentos, 8). Available at: <https://ainfo.cnptia.
embrapa.br/digital/bitstream/item/38991/1/DOC8-1995.pdf>. Accessed on: June 5, 2020.
Valério, J. R.; Barbosa, L. R.; Pereira, A. A. and Oliveira, M. C. M. 2006. Percentual de cupinzeiros abandonados em
pastagens de Brachiaria decumbens altamente infestadas por Cornitermes cumulans (Kollar) (Isoptera: Termitidae).
In: Anais da 43ª Reunião Anual da Sociedade Brasileira de Zootecnia. Sociedade Brasileira de Zootecnia, João Pessoa.