Science of the Total Environment 755 (2021) 142442

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Science of the Total Environment

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Long term effects of fire on the soil greenhouse gas balance of an

old-growth temperate rainforest
Jorge F. Perez-Quezada a,b,⁎, Paul Urrutia a, Javiera Olivares-Rojas a, Ana Meijide c,
Enrique P. Sánchez-Cañete d,e, Aurora Gaxiola b,f,g
a
Department of Environmental Science and Renewable Natural Resources, University of Chile, Casilla 1004, Santiago, Chile
b
Institute of Ecology and Biodiversity, Alameda 340, Santiago, Chile
c
Department of Crop Sciences, Division Agronomy, University of Göttingen, 37075 Göttingen, Germany
d
Department of Applied Physics, University of Granada, 18071 Granada, Spain
e
Centro Andaluz de Medio Ambiente (IISTA-CEAMA), Granada, Spain
f
Departamento de Ecología, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile
g
Centro de Cambio Global, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• The burned site had a shallower water

table and more variable soil water con-
tent.
• The unburned forest soil emitted more
CO2 and captured more CH4 than the
burned site.
• Nitrous oxide fluxes showed no sea-
sonal variability and no difference be-
tween sites.
• The unburned forest soil emitted signif-
icantly more GHGs than the burned site.
• At the ecosystem level, the burned site
was a source of GHGs.

a r t i c l e i n f o a b s t r a c t

Article history: Forest fires can cause great changes in the composition, structure and functioning of forest ecosystems. We stud-
Received 14 May 2020 ied the effects of a fire that occurred >50 years ago in a temperate rainforest that caused flooding conditions in a
Received in revised form 11 September 2020 Placic Andosol to evaluate how long these effects last; we hypothesized that the effects of fire on the soil green-
Accepted 14 September 2020
house gas (GHG) balance could last for many years. We made monthly measurements of fluxes of carbon dioxide
Available online 21 September 2020
(CO2), methane (CH4) and nitrous oxide (N2O) during two years of soils in an unburned forest (UF) and a nearby
Editor: Paulo Pereira site that burned >50 years ago (BS). Our results show that CO2 emissions from soils were higher in the UF than in
the BS, and positively correlated with temperature and negatively with soil water content at both sites. Both sites
Keywords: were net CH4 sinks (higher in the UF) and fluxes correlated positively with soil water content and negatively with
South America temperature (stronger relation in the BS). Emissions of N2O were low at both sites and showed correlation with
Northern Patagonia friction velocity at the UF site. The soil GHG balance showed that the UF emitted about 80% more than the BS
Environmental drivers (5079 ± 1772 and 2815 ± 1447 g CO2-eq m−2 y−1, respectively). Combining our measured fluxes with data
Fire perturbation of CO2 net ecosystem exchange, we estimated that at the ecosystem level, the UF was a GHG sink while the BS
Greenhouse gas budget
was a source, showing a long-lasting effect of the fire and the importance of preserving these forest ecosystems.
Old-growth forest
© 2020 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Department of Environmental Science and Renewable Natural Resources, University of Chile, Casilla 1004, Santiago, Chile.
E-mail address: jorgepq@uchile.cl (J.F. Perez-Quezada).

https://doi.org/10.1016/j.scitotenv.2020.142442
0048-9697/© 2020 Elsevier B.V. All rights reserved.
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al.
1. Introduction
Biogenic greenhouse gases (GHG) are generated by the biological ac-
tivity of all living organisms; the three most important GHG are carbon
dioxide (CO2), methane (CH4) and nitrous oxide (N2O). Anthropogenic
activities such as land use changes, nutrient additions and degradation
of natural ecosystems generally result in large changes in the biogenic
GHG balance as a result of vegetation and soil alteration (Ojima et al.,
1994; Schaufler et al., 2010; Tian et al., 2016). Changes in soil structure
and chemical properties determine whether soils act as GHG sources or
sinks through the effects of the soil environment on the metabolic activ-
ity of soil microorganisms, microfauna and root respiration
(Butterbach-Bahl et al., 2013; Chapin III et al., 2011; Lai, 2009). There-
fore, estimating soil GHG emissions in natural ecosystems is key to
gauging the importance of conservation policies for climate mitigation.
Forest fires are among the most important disturbance events (Seidl
et al., 2017) shaping species composition, structure, and biogeochemis-
try of forest ecosystems (Ribeiro-Kumara et al., 2020). Forest fires also
affect the GHG balance of these ecosystems, with consequences for cli-
mate change (Kim and Tanaka, 2003; Köster et al., 2017). However, cur-
rent evidence shows that the behavior of soil GHG fluxes after forest
fires follows different trajectories. For example, a fire-chronosequence
study in boreal forests in Canada showed that soil CO2 emissions in-
creased with time after the fire, CH4 consumption increased after
25 years, whereas GHG emissions between treatments remained un-
changed 46 years after the fire, suggesting that GHG balances may
take long time to recover (Köster et al., 2017; Ribeiro-Kumara et al.,
2020). Another study on the impact of fire on soil GHG fluxes in a trop-
ical grassland in Congo found contrasting short-term and long-term re-
sults (Castaldi et al., 2010). One month after burning the burned soil
showed significantly lower CO2 emissions than in unburned plots,
burned soils shifted from a net source to a net sink (although weak) of
CH4, while no difference was observed for N2O flux. However, eight
months after burning none of the GHG fluxes differed among plots
(Castaldi et al., 2010). A controlled fire experiment quantified post-fire
gaseous nitrogen (N) losses (i.e. N2O, NO and N2) in an old shrubland
in central Spain, and showed that N2O emissions were doubled by burn-
ing, and one year post-fire gaseous soil N losses were significant in com-
parison to direct combustion losses (Dannenmann et al., 2018). The
effects of climate change add more uncertainty to the predicted changes
in GHG fluxes after forest fires. A study that experimentally increased air
temperature and reduced soil humidity in a burned boreal forest stand
in China reported that seven or eight years after the fire CO2 emissions
increased and soils switched from being CH4 sources to sinks (Song
et al., 2018). Such contrasting evidence highlights that the scarcity of
data hampers our understanding of the effects that fires can have on
the dynamics of soil GHG emissions.
Temperate rainforests of southern South America are some of the
most carbon-dense ecosystems worldwide (Perez-Quezada et al.,
2015; Urrutia-Jalabert et al., 2015). Naturally ignited wildfires are ex-
tremely rare events (Holz and Veblen, 2011), but people use fires to
clear forested lands (Armesto et al., 2009; Kitzberger and Veblen,
1999), which greatly affects soil processes (Pérez et al., 2004) and re-
generation dynamics (Albornoz et al., 2013; Diaz et al., 2007). Fires in
these environments can alter water and nutrient balances, generating
waterlogged and nutrient-poor soils where Sphagnum moss, sedge,
and fern species thrive (Cabezas et al., 2015; Leon et al., 2018; Seaman
et al., 2015) but woody species struggle to regenerate (Albornoz et al.,
2013; Diaz et al., 2008). Forest fires can also alter carbon (C) flux, as re-
ported in recent studies in southern Chile (Perez-Quezada et al., 2018;
Valdés-Barrera et al., 2019). These studies show that the net ecosystem
exchange of a burned forest site was a small C sink (−135 ± 267 g CO2
m−2 y−1) compared to a nearby old-growth forest (−873 ± 114 g CO2
m−2 y−1). The authors argued that this difference could be related to
the higher aboveground productivity present in the unburned forest
compared to the burned site. It is worth noting that the fire in this
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Science of the Total Environment 755 (2021) 142442
area occurred >50 years ago (Holz and Veblen, 2011), therefore the re-
sults reported by Perez-Quezada et al. (2018) and Valdés-Barrera et al.
(2019) suggest that fires can have long-lasting effects on ecosystem
GHG fluxes. The production of GHG fluxes is strongly dependent on
the ecosystem characteristics and therefore we need to produce accu-
rate long-term estimates of soil GHG fluxes from different environmen-
tal conditions (Bond-Lamberty et al., 2020). The effects of fire on the soil
GHG balance have not been studied in these temperate rainforests,
which may respond differently to other forests given the waterlogging
effects created by the fire. This type of study would help filling the gap
in reports about GHG fluxes from Southern Hemisphere ecosystems
(Nicolini et al., 2013; Pastorello et al., 2020).
We performed monthly measurements of soil CO2, CH4, and N2O
fluxes for over two years in an old-growth temperate rainforest and a
nearby site that suffered a human-induced fire >50 years ago (Holz
and Veblen, 2011). Considering the difference in ecosystem productiv-
ity between sites (Perez-Quezada et al., 2018; Valdés-Barrera et al.,
2019) and the waterlogged conditions caused by the fire (Diaz et al.,
2007), we expected that soil CO2 emission would be higher in the un-
burned forest (UF) compared to the burned site (BS). We expected
that the wetter soil condition in BS would increase CH4 emission and de-
crease N2O emission compared to the UF site. Therefore, our objectives
were to: 1) analyse the seasonal variability of soil GHG fluxes in both the
UF and BS; 2) evaluate the effects of environmental variables on GHG
fluxes; and 3) assess if the fire perturbation still affects soil GHG balance.
2. Methods
2.1. Study area
Soil GHG fluxes were measured in an unburned forest (UF) and a
burned site (BS), <1 km distant, in the Senda Darwin Biological Station
(Carmona et al., 2010). Senda Darwin is located on Chiloé Island, 6.5 km
from the Pacific Ocean, at 50 m elevation (41° 52′ S, 73° 40′ W) (Fig. 1),
and is part of the Chilean Long Term Socio-Ecological Research Network.
The climate is temperate with a strong oceanic influence. Meteorologi-
cal records (1998–2016) at Senda Darwin indicate an annual average
temperature of 10 °C and an average annual precipitation of
2059 mm. The vegetation in this area is mainly composed of evergreen
temperate rainforests, which have been replaced in the landscape by
secondary forests, peatlands, shrublands, grasslands, and croplands
(Carmona et al., 2010).
Both sites belong to the same soil Series, which according to Soil Tax-
onomy is classified as a Histic Placaquand and after WRB as a Placic
Andosol. Locally known as ñadi (from native language: seasonal
swamp), are waterlogged volcanic ash soils located on flat fluvial-
glacial terraces. They are characterized by a high content of organic
matter (40–80%) in the first 20 cm, have low bulk density
(0.66–0.98 Mg m−3) and are shallow to very deep (32–158 cm).
These soils include a thin placic horizon 8–65 cm deep that causes
them to be somewhat poorly drained (CIREN, 2003), be poor in nutri-
ents (Veith and Garleff, 1996) and have low pH (4.3–4.7) (Albornoz
et al., 2013).
2.2. Study sites
The UF site is a 100 ha patch of old-growth North Patagonian tem-
perate rainforest, dominated by emergent trees (up to 25 m) of Drimys
winteri Jordan Forst. & G. Forst., Podocarpus nubigenus Lindl., Nothofagus
nitida (Phil.) Krasser and Saxegothaea conspicua Lindl., while the under-
story was dominated by Tepualia stipularis (Hook. & Arn.) Griseb., which
is a tree species that bends and grows horizontally (Gutiérrez et al.,
2009). Soil depth is 52 ± 0.9 cm and stores 72.9 ± 4 kg C m−2 (N =
33; unpublished data). The site is flat (slope 1% NW), located 6 km SE
from the ocean and is surrounded by shrublands (Lat −41.8830, Long
−73.6760) (Fig. 1).
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al.
Fig. 1. Location of Senda Darwin Biological Station (black star) and views of the (a) unburned forest and (b) burned site.
The burned site (BS) is a former forest area that was dominated by
D. winteri, P. nubigenus, N. nitida, S. conspicua and Pilgerodendron
uviferum (D. Don) Florin. The forest was destroyed by fire >50 years
ago, causing soil waterlogging (Diaz et al., 2007) and the proliferation
of Sphagnum mosses (Leon et al., 2018). After the fire the area was occa-
sionally used for light grazing until 1994, when it became part of the
conservation program of Senda Darwin Biological Station. The site is
currently undergoing a secondary succession process (Albornoz et al.,
2013) with canopy height of 0.65 m, dominated by a mix of sedge,
moss, fern, and shrub species; soil depth was 38 ± 3 cm, with a C stor-
age of 11.92 ± 1.34 kg C m−2 (N = 44; Cabezas et al., 2015). The BS site
is about 26 ha, located 6.3 km SE from the ocean, with slope 0.8% and is
surrounded by native forest and grasslands (Lat −41.8790, Long
−73.6660) (Fig. 1).
2.3. Automated measurements of soil GHG fluxes and environmental
variables
Soil CO2 efflux was measured with an automated soil CO2 flux sys-
tem (model LI-8100, LI-COR, Lincoln, NE, USA; hereafter LI-COR), con-
nected to a multiplexer (model LI-8150, LI-COR), sampling 3 closed
chambers per site (20 cm diameter, model LI-8100-104, LI-COR). The
opaque chambers were installed >100 m away from the site borders,
over PVC collars buried ~10 cm into the soil. These collars stayed in
situ during the whole sampling period and were kept free of
3
Science of the Total Environment 755 (2021) 142442
photosynthetically active material by cutting the vegetation inside the
collars to ensure only soil fluxes were measured. The three chambers
were installed 15 m from the analyzer and >10 m from each other.
This system was connected in parallel to a cavity ring-down spectrom-
eter that measures CH4 and N2O concentrations (model G-2308, Picarro
Inc., Santa Clara, CA, USA) which has its own air pump, following the
recommendations of LI-COR (2016). Air temperature (Tair) and humid-
ity in the chambers were also recorded using sensors installed inside the
LI-8100-104 chambers.
We took monthly measurements from September 2014 until De-
cember 2016, but due to power supply and technical problems during
the sampling period, the available data include 24 and 23 field cam-
paigns (out of 28 possible months) in the UF and BS, respectively. We
took measurements once per hour during 24 h in each site, i.e. 2 sites × 3
chambers × 24 flux estimates × 3 gas species = 432 flux measurements
per field campaign. Each measurement lasted 8 min. Soil fluxes were es-
timated using the SoilFluxPro software of LI-COR Inc. for all three gases.
We considered fluxes from the soil to the atmosphere (source) as posi-
tive and those from the atmosphere to the soil (sink) as negative. Cumu-
lative fluxes were calculated based on trapezoidal interpolation
between measured fluxes and the interval between sampling events,
summing the interpolated fluxes for the entire measurement period.
Environmental variables were recorded as 30-minute averages dur-
ing the whole study period at both sites. Net radiation and its incoming
and outgoing short-wave and long-wave components were estimated
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al.
using a 4-component net radiometer (model NR01, Hukseflux, Delft,
The Netherlands). Photosynthetically active radiation (quantum sensor
model LI-190, LI-COR), precipitation (model 52,202, RM Young, Tra-
verse City, USA), Tair and relative humidity (model HMP155, Vaisala,
Helsinki, Finland) were also measured at the site. Soil temperature
(Tsoil, thermocouple probes TCAV, Campbell Scientific Inc., Logan,
Utah, USA; hereafter CSI), soil water content (SWC, reflectometers
model CS616, CSI) and heat flux (model HFP01, CSI) were monitored
at 5 cm depth near each closed chamber; water table depth (WTD)
was measured at each site with a pressure transducer (model CS451,
CSI). Wind speed and friction velocity were measured using sonic ane-
mometers installed at 40 m and 3 m in UF and BS, respectively (model
CSAT3, CSI).
2.4. Statistical analyses
The relation between soil GHG fluxes and environmental variables
was tested with Pearson's product-moment correlation coefficients,
using the monthly averages of each variable (N = 24 and 23 in the UF
and BS, respectively). The relation between each GHG and the environ-
mental variables with highest correlation was further analyzed using
linear regression models.
After verifying the lack of normality in all three GHG flux datasets
using Shapiro-Wilk tests, we could not consistently normalize the data
to fulfill the requirements of linear mixed effect models (Hassler et al.,
2017) or two-way repeated measures ANOVA to evaluate differences
between UF and BS. Normalization of the datasets using log or square
Fig. 2. Monthly averages of environmental variables during the study period at Senda Darwin Biological Station: a) air temperature (black line) and rainfall (gray bars); monthly averages
of environmental variables at the unburned forest (dark line) and burned site (light line): b) soil temperature at 5 cm depth (±S.E, N = 3), c) volumetric soil water content at 5 cm depth
(±S.E, N = 3), d) water table depth (negative values indicate the water table was above the soil surface).
4
Science of the Total Environment 755 (2021) 142442
root transformations led to models that showed significant differences
(P < 0.05) between sites for CO2 and CH4 fluxes, while no differences
were found for N2O fluxes. However, the impossibility of normalizing
the three GHGs with a uniform method and the lack of normality in
the model residuals made these analyses inappropriate for our datasets.
We therefore used non-parametric tests that have been used for this
type of data, the Mann-Whitney U test (similar to Meijide et al., 2020)
and the Kruskal-Wallis test (similar to Wachiye et al., 2020) to assess
differences in the medians (p-value <0.05). These analyses resulted in
similar results, in accordance with those of the linear mixed effects
models. All analyses were performed using the software R version
3.5.3 (R Core Team, 2019), particularly packages ltm and MASS.
3. Results
3.1. Monthly variation of climatic variables and soil GHG fluxes
Monthly values of Tair and precipitation varied markedly, with the
highest precipitation occurring during the coldest months (Fig. 2a).
During the first study year (September 2014–August 2015) annual av-
erage temperature was colder (8.8 °C) and wetter (2361 mm) than
the long-term average, while the second year was even colder (8.1 °C)
and very dry (1249 mm). Tsoil, SWC and WTD also varied markedly
across seasons (Fig. 2b–d). Tsoil was slightly higher in BS (Fig. 2b),
while SWC showed higher seasonal variability at this site (Fig. 2c).
WTD was shallower in BS during the whole study period and was
above ground level in some months during winter (Fig. 2d).
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al. Science of the Total Environment 755 (2021) 142442

Seasonal behavior was observed in soil CO2 and CH4 fluxes from both Table 1
sites, with greater emissions during summer and lower during winter Pearson correlation coefficients between soil GHG fluxes (CO2, CH4 and N2O) and environ-
mental variables measured monthly in an unburned forest (old-growth temperate
periods (Fig. 3). The UF soil showed greater CO2 emission, greater CH4 rainforest) and burned site in Chiloé island, Chile.
uptake, and similar N2O emission compared to the BS soil. Maximum
CO2 emissions in the UF were observed in January 2015 and February, Unburned Forest (UF) Burned site (BS)

2016 (4.80 ± 1.97 μmol CO2 m−2 s−1 and 5.78 ± 1.45 μmol CO2 Variable CO2 CH4 N2O CO2 CH4 N2O
m−2 s−1, respectively; mean ± 1 standard deviation) (Fig. 3a). Mini- Fluxes
mum fluxes were around 30% of the maximum flux of each year CO2 1 −0.72• 0.03 1 −0.77• 0.01
(1.40 ± 0.64 μmol CO2 m−2 s−1 in October 2015 and 1.78 ± CH4 −0.72• 1 −0.12 −0.77• 1 −0.02
0.79 μmol CO2 m−2 s−1 in June 2016) (Fig. 3a). Fluxes in BS followed N2O 0.03 −0.12 1 0.01 −0.02 1

the same seasonal trend, showing higher summer values compared to Radiation
winter months (e.g. in 2015, maximum 3.16 ± 0.54 μmol CO2 Rn 0.65• −0.41 −0.24 0.24 −0.19 −0.17
m−2 s−1 and minimum 0.64 ± 0.11 μmol CO2 m−2 s−1), and consis- LWin 0.13 −0.02 −0.47• −0.1 0.17 −0.06
LWout 0.50• −0.32 −0.41 0.31 −0.21 −0.26
tently lower fluxes compared to UF. The UF soil acted as a CH4 sink dur- SWin 0.52• −0.36 −0.01 0.2 −0.19 −0.1
ing the whole study period, being a large sink during summer months, SWout 0.53• −0.37 0.01 0.26 −0.27 −0.12
reaching values up to −1.38 ± 0.41 nmol CH4 m−2 s−1 during the sec- PAR 0.46 −0.32 0.11 0.22 −0.21 −0.08
ond year (Fig. 3b). The BS soil was also a CH4 sink during summer SHF 0.58• −0.34 −0.42 0.25 −0.04 0.06
months, with fluxes close to zero or slightly positive (e.g. 0.02 ± Humidity
0.1 nmol CH4 m−2 s−1 in November 2014) during the rest of the year. Rainfall −0.21 0.16 −0.28 0.16 −0.25 −0.06
Both the UF and BS soils emitted N2O during the study period, with RHair −0.09 0.09 −0.05 0.03 0.15 −0.13
RHchamber 0.63• −0.38 0.05 0.05 0.25 0.25
maximum values of 0.54 ± 0.73 nmol N2O m−2 s−1 and 1.05 ±
SWC −0.74• 0.71• −0.20 −0.66• 0.91• 0.01
1.86 nmol N2O m−2 s−1, respectively. None of our study sites showed WTD 0.79• −0.87• 0.08 0.63• −0.84• −0.14
a clear seasonal trend for soil N2O flux (Fig. 3c).
Temperature
Tchamber 0.79• −0.35 −0.35 0.54• −0.3 −0.14
3.2. Environmental controls of soil GHG fluxes at unburned forest and Tair 0.72• −0.65 −0.06 0.58• −0.54• −0.42
burned sites Tsoil 0.83• −0.44 −0.18 0.65• −0.59• −0.25

Wind
We found a negative correlation between soil CO2 and CH4 fluxes u* −0.09 0.03 0.50• −0.09 0.32 0.31
(r > 0.7) both in the UF and the BS (Table 1). Temperature seemed to U 0.11 −0.15 −0.38 0.22 −0.28 −0.27
be the most important environmental driver of CO2 flux in the UF and Rn, net radiation; LW, longwave radiation; SW, shortwave radiation; _in, incoming radia-
BS, as Tsoil showed the highest positive correlations (Table 1, Fig. 4a). tion; _out, outgoing radiation (all in W m−2); PAR, photosynthetically active radiation
We also found positive correlations with Tair inside the chamber and (μmol m−2 s−1); SHF, soil heat flux (W m−2); RH, relative humidity (%); SWC, soil
above the canopy. These thermal variables were also significant in BS water content (m3 m−3); WTD, water table depth (m); T, temperature (°C); u*, friction ve-
locity (m s−1); U, wind speed (m s −1). • depicts significant coefficients with p < 0.05. Flux
but showed lower correlations (Table 1). SWC was the most important
data from 3 closed chambers per site.
driver of CO2 flux in BS, presenting a negative relationship in both sites
(Table 1). Soil CO2 flux increased when WTD was deeper at both sites

(Table 1). The results also show a positive correlation between CO2
flux and net radiation, but only in the UF (r = 0.65); the same was ob-
served with relative humidity measured inside the chamber (r = 0.63).
In contrast to CO2 flux, SWC was the most important driver of CH4 flux,
as it was a strong and positive predictor in both sites (Table 1, Fig. 4b).
CH4 flux in the BS was negatively correlated with Tsoil (r = −0.59)
and Tair (r = −0.54); these trends were not present in the UF site. In
the UF site N2O flux was only significantly correlated with friction veloc-
ity (r = 0.50) (Table 1, Fig. 4c) and incoming longwave radiation
(−0.47); we found no other significant controls of N2O flux in the BS.

3.3. Mean fluxes and soil GHG balance

Fluxes show that the soils were a net N2O source and a CH4 sink in
both sites (Table 2). For all three GHGs, fluxes in UF were larger than
in BS. When CH4 and N2O fluxes were expressed as CO2-equivalents
per year, the balance at the soil level showed that both sites are net
sources of GHG; UF fluxes were significantly higher (about 80%) than
BS fluxes (5079 ± 1772 and 2815 ± 1447 g CO2-eq m−2 y−1, respec-
tively) (Table 2).

4. Discussion

4.1. Seasonal variation of soil GHG fluxes

Soils in the UF and BS showed contrasting seasonal variation for CO2

Fig. 3. Monthly means (±1 SD) (N = 3 closed chambers per site) of a) soil carbon dioxide and CH4 fluxes (Fig. 3) as a result of different environmental controls
(CO2), b) methane (CH4) and c) nitrous oxide (N2O) fluxes (F) in an unburned forest (old- (Table 1). Monthly soil CO2 flux showed a clear dependency on Tsoil
growth temperate rainforest, UF) and a burned site (BS) in southern Chile.
(Fig. 4a), as in both sites highest emissions were recorded during

5
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al. Science of the Total Environment 755 (2021) 142442

Chilean temperate rainforests (Urrutia-Jalabert et al., 2015; Beas et al.,

2019) as well as in our UF site (72.9 ± 4 kg C m−2, unpublished data).
CH4 showed a contrasting pattern, with soil CH4 emissions peaking
in winter (Fig. 3) likely in response to higher SWC (Fig. 4b) as winter
rainfall promotes soil waterlogging (Albornoz et al., 2013) (Fig. 2). Wa-
terlogged soil conditions observed in BS (Fig. 2d) can be partly ex-
plained by the shallower soil depth at this site, but are also likely
related to the collapse of soil pore structure reported for this type of
soil when land use changed from native forest to a naturalized grassland
(Dörner et al., 2016). Previous studies of temperate rainforests of Chiloé
Island have shown that SWC increases significantly after a disturbance,
and hydrological models confirmed that soil waterlogging is a common
consequence of disturbances in this area due to the combination of poor
soil drainage and reduced evapotranspiration (Diaz et al., 2007; Pérez
et al., 2009). CH4 uptake values in UF were higher in comparison with
other temperate and boreal forests from the Northern Hemisphere
(Table 3). Our BS site acts as a small CH4 sink, likely because the water
table in our sites is not always close to the soil surface (0.18–0.49 m in
UF and 0–0.43 m in BS). The CH4 fixing capacity of the UF site is similar
to observations from a secondary forest in southern Chile (Beas et al.,
2019), and temperate and tropical mountain forests in the Northern
Hemisphere (Table 3).
In contrast to CO2 and CH4, and in accordance with previous studies
(Beas et al., 2019), we found no seasonal trend in N2O flux (Fig. 3). N2O
fluxes in UF fell within the range reported for a temperate forest in
Germany (Luo et al., 2012) and are close to the mean of a review
study that examined eight forest sites in the Northern Hemisphere
(0.31 nmol N2O m−2 s−1, Nicolini et al., 2013).

4.2. Environmental controls of GHG fluxes

Fig. 4. Linear regression models between GHG fluxes (F) and environmental variables in
an unburned forest (UF, black squares, solid lines) and burned site (BS, gray circles,
dashed lines); a) CO2 - soil temperature (Tsoil), b) CH4 - soil water content (SWC),
c) N2O - friction velocity (u*). All lines represent significant models (p < 0.05). Pearson
correlation coefficients of the models are presented in Table 1. Flux data from 3 closed
chambers per site.
summer months (Fig. 3), which is the period of maximum metabolic ac-
tivity for above- and belowground components in temperate ecosys-
tems (Bardgett and Wardle, 2010). Soil CO2 emission from the UF is
similar to that in a secondary forest stand in southern Chile (Beas
et al., 2019) but high compared to forest ecosystems in the Northern
Hemisphere (Table 3). It is likely that the high soil CO2 emissions that
we observed are a product of the high soil C content often reported for
Different environmental factors control soil CO2 and CH4 fluxes, but
no clear picture emerges for soil N2O flux (Table 1). We found strong
positive effects of Tsoil on CO2 flux in the UF site, which was expected
considering that an increase in Tsoil is one of the major threats for soil
C sequestration (Luo et al., 2012; Wilson et al., 2016). However, in rela-
tion to SWC, our results on soil CO2 flux differ somewhat from previous
studies. For example, Luo et al. (2012) found in a temperate sub-oceanic
broadleaf forest site in Germany that experimental reductions in SWC
barely reduced CO2 flux, whereas in both of our sites SWC had a very
strong and negative effect (Pearson r = −0.74 and −0.66, respectively).
These contrasting results in temperate forest ecosystems between
hemispheres may relate to the difference in seasonal rainfall dominance
as northern temperate summers are often warm and wet, whereas
southern temperate summers are often warm and dry. This implies
that higher SWC and lower temperature in Southern Hemisphere for-
ests decrease plant and soil microbial activity during winter months,
when lower GHG fluxes are observed (Fig. 3). This is corroborated by
Beas et al. (2019), where higher CO2 emissions were observed during
the summer (dry) months in a Chilean temperate rainforest and may

Table 2
Mean ± SE soil fluxes of carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O) and their equivalent in CO2 units for 2014–2015 (Year 1) and 2015–2016 (Year 2) from an un-
burned forest (old-growth temperate rainforest) and burned site on Chiloé island, Chile.

Flux F-CO2 F-CH4 F-N2O F-CO2 F-CH4 F-N2O Soil GHG balance

Site/year μmol m−2 s−1 nmol m−2 s−1 nmol m−2 s−1 g CO2-eq m−2 y−1

Unburned forest (UF)

Year 1 3.53 ± 1.36 −0.98 ± 0.29 0.33 ± 0.42 4898 ± 1881 −14 ± 4 121 ± 155 5005 ± 2040
Year 2 3.62 ± 0.96 −0.83 ± 0.25 0.39 ± 0.46 5021 ± 1326 −12 ± 4 143 ± 171 5152 ± 1504
Mean ± SE 3.57 ± 1.16a −0.91 ± 0.27 a 0.36 ± 0.44 4960 ± 1604a −13 ± 4 a 132 ± 163 5079 ± 1772 a

Burned site (BS)

Year 1 1.93 ± 0.84 −0.24 ± 0.09 0.42 ± 0.74 2672 ± 1172 −3.4 ± 1.2 155 ± 273 2824 ± 1446
Year 2 1.90 ± 0.85 −0.23 ± 0.05 0.49 ± 0.73 2630 ± 1176 −3.3 ± 0.7 180 ± 270 2807 ± 1447
Mean ± SE 1.91 ± 0.85b −0.24 ± 0.07 b 0.46 ± 0.87 2651 ± 1173b −3.3 ± 1 b 168 ± 272 2815 ± 1447 b

Fluxes were estimated from all monthly data available (N = 24 in the unburned forest; N = 23 in the burned site). Different letters represent significant differences between the unburned
forest and the burned site fluxes (p < 0.05, Mann-Whitney U test). Flux data from 3 closed chambers per site.

6
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al. Science of the Total Environment 755 (2021) 142442

Table 3
Mean soil fluxes (F) of CO2, CH4 and N2O and GHG balance recorded in different forest types.

Forest type Country FCO₂ FCH₄ FN2O Balance Source

μmol CO₂ m−2 s−1 nmol CH₄ m−2 s−1 nmol N2O m−2 s−1 g CO2-eq m−2 year−1

Unburned forest Chile 3.53–3.62 −0.83–−0.98 0.33–0.39 5005–5152 Present study

Burned site Chile 1.90–1.93 −0.23–−0.24 0.42–0.49 2807–2824 Present study
Secondary foresta Chile 0.74–5.79 −10.05–5.19 −0.43–0.53 Beas et al., 2019
Naturalized grasslanda Chile 0.09–15.28 −17.62–7.57 −2.48–0.39 Beas et al., 2019
Temperate USA −0.364–−0.389 Dubbs and Whalen, 2010
Temperate Germany 1.85–2.43 −0.24–0.92 0.05–0.68 2584–3675 Luo et al., 2012
Old-growth temperate China 1.45 −0.45 2003 Fang et al., 2010
Temperate-boreal transitional USA −0.569–0.221 Shoemaker et al., 2014
Evergreen Italy 3.06 −0.63 ≈0 4236 Cotrufo et al., 2011; Gundersen et al., 2012
Old-growth boreal China 1.30 −0.01 1809 Fang et al., 2010
b
Tropical mountain Tanzania 0.08–0.66 −0.11–−1.06 0.01 98.8–912.4 Gütlein et al., 2017
Mountain Switzerland 1.11 −0.5–0.83 −0.03–0.07 1524–1577 Krause et al., 2013
a
Values represent range of measured fluxes, as annual values were not reported.
b
Below detection limit.

explain why in our BS site SWC exerted a strong negative control on CO2
flux. High SWC relates to a positive effect of water table depth (WTD) on
CO2 emissions (Table 1), i.e. SWC decreases when WTD increases
(moves deeper into the soil) (Fig. 2c–d).
CH4 flux in UF seem to be strongly controlled by soil water conditions
(SWC and WTD), irrespective of Tsoil (Table 1). However, these results are
in disagreement with another study (Luo et al., 2012), which found that
CH4 flux in a forest site in Germany was positively but weakly affected
by SWC and Tsoil. The effects of fire on CH4 flux are evident, as CH4 flux
at the BS site seems to be regulated by soil water conditions and temper-
ature (i.e. increases with Tsoil). Unsaturated soil conditions (Fig. 2c–d)
might explain the observed CH4 uptake in both sites, agreeing with a
study in southern Chile that found mostly negative CH4 fluxes in a second-
ary forest and naturalized grassland growing in a similar soil type (Beas
et al., 2019).
N2O flux only showed a significant correlation in UF with incoming
long-wave radiation (negative relation) and friction velocity (positive cor-
relation). We did not find other studies in the literature that have looked
at the relation of these variables to N2O flux. However, advective transport
driven by wind can provoke changes in CO2 flux (Roland et al., 2015;
Sánchez-Cañete et al., 2017; Subke et al., 2003). It is probable that a posi-
tive correlation between friction velocity and N2O flux was only detected
because soil N2O concentration was low and changes were only due to
abiotic factors such as the transport generated by diffusion and non-
diffusion processes. The N2O results confirm that this flux does not seem
to be controlled by environmental drivers, in BS at least. Although O2 con-
centration was not measured in our soils, we expect it would have been
high due to the observed CH4 consumption at both sites.
Land use change from a secondary native forest to a naturalized
grassland in an Aquand soil implies a decrease in macropores leading
to a decrease in hydraulic conductivity, a decrease in WTD, increased
SWC variations and higher summer temperatures (Dec et al., 2017). Po-
tential respiration was lower in the grassland, suggesting that aerobic
biological activity was depleted due to the aforementioned changed
conditions (Beas et al., 2019). All these environmental changes were ob-
served comparing our sites, showing that the controls of GHG in UF and
BS are complex. Better understanding of the drivers behind flux dynam-
ics of these gases may help promote better policies to improve GHG
emission mitigation. This is particularly important in Southern Hemi-
sphere temperate ecosystems that are experiencing drier and warmer
summers (Garreaud et al., 2020).
4.3. Effects of fire on the forest GHG balance at soil and ecosystem levels
While soil GHG fluxes obviously change during the post-fire recov-
ery period, there is no clear trend that describes this change. On one
hand, CO2 flux tends to decrease immediately after a fire by >50%
(Kasischke et al., 2005; Kim and Tanaka, 2003; Richter et al., 2000) but
studies have reported that reductions in CO2 flux seem to disappear
within three to five years after the fire (Köster et al., 2017; Kulmala
et al., 2014). On the other hand, as we expected, in our BS site soil CO2
flux is still 53% lower than the UF site (i.e. original ecosystem)
(Table 2). This likely relates to differences in plant community composi-
tion, greater aboveground biomass in UF compared to BS (vegetation
height 25 m and 0.65 m, respectively) and higher soil C content, the
last explained mainly by shallower soil depth at the burned site.
Similar discrepancies have been reported for the effects of fire on CH4
emissions. For example, results from a study in a boreal forest show that
CH4 emissions increased after a fire (Richter et al., 2000), but results
from an experimental fire in a temperate forest in Japan found that soil
CH4 flux can actually decrease after the manipulation (Kim et al., 2011).
Given the soil flooding conditions observed in BS after the fire (Fig. 2d),
we expected this site to be a net source of CH4. Indeed, our burned site
is classified by some authors as an anthropogenic peatland (León et al.,
2016), due to the presence of mosses and other species favored by water-
logged conditions and low soil pH. However, both of our sites are net CH4
sinks; the flux was significantly greater in UF than in BS (Table 2), which
coincides with the observations of a study of an Aquand soil that looked at
the effects of a land use change from a secondary native forest to natural-
ized grassland in Chile (Beas et al., 2019). The fact that our sites have been
under protection for 26 years may have promoted the recovery of the eco-
system function of CH4 sequestration, as suggested by the results from a
study where the influence of fire on CH4 flux lasted several decades in a
boreal forest (Köster et al., 2017).
Results from previous studies suggest that CO2 and N2O fluxes de-
crease immediately after fire but increase during ecosystem recovery.
Such increases have been associated with higher Tsoil (Richter et al.,
2000; Kim et al., 2011) or more light reaching the soil (Kim and
Tanaka, 2003). Similarly, as ecosystem recovery progresses N2O flux in-
creases as a product of C availability related to root and microbial respi-
ration (Richter et al., 2000). Although we expected higher N2O flux in
UF, there was no observable difference between the sites, indicating
that N2O flux had already recovered (Table 2). This agrees with the re-
sults from a boreal forest, where no difference in N2O flux was observed
46 years after a fire (Köster et al., 2017), and between a secondary forest
and a naturalized grassland in southern Chile (Beas et al., 2019).
The biogenic soil GHG balance of our UF site (5079 ± 1772 g CO2-
eq m−2 y−1) is larger than all the values reported for other forests
(Table 3). Although CH4 flux values seem similar to what has been ob-
served in other forests (Table 3), CO2 and N2O fluxes show that our
site emits more of these gases. The larger CO2 and N2O emissions may
be explained by the highly organic nature of Histosols and a lack of min-
eral particles in the UF soil (Albornoz et al., 2013; Perez-Quezada et al.,
2018). The same reasoning applies to explain that the soil GHG balance

7
J.F. Perez-Quezada, P. Urrutia, J. Olivares-Rojas et al.
of the BS (2815 ± 1447 g CO2-eq m−2 y−1) is higher than several other
forest ecosystems (Table 3). As explained above, CH4 flux showed that
our BS acts as a CH4 net sink, which compensates for the rather high
emission fluxes of CO2 and N2O. Considering the NEE reported for the
UF (−873 g CO2 m−2 y−1, Perez-Quezada et al., 2018) and the BS
(−135 g CO2 m−2 y−1, Valdés-Barrera et al., 2019), the ecosystem
GHG balances show that the UF is a net sink (−754 g CO2 m−2 y−1),
whereas the BS is a net source (30 g CO2 m−2 y−1). This implies that
post-fire effects are still occurring and highlights the importance of pro-
tection and post-fire restoration of these ecosystems, which are highly
threatened by natural and human-induced fires (Armesto et al., 2009;
Turetsky et al., 2011; Walker et al., 2019). The significant increase of
soil moisture after disturbance was observed before for temperate
rainforests of Chiloé Island (Pérez et al. (2009), while hydrological
models confirmed that soil waterlogging is a common consequence of
disturbances in these forests due to the combination of poor soil drain-
age and reduced evapotranspiration (Diaz et al., 2007)
4.4. Study limitations and future work
Due to the power requirement of our analyzer we could not sample
more than one site of the unburned and burned conditions. Therefore,
we cannot extrapolate the results of this study due to limited replication,
but we provide data for ecosystems where there is limited information.
Indeed our results show large differences of soil GHG fluxes and balances
between UF and BS, highlighting the complexity of forest disturbances on
GHG emissions. In particular, the effects of fire on soil autotrophic and het-
erotrophic respiration can be very different. North Patagonian rainforests
are not considered to be fire-adapted ecosystems (Kitzberger et al., 2016)
and fires can have long-lasting effects in the landscape (Kitzberger et al.,
2012; Albornoz et al., 2013; Kitzberger et al., 2016). Although we report
autotrophic and heterotrophic elements of soil respiration together and
cannot distinguish them, it is likely that the autotrophic component in
BS is very low, considering that vegetation is mainly formed by shrubs,
ferns, and mosses, which have low belowground biomass. In contrast,
root biomass in the old-growth UF is very dense, thus autotrophic respira-
tion should be high and greater than in the BS. Whether heterotrophic
respiration accounts for almost all soil CO2 flux in BS warrants further
study. We acknowledge that differences in soil GHG fluxes may be associ-
ated with changes in microbial communities, as fires decrease microbial
abundance and composition directly (e.g. temperature) or indirectly
(e.g. quantity and quality of soil C and pH) (Czimczik et al., 2006), but
we did not evaluate this aspect in this study.
Changes in climatic conditions may also impact soil microbial com-
munities; these effects may be different in the BS than in the UF site,
as Aquand soils may be more sensitive to land use changes in terms of
the aerobic biological activation of the soil (Beas et al., 2019). Long-
term records from the Tepual weather station (~70 km) show that pre-
cipitation has decreased about 23% since 1950 (CR2, 2020), which likely
decreased the waterlogging conditions in our BS during this period. Al-
though changes in precipitation may be important in explaining differ-
ences in GHG emissions between sites, we cannot account for this, but
we think that if precipitation was higher (without climate change),
the differences we found between UF and BS would be even larger.
As the burned site was exposed to grazing, we cannot exclude that
this may have also influenced the GHG fluxes measured in this study.
However, as grazing was light, only took place occasionally, and stopped
completely 26 years ago, we consider that its effect may be negligible
compared to the patterns we report for effects of the fire.
Unfortunately, our experimental design for a temperate rainforest
from the Southern Hemisphere does not allow us to disentangle the rel-
ative importance of these effects. However, our results confirm that the
relationship between fire and GHG dynamics is complex and highlights
the need for further studies to improve our understanding of GHG dy-
namics in natural and altered ecosystems. Fire intensity seems to be
8
Science of the Total Environment 755 (2021) 142442
the major factor driving post-fire GHG emissions, therefore studies are
required to inform ecosystem-level post-fire conservation programs.
5. Conclusions
We performed closed-chamber measurements of soil GHG fluxes
during two years at an unburned old-growth temperate rainforest and
a nearby burned site. We found marked seasonal variability for CO2
and CH4 fluxes in both sites; the highest efflux of CO2 and influx of
CH4 occurred during the summer (warmer and drier) season. N2O emis-
sions were very low in both sites, with no apparent seasonal variability.
Environmental controls for GHG fluxes with highest correlations were
soil temperature for CO2, soil water content for CH4, and friction velocity
for N2O.
Working on a Placic Andosol, we observed that after >50 years the fire
still has an effect on the GHG balance. While during the fire large amounts
of CO2 must have been released into the atmosphere from the combustion
of the forest biomass and the organic matter in the soil, we show that after
>50 years the unburned forest soil had a significantly higher emission of
CO2-equivalent compared to the burned site. Considering the net ecosys-
tem exchange of CO2, the unburned forest is a sink, while the burned site
is a source of GHGs. These long-lasting effects make forest fire prevention
a priority in these old-growth temperate rainforests.
CRediT authorship contribution statement
Jorge F. Perez-Quezada: Conceptualization, Methodology, Supervi-
sion, Funding acquisition, Writing - original draft. Paul Urrutia: Investi-
gation. Javiera Olivares-Rojas: Investigation, Writing - original draft.
Ana Meijide: Formal analysis, Writing - review & editing. Enrique P.
Sánchez-Cañete: Formal analysis, Writing - review & editing. Aurora
Gaxiola: Conceptualization, Funding acquisition, Writing - review &
editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
This study was funded by the National Commission for Scientific and
Technological Research (CONICYT, Chile) through the grant FONDEQUIP
AIC-37 and AFB170008 from the Associative Research Program to
Instituto de Ecología y Biodiversidad to JFP-Q and AG, FONDECYT N°
1171239 to JFP-Q and LINCGlobal research program funded by CSIC-
Spain and Catholic University of Chile to AG. Partial funding was pro-
vided by the Vicerrectorado de Investigación y Transferencia from
Universidad de Granada to JFP-Q. The authors also thank the adminis-
tration and personnel at the Senda Darwin Biological Station. We thank
Penelope Serrano-Ortiz and Andrew Kowalski for their helpful com-
ments to improve this manuscript. This is a contribution to the Research
Program of Senda Darwin Biological Station and the Chilean Long-Term
Socio-Ecological Research Network (LTSER-Chile).
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