Global Ecology and Conservation 22 (2020) e01021

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Global Ecology and Conservation

journal homepage: http://www.elsevier.com/locate/gecco

Original Research Article

Post-fire responses of Quercus humboldtii mediated by some

functional traits in the forests of the tropical Andes
Natalia Salazar a, María Constanza Meza a, Josep Maria Espelta b,
Dolors Armenteras a, *
a
n de Ecosistemas ECOLMOD, Departamento de Biología, Universidad Nacional de
Laboratorio de Ecología del Paisaje y Modelacio
Colombia, Bogota
, Colombia
b
CREAF, Cerdanyola del Vall
es, 08193, Catalonia, Spain

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

Article history: The Andean forest is a high diversity ecosystem. These forests are negatively affected by
Received 21 November 2019 anthropogenic pressures that have greatly increased wildfires. Wildfires may increase
Received in revised form 13 March 2020 species susceptibility to other disturbances like insect pests. Little is known of these
Accepted 13 March 2020
ecosystems, their responses to wildfires, or their interactions with other disturbances. This
study seeks to understand what traits mediates the response of Quercus humboldtii to fires
Keywords:
and whether a possible interaction of this disturbance with insect herbivory may occur. We
Fire
analysed changes in biomass, structure and composition and determined the variation in
Herbivory
Survival
oak regrowth after fires. We studied oak survival and its relationship with functional traits
Regrowth (height and bark thickness) and its interaction with fire and herbivory. We found that after
Bark thickness the last fire, there was an impact on the forest in its structure with a mortality of 40% of
adult trees and a reduction in tree species diversity. Structural characteristics, such as tree
height and bark thickness, influenced survival of oaks while fire stimulated resprouting
from the root collar. Although a high herbivory by insects was found, we did not observe
any interaction with fire. This study proves that wildfires in northern Andean forests may
produce a severe amount of tree mortality and decrease tree diversity. Yet, the dominant Q.
humboldtii appears to be a resilient species because its ability to resprout after fire. This
response should be monitored to assess potential effects that an increase in the frequency
of wildfires coupled with other disturbances may have in changing species composition
and structure of Andean forests under new climatic scenarios.
© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

One of the major challenges of tropical ecosystems is to understand how these dynamic systems respond to the un-
precedented levels of disturbances that are currently impacting them. Many tropical landscapes are undergoing rapid

n,
changes in composition and structure due to climate change (Feeley and Silman, 2010; Feeley et al., 2011; Young and Leo
2007) and other anthropogenic disturbances (Valencia et al., 2013). High elevation mountain forests in the tropical Andes

* Corresponding author. Departamento de Biología, Edificio 421, Oficina 223, Facultad de Ciencias, Universidad Nacional de Colombia, Bogota
, D.C. (CP
111321) Colombia.
E-mail addresses: nasalazarl@unal.edu.co (N. Salazar), mmezae@unal.edu.co (M.C. Meza), Josep.Espelta@uab.cat (J.M. Espelta), darmenterasp@unal.edu.
co (D. Armenteras).

https://doi.org/10.1016/j.gecco.2020.e01021
2351-9894/© 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).
2 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021

are ecosystems of great biodiversity and endemicity (Bubb et al., 2004), partly due to the great concentration of fauna and
flora species restricted to South America (Tejedor Garavito et al., 2012). These forests provide important ecological services
such as biodiversity hotspots, habitat protection and water and climate regulation (Bubb et al., 2004; Tobo
n, 2008). Despite
their importance, the Andean forests are also facing great pressures and disturbances of anthropic origin. The tropical Andes
have undergone a long history of transformation associated with human settlements, since the first indigenous occupations
to modern times (Little, 1981; Young, 2007). However, climate change is perhaps one of the most important current threats to
mountain ecosystems (Feeley and Silman, 2010), coupled with mineral exploitation, deforestation, forest fires and frag-
mentation due to the expansion of the agricultural frontier and urban development (Etter and Van Wyngaarden, 2000;
Armenteras-Pascual et al., 2011; Tejedor Garavito et al., 2012).
The capacity for recovery after disturbances of these tropical forest systems will be extremely important under increasing
human pressures. However, knowledge about the resilience of tropical mountain ecosystems is scarce. Mountain tropical
ecosystems can be particularly vulnerable since many of the species in these Andean forests do not exhibit adaptations that
allow them to persist under disturbance regimes. Fire is a disturbance that has shaped the composition of vegetation for
centuries through its effects on structure, productivity and biodiversity (Cochrane, 2009). Ecosystem responses to fire are,
indeed, highly ecosystem-specific (Keith et al., 2009) and dependent on fire characteristics. For example, medium intensity
fires can increase plant species richness by different mechanisms: i.e. increasing habitat heterogeneity, decreasing the
abundance of the dominant species, and allowing the establishment of less competitive ones in denser forest conditions but
that become more competitive in open environments. However, high intensity wildfire decreases plant diversity and allows
the arrival of exotic species (Denslow, 1985; White and Pickett, 1985). Likewise, in areas affected by fire, changes in envi-
ronmental conditions may allow the establishment of other organisms, especially insects (Schowalter, 1985; Hyv€ aRinen et al.,
2009; Hla
sny et al., 2019). It is important to note that the ability of forest systems to recover from these disturbances will also
depend on the species present and their strategies for resisting, based on their functional traits, such as bark thickness
(Pausas, 2017; Casals et al., 2018) or their ability to resprout after fire from a protected bud bank (Espelta et al., 2003).
The genus Quercus expands globally from lowlands to mountain areas (Kappelle, 2006; Terradas, 1999) and several studies,
mainly in temperate zones, have shown the relationship of the presence of this genus Quercus with fire occurrence mediated
by climate factors (e.g. drought, lightning) and anthropogenic ignitions, although the relative importance of them is still a
debate (DeSantis et al., 2010). Indeed many studies indicate that oaks have a positive capacity to respond to fire (Abrams,
1992; Espelta et al., 2003; Leverkus et al., 2014). This response is associated with the ability to resprout from dormant
buds located at the root collar following the death of the main shoot, providing resilience of Quercus forests in frequent fire
regimes (Johnson et al., 2002; Leverkus et al., 2014). Species of this genus, in addition to their hardwood, have thick bark in
maturity, ((Laboratory, 1967; Lorimer 1985 in Abrams, 1992), which makes them more resistant to fire injury and damage.
Moreover, they may deep root systems that may convey some advantages in dry post fire conditions (Alfaro Reyna et al., 2019;
Anderegg et al., 2015). Thus, the regeneration of many oak species has been suggested to be favoured under climate change
predictions of drier conditions and more frequent and severe fires (Vose and Elliott, 2016). Yet, it must be also highlighted that
the Quercus genus present also many species intolerant to fire (Varner et al., 2016) and, therefore more research is needed to
fill the knowledge gap in this regard.
Quercus humboldtii is the only species of oak that exists in Colombia, and biogeographically it is the only representative of
the genus in South America (Kappelle, 2001). This oak tree is distributed from 1100 to 3200 m.a.s.l. (Gonz
alez et al., 2006;
Pulido et al., 2006; Rangel-Ch, 2017) in the three mountain cordilleras of the Colombian Andes, with the western part of the
eastern mountain cordillera having the greatest coverage of the species (Gonza
lez et al., 2006). In the Andean region, de-
mographic density and anthropogenic pressures are high, so the permanence and conservation of oak forests is threatened
(Gonza
lez et al., 2006; Guerrero Rodriguez et al., 2010) as the he expansion of the agricultural frontier using fire to clear land
of natural vegetation is becoming more frequent. Unfortunately, here is no knowledge of the response of Q. humboldtii to fire,
and whether this response is similar to the one reported for other Quercus species located in temperate zones. Given the
importance of understanding the impact and recovery of Andean forests to fire, the main aim of this study was to evaluate the
ecological responses of Andean oak forests to fire, addressing three fundamental questions: i) what is the impact caused by
fire on the forest structure, composition, diversity and loss of biomass; ii) how does oak (Q. humboldtii) respond to fire and
which characteristics favour its survival or persistence; and iii) does an interaction between herbivory and fire exist that
affects forest regeneration and development?

2. Materials and methods

2.1. Study area

The study area corresponds (Fig. 1) to the oak forest located in the Santuario de Fauna y Flora Iguaque (SFFI) in the
Colombian Andes, in the Department of Boyaca
, approximately between 5
670 5800 - 5
670 98 00 north latitude and 73
470 6200
- 73
480 18 00 west longitude and an altitude between 2452 and 3005 m.a.s.l. The study area is located in the ecosystem of
natural forests of the high orobiome of the Andes (IDEAM et al., 2007) and the humid montane forest (Gutie
rrez Rey, 2002).
The area has an annual average temperature between 16.3 and 18.8
C and an annual average rainfall between 810 and
1000 mm, with August and September being the months with the highest humidity deficit (Naturales de Colombia, 2006).
 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021 3

Fig. 1. Location of the sampling plots within the SFF Iguaque, in the Andean region of Colombia. Each yellow point corresponds to a plot.

The SFFI was declared a protected area in 1977. This area is an interesting case study for understanding the responses of
Andean forests to disturbances. Fire events have been recorded in the region since 1927 (Naturales de Colombia, 2006), with
increasing frequency, especially during the dry season and particularly during years of prolonged drought. The largest fire
within the protected area was recorded in 2003 with an area of around 1100 ha that affected most of the paramo vegetation
and some native forests (Naturales de Colombia, 2006). The last recorded fire occurred at the end of August and beginning of
September (dry season) of 2015 and affected approximately 887 ha. This damaged the great majority of oak (Quercus) and
encenillo (Weinmannia) forests, as well as pasture and pasture areas, which were within the protected area (Aguilar and
Isaacs, 2016).

2.2. Sampling sites

Fieldwork was carried out in June 2018. We established twelve plots with an area of 900 m2 (30  30 m each); six controls
were established in unburned areas and six plots in burned areas of oak forests. Given the reduced area affected by fire we had
to locate the plots using a minimum of 50 m to each other, or greater when possible, and they had similar altitude (between X
and Y) and orientation (Table 1). We assumed that forest structure of burned plots before the fire was similar to the control’s
ones. The control areas did not have a history of recent fire disturbances.

2.3. Data collection

In each of the plots, we measured all live or dead mature trees with a diameter at breast height - DBH 10 cm (plots of
30  30 m) (Table 3). Natural regeneration was also measured: saplings (total height, TH > 1.5 m and DBH <10 cm) within the
subplots of 5  5 m, seedlings (TH between 30 cm and 1.5 m, DBH <10 cm) within the subplots of 2  2 m and sprouts
(TH < 30 cm, DBH <10 cm) within the subplots of 1  1 m. Four repetitions of each subplot were made per size category within
the 30  30 m plots. The total height (TH) of the trees was determined where the top of the tree was visible. The basal area
(BA) for each tree calculated from tree diameter and biomass was estimated for all adult trees (all species) using the allometric
equation of Chave et al. (2014). All trees were identified to the species level. Shannon and Evenness indices were calculated for
diversity and richness analyses.
Our analyses of survival, regrowth and herbivory was focused on Quercus humboldtii (oak), with 383 individuals (>10 cm
DBH) in the sample. Quercus species have the ability to sprout from the root, stem or canopy after a disturbance such as fire
(Espelta et al., 2003, Bonfil et al., 2004), and sprouting is influenced by fire severity. Therefore, the mode of sprouting
4 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021

Table 1
Plot localization and spatial variables of the burnt and unburnt plots, SFF Iguaque.

Burnt Unburnt

Site code Elevation (m.a.s.l) Slope X Y Site code Elevation (m.a.s.l) Slope X Y
B1 2602.3 5
73.4762 5.6758 UB1 2870.3 24
73.4646 5.6826
B2 2588.3 55
73.4758 5.6767 UB2 2924.7 4
73.4637 5.6834
B3 2534.9 43
73.4770 5.6773 UB3 2977.1 39
73.4625 5.6840
B4 2512.8 45
73.4784 5.6773 UB4 3005.7 48
73.4637 5.6843
B5 2479.4 32
73.4794 5.6779 UB5 2631.2 47
73.4727 5.6796
B6 2460.9 45
73.4818 5.6798 UB6 2452.1 12
73.4795 5.6790

corresponds to the degree of fire severity, trees that regrow from the canopy, stem and root can persist after fire. Trees that
regrow from the stem are moderately affected; those that regrow only from roots have been very affected by fire result from
high severity fires, and severity is greatest when trees are completely killed by fire (Espelta et al., 2003; Pausas et al., 2017). So,
to determine the ability for regrowth, we classified each tree according to three different types of resprouting: root, stem and
canopy (Annex 1). We recorded the number of sprouts per tree and its longitude. We measured the height of the tree fire scar
(HTFS) for each tree affected by fire. We did this measurement to have an estimate of the effect and intensity of the fire.
A sub-sample of 125 trees of Q. humboldtii was used to evaluate whether bark thickness might influence the capacity and
quantity of regrowth in the oaks. For each tree in the sub-sample a piece of bark was collected, and its thickness was measured
with a digital micrometre. The same sub-sample (125 trees) was used to determine the foliar herbivory. Samples of
approximately 30 leaves per tree were collected, to estimate the percentage of insect herbivory on leaves, and these data were
normalized for the respective analyses.

2.4. Statistical analysis

2.4.1. Forest structure, composition and species richness

A measure of absolute abundance was taken as the number of individuals of each species located within each plot. The
relative abundance was calculated as the percentage of individuals of each species. Shannon and Evenness diversity indices
were calculated for individuals with DBH> 10 cm and for natural regeneration.
To determine significant differences of floral composition between the burned sector and the unburned sector, we per-
formed a non-metric multidimensional scaling analysis (NMDS) using the Bray-Curtis dissimilarity coefficient in order to
visualize and identify patterns based on dissimilarity matrices calculated from response variables (absolute abundance of
species) without the influence of external information (independent variables) (Fig. 2). For this analysis, a 2-dimensional a
priori number was defined (reduced stress value - differences between a reduced space and its original distance). We carried
out an ANOSIM analysis (analysis of similarity of the abundance matrix). We considered all species with a DBH> 10 cm as
“mature trees”. In the case of natural regeneration, only species with an abundance of more than 10 individuals per plot were
used for the analyses.
We did a principal component analysis (PCA) to represent the variability of the data between plots and forest type (Fig. 3).
Response variables used were Shannon Wiener equity index and the evenness equitability index, and structural data of
mature trees (Total Biomass, Average Diameter, Average Total Height). We used the plot as a classification variable, and we
established a partition by type of sector (burned and unburned). For this analysis, we used the software INFOSTAT 2017.
Biomass was estimated using the equation of Chave et al. (2014), an allometric equation (AGB ¼ 0.0673  (rD2H)0.976)
where AGB is aboveground biomass, r is the wood density for each species (when the density of the species is not available,
the density of the genus was used); D is the diameter at breast height and H is the tree total height. We used and ANOVA
(Fisher LSD) to test for differences between burnt and unburnt plots. Biomass was estimated only for mature trees, individuals
with growth habits such as lianas, palms and arboreal ferns were excluded (Fig. 4).

2.4.2. Survival, regrowth and herbivory

We analysed the influence of individual characteristics and fire severity on the survival and resprouting ability of oaks by
means of general (LM) or generalized linear models (GLMER), depending on the error distribution of the dependent variable.
To account for environmental heterogeneity, we also included the factor ‘plot’ as a random variable in all models and ran
mixed-type models. Selection of mixed effects models was made according to the Akaike information criterion (AIC),
selecting the model with the lowest AIC. To determine which factor influences the survival of oaks in the burned areas, the
structural variables, diameter at breast height (DBH) and total height (TH) were included in the model in addition to the
height of the tree fire scar (HTFS) as a proxy for fire severity. These factors were included as fixed effects while we used a
binomial distribution for the response variable.
The regrowth ability of oaks after fire was analysed in three steps. First, we evaluated the influence of TH and HTFS on the
type of regrowth (i.e. from the canopy, stem or root) considering that these three types of resprouting represent a different
and increasing range on the fire severity scale (Espelta et al., 2012). Second, we tested the influence of the individual basal
 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021 5

Fig. 2. NMDS. Graph a) for adult trees with DBH 10 cm. Graph b) for natural regeneration (individuals with DBH  10 cm). B indicates burnt, UB indicates unburnt
plots and the number indicates plot number. Individual numbers are the species (Supplementary information).

area (AB), TH and HTFS on the vigour of resprouting, using as a proxy the number of resprouts produced (Espelta et al., 2003).
Finally, in 10 trees per plot having measured their bark thickness we investigated the influence of this factor on the number of
resprouts produced. For all this analysis we used Poisson distribution for the dependent variable.
Finally, by means of a linear model we examined if herbivory was influenced by the state of the forest (burned vs. un-
burned) and the structural characteristics of trees (DBH). In all models we first included all possible interactions among the
fixed factors and eliminated the non-significant ones. Most of the analyses were done with the software R (Version 1.1.463).
We used Past 3.14 for the diversity indices calculations and Xlstats for a Mann Whitney test. For NMDS and ANOSIM analyses
we used the Vegan 2.3e5 library, and for GLM, LM, GLMER and LME we used the lme4 package.

3. Results

3.1. Forest structure, composition and species richness

We collected 72 specimens of vascular plants within the sampling plots. We could identify to species level a large fraction
of these specimens (94.4%), while 2.77% could be only determined to genus levels and 2.77% could not be determined. The
6 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021

Fig. 3. Principal component analysis, richness and structure multivariate analysis.

Fig. 4. Above ground biomass (AGB in Mg/ha) for burned and unburned areas.

relative abundance (Table 2) was dominated by the species Quercus humboldtii (mature trees) in the unburned and burned
forest.
With relation to alpha diversity values, a greater diversity of species was found in the unburned sector compared to the
burned sector. A Shannon index value for mature trees is 1.37 (E.E. 0,08) in the unburned sector and 0.50 (E.E. 0,08) in the
burned sector. In the case of natural regeneration, a Shannon value of 3.1 (E.E. 0,02) was obtained for the unburned sector and
2.9 (E.E. 0,02) for the burned sector.
 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021 7

Table 2
Relative abundance of the species in both burned and unburned forest.

Forest type Species Relative Abundance

Unburned Mature trees Quercus humboldtii Bonpl. 65.10%
Clusia multiflora Kunth 12.08%
Viburnum cf. triphyllum Benth. 7.70%
others 14 species 15.10%
natural regeneration Myrcianthes rhopaloides (Kunth) McVaugh 15.60%
Viburnum cf. triphyllum Benth. 11%
Cybianthus iteoides (Benth.) G.Agostini 7.80%
another 45 species 65.60%
Burned Mature trees Quercus humboldtii Bonpl. 88.70%
Clusia multiflora Kunth 6.60%
another 15 species 4.70%
natural regeneration Pteridium aquilinum (L.) Kuhn 21.30%
Dodonaea viscosa (L.) Jacq. 10.40%
another 45 species 68.40%

Table 3
Families, species and number of mature trees alive and dead for all plots established both in the burned and in the unburned forest.

Forest Type Families Species Number of trees

DBH>10 cm

Dead Alive
Burnt Adoxaceae Viburnum cf. triphyllum Benth. 1
Betulaceae Alnus acuminata Kunth 5
Clusiaceae Clusia multiflora Kunth 8 6
Fagaceae Quercus humboldtii Bonpl. 47 142
Myricaceae Morella pubescens (Humb. & Bonpl. ex Willd.) Wilbur e 1
Oleaceae Fraxinus chinensis Roxb. e 1
Pinaceae Pinus patula Schiede ex Schltdl. & Cham. e 1
Primulaceae Geissanthus andinus Mez e 1
Total 61 152

Unburnt Adoxaceae Viburnum cf. triphyllum Benth. 7 16

Aquifoliaceae Ilex cf. pernervata Cuatrec. e 3
Araliaceae Oreopanax incisus (Willd. ex Schult.) Decne. & Planch. e 9
Clusiaceae Clusia multiflora Kunth 7 29
Cunoniaceae Weinmannia pubescens Kunth 1 5
Elaeocarpaceae Vallea stipularis L.f. e 4
Escalloniaceae Escallonia paniculata (Ruiz & Pav.) Schult. e 1
Euphorbiaceae Croton cf. smithianus Croizat e 1
Fagaceae Quercus humboldtii Bonpl. 19 175
Lauraceae Ocotea heterochroma Mez & Sodiro e 9
Melastomataceae Miconia cf. squamulosa Triana e 1
Meliaceae Cedrela montana L. e 3
Mora Morus insignis Bureau e 2
Piperaceae Piper bogotense C.DC. e 1
Primulaceae Geissanthus andinus Mez e 2
Sabiaceae Meliosma quercifolia e 2
Verbenaceae Lippia hirsuta L.f. e 1
Total 34 264

There were no significant differences in the composition of species of mature trees (ANOSIM R ¼ 0.034; P ¼ 0.26). Species
of mature trees that occurred in the burned and unburned sectors were Q. humboldtii, Clusia multiflora, Geissanthus andinus
and Viburnum. cf. triphyllum. Significant differences in the composition of species of natural regeneration between burned and
unburned sectors were evident (ANOSIM R ¼ 0.5093; p ¼ 0.005). There were 24 species registered exclusively in the burned
area. The most abundant were Dodonaea viscosa (L.) Jacq., Solanum vestissimum Dunal, Myrsine pellucida (Ruiz & Pav.) Spreng
and Baccharis cf latifolia (Ruiz & Pav.) Pers. In the unburned sector there were 19 species that regenerated naturally and were
not recorded in the burned sector. The most dominant of these species were Cestrum cf. tomentosum L.f., Ilex cf. pernervata
Cuatrec., Picramnia sphaerocarpa Planch. and Abatia parviflora Ruiz & Pav. The two forest types shared 23 species, including
the presence of the invasive fern Pteridium aquilinum.
The first two axes in the analysis of principal components explain 67.7% of the variability in the data (Fig. 3). The first axis
was mainly correlated in a positive way with biomass (0.92) and negatively with an evenness index (0,68). The second axis
8 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021

was correlated with DBH (0.74) and the third axis was mainly positively correlated with taxa in natural regeneration (0.86)
and negatively with the DBH (0.49) and an evenness index (0.49). Biomass was highly correlated with diversity (Shannon)
of mature trees (0.70) and diversity in natural regeneration (0.71). When the number of species with DBH> 10 cm increased,
the equality in the distribution of species decreased (0.72). On the other hand, there was a greater correlation between the
plots in the unburned sector with the diversity of natural regeneration and biomass and height of mature trees.
The average biomass showed significant differences between unburnt and burnt plots (Fig. 4, F 07.204, p < 0.05), The
average biomass (living and dead trees) found in unburned forests was 224,44 Mg/ha (±SE 39) and the total biomass of live
trees was 1244 Mg, where species such as Q. humboldtii and Cedrela montana had the highest average biomass 587 and
264 kg.tree1, respectively. The high biomass value in one of the unburned oak plot is due to the fact that it a less accessible
plot containing a higher density of tree individuals (.i.e. 71 adult trees) with a DBH> 10 cm, is the only plot in which trees (i.e. 2
adult trees) have a DBH> 100 cm and has the higher number of individuals (i.e 39 adult trees) taller than 14 m. Burned forests
had an average biomass of 76.40 Mg/ha (±SE 39,0) and 341 Mg of total living biomass in all 6 plots, which corresponded to
34.05% of living biomass in the unburned forests. In terms of carbon stock, there was 673 Mg C ha1 in the unburned forests
and 229 Mg C ha1 in the burned forest (of live and dead biomass).

3.2. Survival and regrowth

The survival of the oak in the burned forests was high as 75.13% of the trees survived. The model indicated that survival
was negatively influenced by HTFS (GLMER) and positively by TH (GLMER) while DBH had no influence (Table 4).
The ability for sprouting in trees affected by fire (Table 4) was mainly influenced by TH (GLMER) and marginally by HTFS
(GLMER). The height of the tree affected the possibility of regrowth, however the model does not show a very significant
relationship, so we analysed how the number of sprouts of each type might be related to the structural variables already used.
In this sense, we found that TH (GLMER) and AB (GLMER) were significantly related to the number of root sprouts in the trees.
The HTFS (GLMER) showed no relationship. At lower TH and higher AB there was a greater number of root sprouts, while at
higher TH and lower AB there was a greater count of stem regrowth. TH (GLMER) was significantly related to this type of
sprout and AB (GLMER) had a relative significance while HTFS again, was unrelated. Canopy sprouts were not used for this
analysis since there was not enough data. In the analysis of the subsample, where 10 trees were taken per plot, we tested
whether bark thickness at the DBH and at the base of the stem was related to the number of sprouts (Table 4).

3.3. Herbivory

Regarding the foliar herbivory model, we found that TH (LM) was related to the herbivory and the type of forest - FT (LM)
was marginally significant with a greater influence of herbivory in the unburned forests. This means that at higher TH, trees
had a higher percentage of herbivory, while the forest type - FT, whether it was burned or not burned, influenced herbivory,
but it did not determine it (Table 5) (see Table 6).

4. Discussion

4.1. Forest structure, composition and species richness

Fire had significant effects on the forest structure, and it decreases species richness and diversity, as several of the tree
species co-existing with Q. humboldtii do not tolerate fire and disappear in the burned areas. The greater number of in-
dividuals in the regeneration compartment and the lower number of mature trees in the burned areas occurs because fire
affects mature trees that die over time and as this mortality increases, it opens gaps that allow new micro-climatic and light
conditions. This allows the establishment and development of medium-size species that probably arrive by seed dispersion or
recover after sprouting from stems that were top killed by fire. Similar effects of greater recruitment from natural regener-
ation and high mortality of mature trees, changing the structure and composition of forests, have been reported in studies on
the dynamics of burned forests in the Andean Cordillera (Oliveras, 2014) and lowland parts of South America, such as the
Amazon (Barlow and Peres, 2008). Fire may also increase the presence of invasive species adapted to the new post-fire

Table 4
Quantity of trees with or without regrowth and type of resprouting.

Nº trees with regrowth Type of resprouting

Root Stem Canopy Root þ Stem Root þ Canopy Stem þ Canopy Root þ Stem þ Canopy

82 34 1 16 1 3 3
Nº trees without regrowth 2

Root ¼ When the tree had only root regrowth, Stem ¼ When the tree had only stem regrowth, Canopy ¼ When the tree had only canopy regrowth,
Root þ stem ¼ When the tree had root and stem regrowth, Root þ canopy ¼ When the tree had root and canopy regrowth, Stem þ canopy ¼ When the tree
had stem and canopy regrowth and Root þ Stem þ canopy ¼ When the tree had root, stem and canopy regrowth.
 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021 9

Table 5
Results of the different mixed generalized linear models and lineal model.

Model Variables Estimate s.e. z t p Signf. Codes

Survival TH 0.3427 0.0835 4.106 4.02E-05 ***
HTFS 0.3849 0.1054 3.651 0.000261 ***
DBH 0.0213 0.0151 1.412 0.158007
Resprouts TH 0.0609 0.0262 2.324 0.0201 *
HTFS 0.0825 0.0430 1.92 0.0548 .
Root resprouts TH 0.1013 0.0225 4.505 6.64E-06 ***
HTFS 0.0349 0.0236 1.475 0.14
BA 9.8565 1.1730 8.403 <2e-16 ***
Stem resprouts TH 0.0928 0.0185 5.022 5.12E-07 ***
HTFS 0.0647 0.1064 0.608 0.5431
BA 1.2542 0.5972 2.1 0.0357 *
Bark thickness and resprouts Base Bark 0.0687 0.0273 2.518 0.0118 *
DBH Bark 0.0744 0.0290 2.563 0.0104 *
Herbivory TH 0.0411 0.0037 4.054 9.54E-05 ***
FT 0.0152 0.0223 1.843 0.0681 .

TH: Total high, DBH: diameter at breast high, HTFS: height of the tree fire scar, FT: Forest type, BA: Basal area.

conditions of the area, becoming a problem for regeneration and further increasing flammability (Pausas and Keeley, 2017) as
is the case for the increasing presence of the fern Pteridium aquilinum in our burned sites. In addition, vine species such as
Muehlenbeckia tamnifolia (Kunth) Meisn. can climb the surviving trees in burned areas, suffocating them, and leading to
possible death. The decrease in the number of mature trees in the burned areas resulted in the loss of almost 66% of the carbon
stock an intermediate impact in comparison to studies in Andean forests in Peru that reported 20.67% loss (Miyamoto et al.,
2018), or in Colombia with 87.7% of carbon stock loss (Yepes et al., 2010). The lower values reported in our study in comparison
to other Colombian sites may be due that in other studies the loss of biomass occurred by the synergy of several disturbances
such as selective logging and fires.

4.2. Survival and regrowth

Based on our results, tree height and bark thickness were the two main functional attributes influencing survival success.
Increasing survival with increasing height may be due to the distance of the canopy from the ground and from the heat of the
fire (Ordo
n
~ ez et al., 2005). This paramount importance of tree height was also indicated by the fact that the lower the height
of the flame scar (a proxy of fire intensity), the greater the survival rate. In addition, as reported by previous studies, a thicker
bark offered greater protection to the cambium from the heat of the fire increasing tree survival (Lorimer, 1985 in Abrams,
1992; Pausas, 1997; Pausas, 2017). In our study, bark thickness was also associated with increasing resprouting from the
buds in the stems, probably as they benefited from higher protection (Espelta et al., 2003). The size of the tree and the basal
area were also characteristics associated with a positive response in oaks sprouting. Trees with higher basal areas respond
with more sprouting and increased heights from all types of sprouts, i.e., root, stem, canopy. Results like ours have been
reported in other studies (Quevedo et al., 2007). In areas were fires effect a greater proportion of the trees to a more severe
degree including stem injury and canopy scorch, sprouts are most abundant from the root, or base of the tree burned (Espelta
et al., 2012). In addition, as we observed the greater the intensity of the disturbance (flame height), the lower the tree height
at which the new resprouts emerged (Pausas et al., 2017).

4.3. Herbivory

In areas affected by fire, with new microclimatic conditions after burning, the arrival and establishment of herbivorous
insects increases (Schowalter, 1985). In general, the most numerous records are of wood-eating beetles that exploit wood in
decomposition (Hyva €Rinen et al., 2009; Hla

sny et al., 2019). However, there are other types of insects that are generalists,
suckers or chewers that also benefit from the new habitat created in burned over forests (Kerstyn and Stiling, 1999; Arellano
and Castillo-Guevara, 2014). Chewing insects were most abundant in our study as revealed by our leaf analysis of herbivory.
These findings were observed for the entire study area in both burned and unburned areas. However, there was a significant
but marginally greater presence of herbivory in the unburned forest. We also observed that taller trees have a higher per-
centage of herbivory. Taller trees can provide greater nutrients and better foliar qualities for insects, thus allowing dense
insect populations (Scriber and Slansky, 1981; Thompson and Pellmyr, 1991; Hunter and Price, 1992 in White, 2013). In
addition, taller trees may be more apparent to insect herbivores (apparency effect in (Castagneyrol et al., 2013) and thus suffer
from higher herbivory damage (Ruiz-Carbayo et al., 2017) Other factors such as, fragmentation and edge effects might affect

squez et al., 2007; Alvarez, 2009 in Lo
the increase of pests (e.g. Va
pez-Galv

an, 2014), although our study did not include an
analysis of these factors. The evidence in the field indicates that the area suffered processes of intervention that might have
led to current levels of fragmentation.
10 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021

Table 6
Delta method R - square marginal (R2m) and conditional (R2c) for the mixed generalized linear models and r-squared and
adjusted r-squared for the linear model (Herbivory).

Model d
R2 m R2 c
Survival 0.1961455 0.2977782
Resprouts 0.07253826 0.1140935
Root resprouts 0.2007025 0.6917764
Stem resprouts 0.3302229 0.7504504
Bark thickness and resprouts 0.158967 0.158967
Herbivory R-squared Adjusted R-squared
0.25 0.2361

5. Conclusions

Our study provides evidence of biomass loss in the large trees, decreased tree diversity and modification of the structure
and composition of a montane Andean forest due to fire. Previously, only deforestation had been reported as a cause of loss of
diversity in this type of ecosystem (Guerrero Rodriguez et al., 2010). Our results illustrate how the oak responded to fire in the
short term, but we suggest continuing monitoring to follow up the effects in the long-term since we don’t know yet about the
survival of the oak sprouts, as it may not be straight forward for them to survive to once again form large trees. There is a need
to state clearly if the oak in these systems is more sustainable in unburned areas than burned. Further research is needed also
to understand diversity in natural regeneration after a fire. Some questions to be answered would be if the species that are
colonizing these affected areas are less susceptible to fire, if they are invasive, or if they are species that were already part of
the composition of the forest. We also suggest a study on soil characteristics to determine if there is loss of nutrients and if this
affects the forest diversity.
Our study revealed that oak survival depended on some of its functional traits, such as the total height and bark thickness
that increased its ability to regrow after fire. This shows that, although Q. humboldtii is a tropical species, the species shows
resistance to fire in a similar way to species of the same genus from Mediterranean-type areas subjected to intense fire re-
gimes (see Espelta et al., 2012). Therefore, our results may be considered a first step towards clarifying fire resistance the
studied species given the presence of some fire resistance traits although this nature is not so clear as it is for many temperate
species of oaks (Varner et al., 2016) particularly given the fact of the lack of information of the oak’s fire niche for Q. humboldtii.
Moreover, to have a more complete view of fire tolerance it would be necessary to assess the response of Q. humboldtii, to fire
regimes varying in their recurrence and intensity, as this may result in large differences in the response of oaks (Bonfil et al.,
2004) Up to now, we know that the oak has a recovery response three years after the fire but we do not know whether there
may be a decay of trees if other disturbances such as pests or prolonged droughts occur (Espelta et al., 2012). It would also be
very interesting to establish a risk model of oak mortality in certain climatic conditions, in order to determine its survival,
since the drought conditions due to climate change could affect not just the intensity of the fire and a greater mortality of Q.
humboldtii but also the survival ability of resprouts in the mid-term (Cotillas et al., 2009) and their ability to reproduce
(Sanchez-Humanes and Espelta, 2011) Finally, the study of the root system of the species would also help elucidate the
resistance to water stress under dry post fire conditions (Alfaro Reyna et al., 2019).
Although the response of this oak species after fire was relevant, we also found high mortality of trees of different species,
some dead standing or fallen, and we observed the presence of detrital material that over time could increase. We highly
recommend monitoring and making some tests of the feasibility of the removal of this combustible material to avoid future
fires of greater intensity but also to understand forest recovery. In addition, this material can become a means for the
propagation of pests that affect the surviving trees. Despite not finding a strong relationship between disturbances with our
sample (fire þ herbivory), but it is important to follow up and monitor pests, and whether these are associated with detrital
material or not. Such relationships could then be addressed with alternatives of biological control through research projects
that could provide the answers. Another management option that could be considered is the study of the ecology and the
need or not for control of invasive species such as the fern (Pteridium aquilinum), a species that was common in a large
proportion in burned areas, but which was also reported in unburned forests. Understanding the ecology of this species and
the possibilities of eradication could be a tool for the understanding and enhancement of forest recovery that would help
management of the area. Finally the presence of a pine, a non native species, is explained by the natural propagation of
planted pines in the past. Pines are still present in the buffer areas of the park, so recommendation of environmental edu-
cation regarding suggestion to use native species outside the area remains a key management action for the area.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
 N. Salazar et al. / Global Ecology and Conservation 22 (2020) e01021 11

Acknowledgments

To the National University of Colombia for the academic support. To Parques Nacionales Naturales de Colombia, officials of
the Santuario de Fauna y Flora Iguaque (SFFI), especially the Head of the SFFI William Zorro and the professional María
Mercedes Nun ~ ez for their accompaniment and management. To the Asociacio
n de Acueductos Veredales de la Quebrada
Chaina- Asochaina and its coordinator Amparo Rojas, for allowing and carrying out the accompaniment in the field work in
the protected area. Finally, we would like to thank Omar Chaparro for his field support and Thomas R. Defler for the English
edition of this manuscript.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.gecco.2020.e01021.

Funding

Funding was provided by USAID e Partnerships for Enhanced Engagement in Research (PEER) and The National Academies
of Science, project Degradation of Tropical Forests in Colombia: Impacts of fire (NAS Subaward Letter No, 2000007526).

Contributions

NS and MCM contributed to methodology, data collection and data analysis. D.A. designed the project, contributed to the
conceptualization, methodology, and analyses. JME contributed to the statistical analysis. NS and DA wrote the manuscript. All
authors read and approved the final manuscript.

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