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Effects of fragmentation on functional diversity associated with aboveground

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Article in Landscape Ecology · November 2018

DOI: 10.1007/s10980-018-0719-8

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Landscape Ecol
https://doi.org/10.1007/s10980-018-0719-8 (0123456789().,-volV)
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RESEARCH ARTICLE
Effects of fragmentation on functional diversity associated
with aboveground biomass in a high Andean forest
in Colombia
Slendy Rodrı́guez-Alarcón . Nelly Rodrı́guez-Eraso
René López-Camacho
Received: 1 March 2018 / Accepted: 30 September 2018
Ó Springer Nature B.V. 2018
Abstract
Context Forest fragmentation alters the composi-
tion, structure and function of ecosystems and affects
ecological processes that are fundamental for the
provision of ecosystem services where functional
diversity is sensitive to its effects. Analyzing the
functional responses of the plant community to
fragmentation can provide new approaches to its
conservation and management.
Objectives We analyzed whether the functional
diversity of woody individuals associated with above-
ground biomass (AGB) in a high Andean forest in
Colombia is affected by fragmentation.
Methods Based on three fragmentation categories
identified using landscape metrics, we selected ten
forest fragments. Multitrait and monotrait functional
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10980-018-0719-8) con-
tains supplementary material, which is available to authorized
users.
S. Rodrı́guez-Alarcón  I. Pineda-Rincón 
R. López-Camacho
Facultad de Medio Ambiente y Recursos Naturales,
Universidad Distrital Francisco José de Caldas,
Bogotá D.C., Colombia
N. Rodrı́guez-Eraso (&)
Departamento de Biologı́a, Facultad de Ciencias,
Universidad Nacional de Colombia, Bogotá D.C.,
Colombia
e-mail: nrodrigueze@unal.edu.co
. Ivanov Pineda-Rincón .
diversity indexes (foliar and wood) weighted by
aboveground biomass were calculated in plots of
0.1 ha in each fragment. Analysis of variance was
performed, and simple linear regressions were quan-
tified to identify the relationships between functional
diversity and fragmentation.
Results The category of large fragments had a higher
average AGB than did the medium and small
fragments. Fragmentation had effects on the variance
of some foliar and stem traits but not on functional
dominance. For the multitraits indexes, the edge
contrast was negatively related with functional
dispersion.
Conclusions The categories analyzed have similar
responses in terms of functionality associated with
AGB. We highlight the importance of small fragments
in the maintenance of plant functional diversity and as
reservoirs of AGB. We underline that small fragments
are important to consider in the development of
conservation and connectivity strategies.
Keywords Community-weighted variance  Edge
contrast  Functional traits  Path area  Tropical forest 
Wood density
Introduction
Changes in land use and fragmentation represent a
threat to biodiversity worldwide and cause the
123

alteration of important ecological processes such as
primary productivity, nutrient cycling, microclimatic
flows, and other changes (Hitimana et al. 2004;
Fischer and Lindenmayer 2007) such as alterations
of forest biomass distribution patterns and carbon
stocks (Ziter et al. 2013). The fragmentation of
tropical forests in particular alters their capacity to
store carbon, increasing carbon emissions in the world,
with total carbon losses estimated to be 0.34 GtC per
year (Brinck et al. 2017). Moreover, the heterogeneous
landscapes that result from fragmentation can be
considered important ecological filters that explain
changes in the composition and functional diversity
(FD) of plants (Duflot et al. 2014). Fragmentation
generates abrupt changes in the size, shape and
configuration of the resulting patches (Saunders
et al. 1991; Fahrig 2003) and not only modifies the
diversity and composition of species (Bender et al.
1998; Fahrig 2003; Echeverria et al. 2007; Arroyo-
Rodrı́guez et al. 2013; Duque et al. 2013; Haddad et al.
2015) but also affects the diversity of some functional
traits in plant communities that are important in
providing services (Quétier et al. 2007; Girão et al.
2007; Mayfield et al. 2010; Lavorel et al. 2011;
Houghton et al. 2012). For example, environmental
stressors are stronger in small, isolated, irregular
fragments with high edge contrasts, reducing commu-
nity leaf variability by filtering species with stress-
tolerant leaf traits (Munguı́a-Rosas et al. 2014;
Arellano-Rivas et al. 2016), and increasing the mor-
tality of large trees inside the fragments. This gives
way to the growth of species with lower wood density
and high light demand, which reduces aboveground
biomass (AGB) and stored carbon (Laurance et al.
1997; Dantas de Paula et al. 2011; Berenguer et al.
2014; Chaplin-Kramer et al. 2015).
One way to examine the effects of forest fragmen-
tation on ecosystem functions of species and their
implications for the provision of ecosystem services is
to assess functional diversity (Kooyman et al. 2013;
Magnago et al. 2014; De Frutos et al. 2015), because
FD is considered a modifier and regulator of ecosys-
tem processes and services (Dı́az et al. 2006; Lavorel
et al. 2011; Lavorel 2013). Research exploring the FD
of plants along fragmentation gradients is recent and
has focused on reproductive traits, dispersion, regen-
eration and growth form (Girão et al. 2007; Kooyman
et al. 2013; Sonnier et al. 2014; Munguı́a-Rosas et al.
2014; De Frutos et al. 2015; Carneiro et al. 2016;
123
Landscape Ecol
Mendes et al. 2016) and rarely links FD with AGB
(Ziter et al. 2013; Magnago et al. 2014). AGB, as a
property of ecosystems related to the ecosystem
services of carbon fixation and storage and thus
having implications for global environmental change,
has been considered to be influenced by the dominance
of some functional traits (Conti and Dı́az 2013).
Research has shown that community-weighted means
(CWMs) of specific leaf area (SLA), maximum height
(Hmax), wood density (WD) and leaf dry-matter
content (LDMC) are all important predictors of an
increase in aboveground biomass, since these traits
contribute to carbon storage, and CWMs can explain
the productivity of AGB because they are parallel to
the relationships between the trait values and the
performance of the plants. For example, a high CWM
of SLA indicates the dominance of species with rapid
growth and high productivity, while a high CWM of
LDMC or WD indicates the dominance of conserva-
tive species associated with low productivity (Finegan
et al. 2015). In terms of multivariate functional
diversity (multitrait), which is related to the variation
in functional traits that influence ecosystem processes,
it has been found that AGB is positively associated
with functional dispersion (Ziter et al. 2013; López
2015).
Previous studies showed that fragmentation has
different impacts on plant functional composition and
diversity, affecting carbon storage in the ecosystem.
For example, fragmentation does not have a significant
impact on the functional richness associated with
AGB nor on the tree community structure or FD, but it
does impact functional divergence and functional
evenness in small fragments of Brazilian forest, which
reduces functional redundancy and improves biomass
reserves due to reduced competition (Magnago et al.
2014, 2015, 2016). A positive relationship between
functional dispersion and carbon in AGB due to the
presence of abundant species that are functionally
different has been found in unmanaged forests of
Canada (Ziter et al. 2013). Fragmentation reduces FD,
although small fragments with few functionally sim-
ilar tree species have high AGB in South Africa (Rolo
et al. 2018). Aldana et al. (2017) found that AGB
stocks are adversely affected by fragmentation and
loss of species richness in lowland forests of Colom-
bia. Despite this research, there is still a knowledge
gap regarding the relationship of fragmentation with
functional diversity associated with aboveground
Landscape Ecol
biomass stocks (Ziter et al. 2013; Magnago et al. 2014;
Aldana and Stevenson 2016; Rolo et al. 2018)
particularly in Andean forests, where there has been
little research.
In Colombia, the Andean and high Andean forests
of the Eastern Cordillera are part of a global
biodiversity hotspot (Orme et al. 2005), and they are
considered conservation priority ecosystems because
they have undergone extensive transformation pro-
cesses and fragmentation due to intense agricultural,
livestock and urbanization activities. The loss of these
forests is most pronounced around the metropolitan
area of Bogotá, Colombia’s capital, given the accel-
erated urban growth in recent years (Rubiano et al.
2017). These forests are important systems for under-
standing the responses of FD relating to AGB in the
face of fragmentation, as well as for helping us to
understand the functional role of the small remnants
that still persist. Research related to FD in Colombia
has focused on evaluating some foliar and reproduc-
tive traits at the edges of fragments with different types
of vegetation (Montenegro and Vargas 2008) and the
relationships between FD indexes and AGB in
successional forests (López 2015). In contrast, frag-
mentation studies have focused on the calculation of
landscape metrics and their effect on species compo-
sition and diversity (Duque et al. 2013).
The study of AGB in fragmented landscapes from
the perspective of FD broadens the analysis to clarify
the ecosystem function and their response to changes
such as fragmentation and to help in establishing
environmental policies and management based on
mutually beneficial outcomes in these landscapes,
where the forest remnants play key ecological and
functional roles in carbon storage and biodiversity. In
this study, our objective was to investigate how
fragmentation, evaluated through landscape metrics,
is related to tree functional diversity associated with
AGB in a high Andean forest in Colombia. Our
hypothesis is based on the fact that small, irregular and
isolated fragments that are surrounded by land vege-
tation cover with a greater edge contrast could have
low FD since the loss of functions is greater over time
in smaller and more isolated fragments, which tend to
maintain smaller AGB reserves (Haddad et al. 2015;
Magnago et al. 2015, 2016).
Materials and methods
Study area
The study area is located in the municipalities of
Guasca and La Calera (Department of Cundinamarca,
tropical Andean region, 4°560 4.3800 N, 74°20 32.9900 W;
4°340 48.8300 N, 73°430 36.0100 W), with a total extent of
692.3 km2. The study was carried out in high Andean
forest with altitude between 2800 and 3200 m (Cua-
trecasas 1958; Rangel-Ch 2000) (Fig. 1, Fig. S1). The
annual precipitation of the zone varies between 800
and 1500 mm, with an annual average temperature
between 7 and 13 °C and a humidity regime varying
from semihumid to very humid (Sguerra et al. 2011).
The predominant soils in the region are inceptisols
(association Humic Dystrudepts and Andic Dys-
trudepts) with the presence of some Typic Hapludands
andisols with fine to medium-thick textures and strong
acidity and formed from parent material of sandy and
silty clay sedimentary rocks (IGAC 2000, 2014).
The landscape is dominated (43.3%) by an anthro-
pic matrix with a predominating mosaic of pastures
and a mixture of crops and pastures. The agricultural
areas are scattered through out the pastures and are
located near the flatter areas, with potato as the main
crop. Forest ecosystems represent only 11.7% of the
study area, and they are embedded in the anthropic
matrix. Most forests occupy areas with steep slopes
and are difficult to access (Rodrı́guez-Alarcón 2018).
Some forest fragments have been consolidated as Civil
Society Nature Reserves (CSNRs), and most are part
of the buffer zone of the Chingaza National Natural
Park (NNP) and the Blanco River Protective Forest
Reserve (PFR) in Cundinamarca, which are important
for the conservation of the capital city’s and sur-
rounding lands’ water supply (Sguerra et al. 2011).
Landscape metrics and fragmentation categories
We used a land cover map for 2015 with a scale of
1:25000 (Rodriguez-Alarcón 2018) to calculate a
series of landscape metrics that have been commonly
used as surrogates for landscape fragmentation
(Schindler et al. 2013; Rolo et al. 2018). For each of
the 260 forest fragments that were identified, four
metrics at the patch level were calculated using the
FRAGSTATS 4.2Ò program (McGarigal et al. 2012):
patch area (PA) and patch shape (SHAPE), which can
123

Fig. 1 Study area and fragmentation categories. The dots listed correspond to the sampling units (plots of 0.1 ha). Fig. S1 shows the
color image
influence the community size and species persistence
and are measures of the degree of fragmentation; edge
contrast (ECON), a measure of contrast between a
patch and its immediate neighborhood; and euclidean
distance to the nearest neighbor (ENN), a measure of
proximity between forest patches (McGarigal and
Cushman 2002; Fahrig 2003; Haddad et al. 2015).Th-
ese metrics are widely used in general fragmentation
studies (Schindler et al. 2013) and studies aiming to
characterize relationships between aspects of land-
scape configuration and plant biomass in fragmented
forests (Hernandez-Stefanoni et al. 2011; Magnago
et al. 2016; Melito et al. 2018). Pearson correlation
coefficients between each pair of metrics were com-
puted, and we did not find any significant relation-
ships, except for patch area and shape (p \ 0.01).
Through a principal component analysis (PCA) and
cluster analysis based on the first principal component
of the PCA (Ward classification method), three
categories of fragmentation were established, that
were the basis for field work. The analyses were
performed with the ‘‘FactoClass’’ package in R,
123
Landscape Ecol
version 3.3.3 (Pardo and Del Campo 2007; R Core
Team 2017). Table S1 shows the characteristics of
each category in relation to the calculated metrics for
whole landscape forest patches, where the fragments
of category III are the largest.
Aboveground biomass and functional traits
Ten plots of 0.1 ha (100 m 9 10 m) were established
at random, taking into account ease of access: four
plots of fragments in category I, three in category II
and three in category III. Two plots of the last category
were located in the same fragment, because that
fragment presented accessible facilities and is part of
the forest reserve areas. The plots were located
towards the center of the fragment to avoid edge
effects (Girão et al. 2007; Mendes et al. 2016), taking
into account a distance of not less than 100 meters
from the edge of the fragment, and their locations were
corroborated inside the patch and outside the edge
using Riitters et al. (2000) methodology in SAGA
software (Conrad et al. 2015) (Fig. 1). Given the large
Landscape Ecol
number of fragments grouped into category I, through
a cluster analysis, the category was subdivided by area
into four groups (1.15–20.6; 20.9–36.3; 36.8–67.9;
and 71.2–150 ha) to randomly select a representative
fragment to sample by subgroup. The descriptive
statistics of the landscape metrics for sampled frag-
ments are shown in Table 1.
In each plot, all live woody plants with a diameter at
breast height (DBH) C 5 cm were counted, and the
DBH and height of each individual were recorded.
Botanical material was identified using herbarium and
literature sources, and it was processed following
established standards for the management of biolog-
ical collections. The material in a reproductive state
was deposited in the collection of the Forest Herbar-
ium (UDBC) of Francisco José de Caldas Distrital
University. For each plot, AGB was used as the
weighting parameter for the calculation of the func-
tional diversity indexes. Estimation of biomass was
performed using the allometric equation of Pearson
et al. (2005) (Eq. 1), where AGB is the aboveground
biomass per woody individual (kg), and DBH is the
diameter at breast height (cm). We chose this equation
because it does not include wood density or height,
which are functional traits included in the FD indexes
in which AGB was used as a weighting parameter.
AGB per plot was obtained as the sum of the
biomasses of the individuals registered in the plot,
and the value obtained was expressed in megagrams
per hectare (Mg ha-1):
AGBðKgÞ ¼ expð 2:289 þ 2:649  InðDBH Þ
 0:021  InðDBH 2 ÞÞ
For the measurement of functional traits, quantita-
tive traits were selected from the TRY (TRY Initiative
on Plant Traits) database (Kattge et al. 2011) as well as
the traits proposed by Cornelissen et al. (2003) and
Table 1 Number (n), mean, standard deviation (in parentheses) and range of each landscape metric for the sampled fragments, by
category
Landscape metrics Category I (n = 4)
Mean (SD) Range
PA (ha) 46.46 (27.9) 19.6–73.6
SHAPE 2.97 (0.92) 2–4.06
ENN (m) 111.8 (140.9) 25–322.06
ECON (%) 81.3 (8.5) 70.9–91.6
Pérez-Harguindeguy et al. (2013), since they are
relevant for AGB: maximum height of the plant
(Hmax) (m), density of the wood (WD) (gr cm-3),
specific leaf area (SLA) (cm2 g-1) and leaf dry-matter
content (LDMC) (g). The leaf and wood density
functional traits were obtained from direct measure-
ments in the field of five (5) mature woody individuals
of each of the species found (in general, for the three
fragmentation categories) and following the protocols
established by Pérez-Harguindeguy et al. (2013) and
Salgado-Negret et al. (2015).
For cases where the density of wood could not be
measured due to the low abundance of individuals or
thin diameters, the information was obtained from the
traits reported by López (2015) and Garnica and
Saldarriaga (2015) and, for morphospecies identified
to the genus level (2 morphotypes), from database The
Global Wood Density (GWD) in the subsection
Tropical South America (Chave et al. 2009), using
the average wood density for the taxonomic
group.Maximum height was obtained from measure-
ments taken in the field, according to the procedure
established by Pérez-Harguindeguy et al. (2013) and
Salgado-Negret et al. (2015). In the case of rare
species, maximum height was obtained by reviewing
herbarium specimens collected in the same study area
and taking into account that these were greater height
values than those recorded in the field.
Data analysis
Multitrait indexes were calculated because they allow
ð1Þ
the functionality of the community to be characterized
(Casanoves et al. 2011); these indexes were: func-
tional richness (FRic), functional evenness (FEve),
functional divergence (FDiv) and functional disper-
sion (FDis). In the multifunctional space, FRic
Category II (n = 3) Category III (n = 3)
Mean (SD) Range Mean (SD) Range
219.6 (40.8) 177.4–258.9 1664.4 (521.6) 1363.2–2266.7
6.24 (1.71) 4.41–7.8 11.7 (0.73) 11.3–12.5
20.8 (5.18) 15–25 19.3 (1.14) 18–20
74.9 (15.5) 58.3–89.1 82.3 (1) 81.7–83.5
123

represents the volume occupied by the community;
FEve measures the uniformity of the species distribu-
tion; FDiv quantifies the difference in the distances
between species; and FDis refers to the average
distance of each species to the centroid of the
community (Laliberté and Legendre 2010; Casanoves
et al. 2011). Additionally, we calculated two monotrait
indexes: community-weighted mean (CWM), an
indicator of the functional dominance of the commu-
nity (Roscher et al. 2012), and community-weighted
variance (CWV), which quantifies the variation in the
values of each trait in the community (Sonnier et al.
2010). For the calculation of these indexes, the AGB
of each species was used as a weighting parameter to
evaluate the functional diversity-aboveground bio-
mass association. The trait values were standardized,
and the functional diversity indexes were calculated
with ‘‘FD’’ in R (Laliberté et al. 2014).
The normality of the data was assessed and
confirmed (Shapiro–Wilk test, p [ 0.05), as was the
homogeneity of variances (Levene’s test, p [ 0.05).
The differences in the components of FD and AGB
between the fragmentation categories were evaluated
by analysis of variance (ANOVA) using ‘‘car’’ (Fox
and Weisberg 2011), with post hoc Bonferroni
correction carried out using ‘‘multcomp’’ (Hothorn
et al. 2016). Additionally, the differences in the FD
components between the fragmentation categories
were evaluated with multivariate analysis of variance
(MANOVA) and with the Hotelling comparison test
using ‘‘Hotelling’’ (Curran 2017). For AGB, PA and
CWV.Hmax, a logarithmic transformation (ln) was
implemented, and the ENN variable was transformed
with the function 1/x. Pearson correlation analysis and
simple linear regression analysis (Kooyman et al.
2013; Mendes et al. 2016) between functional diver-
sity (dependent variable) and landscape metrics
(independent variable) were performed. Assumptions
for error distributions were verified using the Shapiro–
Wilk test for normality, the Breusch-Pagan test for
homoscedasticity, and the Durbin–Watson test for
independence. All analyses were performed in R 3.3.3
with a level of significance of a = 0.05.
Results
Considering all of the fragments, we sampled a total of
1390 trees belonging to 90 species and 30 families. A
123
Landscape Ecol
total of 49 species were present in category I, 52
species in category II, and 35 species in category III
fragments, with 15 species shared among the three
categories. The AGB of the sampled fragments varied
between 149.1 and 637.6 Mg ha-1. Category III
showed the greatest stock of biomass, with an average
of 516.2 ± 200.8 Mg ha-1. Category I presented an
average of 187.8 ± 46.4 Mg ha-1, and category II, of
209.7 ± 34.7 Mg ha-1. Category I and II showed no
significant differences in AGB, while category III was
significantly different (ANOVA: F = 9.43, p \ 0.05;
Fig. 2). The species with the highest contribution to
biomass that are present in all categories of fragmen-
tation are Weinmannia balbisiana, Miconia cundina-
marcensis, Hedyosmum parvifolium, Drimys
granadensis and Brunellia propinqua.Species such
as Weinmannia tomentosa and Weinmannia rollottii
are important in the composition of these forests and
make considerable contributions to some of the
fragmentation categories (Fig. 3).
Although functional diversity indexes differed
among the sampled fragments (Table S2), no signif-
icant differences were found for the FD components
among the fragmentation categories (ANOVA and
MANOVA, p [ 0.05). However, it was observed that
the fragments of category III tended to show the
highest averages CWM values of specific leaf area and
maximum height (Table 2). Inverse relationships were
found between the functional diversity indexes and the
landscape metrics: edge contrast and functional
dispersion (R2 = 0.42, p = 0.026), edge contrast and
community-weighted variance of leaf dry-matter
Fig. 2 Variation in aboveground biomass (logAGB, Mg ha-1)
between and within the three fragmentation categories. The
error bars represent ± standard error. ANOVA: F = 9.43,
p \ 0.05. The letters above the bars represent the differences
among categories determined with a post hoc Bonferroni test.
Stocks with a letter in common are not significantly different
(p [ 0.05)
Landscape Ecol

Fig. 3 Contributions of
species with higher
aboveground biomasses (log
AGB, Mg ha-1) to each
category of fragmentation
(I–III)

Table 2 Mean and standard deviation (in parentheses) of the functional diversity of the tree communities in the three categories of
fragmentation in the high Andean forest, Colombia
Functional diversity Fragmentation category
I II III

FRic 6.85 (6.67) 9.49 (0.16) 4.31 (2.9)

FEve 0.45 (0.16) 0.53 (0.11) 0.46 (0.27)
FDiv 0.80 (0.07) 0.87 (0.03) 0.72 (0.12)
FDis 1.43 (0.14) 1.37 (0.4) 1.16 (0.16)
CWM.SLA 84.40 (15.5) 90.27 (24.3) 98.78 (12.6)
CWM.LDMC 0.31 (0.04) 0.33 (0.03) 0.33 (0.02)
CWM.WD 0.50 (0.05) 0.50 (0.03) 0.50 (0.02)
CWM.Hmax 20.88 (0.95) 21.05 (1.08) 21.15 (1.39)
FRic functional richness, FEve functional evenness, FDiv functional divergence, FDis functional dispersion, CWM community-
weighted mean, SLA specific leaf area (cm2 g-1), LDMC leaf dry-matter content (g g-1), WD wood density (g cm-3), Hmax
maximum height (m)

content (CWV.LDMC) (R2 = 0.43, p = 0.023), and
between community-weighted variance of wood den-
sity (CWV.WD) and patch area (R2 = 0.57,
p = 0.007), the shape of the fragment (R2 = 0.56,
p = 0.008), and the Euclidian distance to the nearest
neighbor (R2 = 0.61, p = 0.005). Fragments with
greater edge contrast had lower levels of functional
dispersion and less variance in leaf dry-matter content.
Larger fragments that were irregular in shape and had
closer neighbors showed lower variance in the density
of wood (Fig. 4).

123

Fig. 4 Simple linear regression analysis between functional
diversity and landscape metrics.The patch area (PA) is on a
logarithmic scale, and the Euclidean distance to the nearest
neighbor (ENN) is presented as 1/x. The community-weighted
variances (CWVs) of the leaf dry-matter content and the wood
density were multiplied by 100 to improve visualization.
a Functional dispersion (FDis) as a function of the fragment
Discussion
The effects of fragmentation on the FD associated with
AGB is complex, and gaps in knowledge of these
effects remain (Magnago et al. 2014; Rolo et al. 2018).
Our results suggest that high Andean forest fragmen-
tation does not affect functional diversity associated
with aboveground biomass in terms of richness,
evenness and functional divergence or in terms of
community-weighted mean traits, while the functional
variances of leaf dry-matter content (CWV.CFMS)
and wood density (CWV.DM) and the functional
dispersion index (FDis) related to AGB are sensitive to
the effects of fragmentation. We found that the range
of variation in wood density seems to be sensitive to
the size, shape and nearness of other fragments, and as
the edge contrast of a patch increases, the functional
dispersion and variance in leaf dry-matter content
decrease (Fig. 4), which ultimately influences AGB by
123
Landscape Ecol
edge contrast (ECON, %); b Community-weighted variance of
leaf dry-matter content (CWV.LDMC) as a function of the edge
contrast (ECON, %); c–e Community-weighted variance of
wood density (CWV.WD) as a function of (c) patch area (PA,
ha), d patch shape index (SHAPE), and e Euclidean distance to
the nearest neighbor (ENN, m)
reducing the functional variability in traits that
contribute to this ecosystem process.
The aboveground biomass stocks found in this
study are within the range established by Yepes et al.
(2015) for tropical montane forests south of the
Colombian Andes, and they are larger than those
reported for the same study area by López (2015) and
Pérez and Dı́az (2010) (113.04 Mg ha-1 and
117.8 Mg ha-1, respectively), and those for montane
forests in Colombia, where AGB is estimated to be
between 257.6 and 295.1 Mg ha-1 (Phillips et al.
2011a, b). These differences are attributed to the
method of calculation used in the study, given that we
did not include the variables of wood density and
height, which improve the estimated values compared
with the model based solely on diameter (Chave et al.
2005, 2006; Pérez and Dı́az 2010; Alvarez et al.
2012, 2014). However, when calculating AGB with
the equations established by Chave et al. (2005) and
Alvarez et al. (2012), the stocks we found are similar
Landscape Ecol
to those reported in these studies (Fig. S2). Other
factors, such as soil fertility and moisture and climatic
and topographic conditions, equally influence the
variation in AGB in forests (Laurance et al. 1999; de
Castilho et al. 2006; Peña and Duque 2013), so it is
important to consider them to complement this type of
study.
Our results show that the category of large
fragments had the highest AGB (Fig. 2), which is
similar to the results found by Magnago et al.
(2015, 2016). We found no significant differences in
AGB between fragmentation categories I and II. This
result is associated with the fact that the average basal
area was similar in the small and medium-sized
fragments that were sampled, which is an important
factor determining the biomass value (Baker et al.
2004). This result agrees with the data reported by
Magnago et al. (2015) and Rolo et al. (2018), where
small fragments can store high levels of biomass, since
they can have a structure and tree composition similar
to those of large fragments (Fig. 3). However, cate-
gory III, despite having a similar tree composition,
differs at the structural level from categories I and II
(Fig. 2) because it has a larger number of large trees
(height and basal area). According to Brown and Lugo
(1992), Slik et al. (2013), Berenguer et al. (2014) and
Aldana et al. (2017) large trees are the main contrib-
utors to AGB. Although, tall arboreal individuals with
a large diameter were within the fragmentation
categories I and II recorded, the proportion of these
in category III was higher. This can be related to the
fact that mortality and rates of loss of basal area are
higher within small fragments and, therefore, AGB
decreases, as reported by studies on ecosystems in
southern Brazil (Gross et al. 2018).
In this study, we found an inverse relationship
between edge contrast and functional dispersion
associated with AGB (Fig. 4a), which is explained
by the gradual transitions in land vegetation cover
adjacent to a forest (for example, from forest to
shrubland or types with lower contrast) and the fact
that ecotones where young trees and shrubs are
established allow more-permeable coverings and,
consequently, greater biological connectedness and
less influence of the edge effect (Cadenasso et al.
1997; López-Barrera 2004). This implies an expansion
of habitats that offer more niche space that species can
occupy(Stein et al. 2014; Arellano et al. 2017),
allowing greater functional dispersion and lower
competition per niche, which could improve biomass
reserves. Therefore, habitat heterogeneity between
types of cover can have a positive effect on FD
(Sonnier et al. 2014), and edge effects have a
differential impact on the diversity of plant functional
traits (Guerra et al. 2017). The same pattern is present
in the decrease in the variance of leaf dry-matter
content of the community (Fig. 4b) associated with
high edge contrasts, which implies greater functional
isolation (Matteucci 2004).This suggests that frag-
mentation generates environmental stressors that act
as a filter and may decrease community leaf variability
by favoring the establishment of some species with
leaves tolerant to stress due to their medium–high
LDMC such as Bejaria resinosa, Brunellia propinqua,
Cavendishia bracteata, Miconia ligustrina and Myr-
sine coriacea, which may influence the maintenance
of AGB reserves (Arellano-Rivas et al. 2016).
The fact that functional variation in wood density
(CWV.DM) responded significantly to patch area and
shape and the distance to the closest forest patch
(Fig. 4c–e) suggests a pattern of lower variance in this
trait in large, irregular and nearby fragments. This
pattern is associated with the hypothesis that the forest
fragments of the study area are relicts of a large source
fragment that covered much of the territory in the past,
and now they share species with similar wood
densities because the species in the plant community
prior to fragmentation would have coexisted in local
communities and in a regional species group (Haddad
et al. 2017; Rubiano et al. 2017). The persistence of the
fragments over time (more than 40 years) also
contributes to the stabilization of traits such as wood
density and basal area, as these traits increase rapidly
after fragmentation before stabilizing over time (Lau-
rance et al. 2006). This persistence might also explain
why CWM.WD did not respond significantly to the
fragmentation landscape, a result that suggests that
this functional attribute is not affected by fragmenta-
tion and that is similar to the result reported for the
Atlantic Forest in Brazil (Magnago et al. 2014). This
could be interpreted as the result of high ecological
similarity at the community level, associated with the
predominant genera of these forests, as seen in
Amazonian forests (Baker et al. 2004).
The fragmentation does not appear to alter func-
tional dominance (CWM) and multitrait indexes—
richness, evenness and functional divergence— asso-
ciated with AGB. This is explained by the high
123

taxonomic similarity between fragments ([ 66%
Bray–Curtis similarity, Fig. S3), which host species
with a variety of traits and functional strategies that
show a similar number of functions that contribute to
AGB, regardless of the fragmentation variables eval-
uated (Kooyman et al. 2013; Magnago et al. 2014).
Although some authors have reported that fragmenta-
tion can decrease the FD of plants (Girão et al. 2007;
Rolo et al. 2018), affect evenness and functional
divergence (Magnago et al. 2014), and significantly
increase functional richness (De Frutos et al. 2015),
our results support current hypotheses that argue that
these fragmentation processes do not always lead to a
loss of species and FD because they can follow
numerous response trajectories (Mayfield et al. 2010).
Independent of size, shape and isolation, forest
patches contain groups of species that are functionally
important for the storage of AGB (Fig. 3). Even when
the large fragments (category III) show differences in
AGB, it is clear that they contain high taxonomic
similarity and values of FD similar to those in the
fragments of categories I and II (Kooyman et al. 2013;
Ziter et al. 2013). Our research demonstrates the
importance of small fragments in highly transformed
high Andean ecosystems as FD and AGB reservoirs,
providing incentives to promote their conservation,
restoration and connectivity.
Small fragments of this ecosystem should be taken
into account in the design of multifunctional land-
scapes because i) they are considered stepping stones
to achieve species connectivity, functional linkage and
the continuity of ecological processes (Arroyo-Rodrı́-
guez et al. 2009; Ribeiro et al. 2009; Sfair et al. 2016).
In light of the results of this research, these patches are
important for the maintenance of and increase in
functionality in terms of biomass, since they maintain
considerable amounts of functional diversity and
aboveground biomass. Also, ii) they can help to
diminish edge effects by means of matrix restoration,
and they can act as dampening zones that reduce the
pressure on the largest patches (Hernández-Ruedas
et al. 2014). Additionally, they constitute key pieces in
the conservation corridor of the high Andean
mountains.
Despite the high levels of fragmentation of the high
Andean forest that we studied, functionality associated
with the AGB stock persists in the analyzed categories,
which may be related to the conservation efforts that
take place in the study area, such as the consolidation
123
Landscape Ecol
of the Civil Society National Reserve, the Rı́o Blanco
PFR and the buffer zone of Chingaza NNP. This helps
to protect fragments from human pressure or mini-
mizes this pressure and contributes to the maintenance
of plant community structure. This in turn leads to
recognition of the ecological importance of the
fragments of categories I and II as reservoirs of tree
species that are important for carbon sequestration and
even other ecosystem services that should be evalu-
ated (Tulloch et al. 2016). In this sense, these
fragments could have potential cobenefits for the
payments of the carbon market and/or the protection of
biodiversity (Dı́az et al. 2009; Phelps et al. 2012), and
these benefits are important to consider in future
conservation plans. We clarify that it is necessary to
conserve all forest fragments independent of their size,
since the total quantity and quality of this habitat in the
landscape is key for the maintenance of biodiversity
and ecosystem services (Fahrig 2013; Haddad et al.
2015).
Even though no relationship was found for all the
indexes of functional diversity, we recommend
increasing the number of fragments sampled and
evaluating the effect of fragmentation on other
services of high Andean ecosystems while incorpo-
rating the role of the matrix, the history of land use, the
disturbance regimes and the age of the fragments.
Likewise, we recommend investigating the effects of
fragmentation on the process of functional community
assembly (Mayfield et al. 2005, 2010, 2013), evalu-
ating the intra- and inter specific variation in species
traits in the fragments and studying other functional
traits, in addition to researching the edge effect and
environmental factors that influence the FD and AGB
of the forest. We agree with the suggestion of Poorter
et al. (2017) that the inclusion of functional attributes
should be an integral component of global strategies
for the conservation of biodiversity and ecosystem
services.
Acknowledgements We thank the Thomas van der Hammen
research stimulus program (Bogotá Botanical Garden) for
funding part of this project. We thank friends for their help
with the field work, especially Nicolas P. Cremaschi, and the
owners of the properties where the monitoring plots were
established. Thanks to R. González-M for statistical assistance,
D. Cabrera-Amaya and E. Sastoque for help with the
identification of plants, and the Universidad Distrital for the
use of laboratories and equipment.
Landscape Ecol
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