New Forests
DOI 10.1007/s11056-015-9519-z
Growth of native tree species planted in montane
reforestation projects in the Colombian and Ecuadorian
Andes differs among site and species
Matthew C. Bare1 • Mark S. Ashton1
Received: 9 April 2015 / Accepted: 28 October 2015
Ó Springer Science+Business Media Dordrecht 2015
Abstract The tropical Andes in Ecuador and Colombia are a biodiversity hotspot that has
endured centuries of forest clearance and degradation. Forest restoration has been identified as a regional conservation priority; in recent decades, native species reforestation
projects have proliferated, but little information exists on growth performance of commonly planted tree species in relation to site and soil nutrient status. This study analyzed
growth of seven common native species (Alnus acuminata, Baccharis bogotensis, Cedrela
montana, Myrica pubesens, Quercus humboltii, Sambucus nigra, Smallanthus pyramidalis)
on 12 montane forest sites across the northern region of the tropical Andes. Andean alder
(A. acuminata) was the most commonly planted species, and grows at a mean annual
diameter increment (MAI-d) of 1.81 cm y-1 and a mean annual height increment (MAI-h)
of 0.95 m y-1. S. pyramidalis, a short lived pioneer of the Asteraceae family, also
exhibited fast growth rates of 1.64 cm MAI-d and 1.21 m MAI-h. Andean oak (Q. humboltii) was the second-most commonly planted species, growing with an MAI-d of 0.99 cm
and MAI-h of 0.56 m. Soil magnesium and potassium were significant predictors of MAI-d
and MAI-h for A. acuminata, while soil nitrogen, phosphorous, sodium, and calcium were
negatively associated with growth (p \ .001). We speculate that A. acuminata did not
grow as well on soils richer in calcium and phosphorus because they were less conducive
to nitrogen symbiosis common to this species. Soil magnesium and calcium were significant predictors (p \ .05) of diameter growth for Q. humboltii. For both species, we
attribute growth responses to soil nutrients as a result of the variable nature of fertility in
the complex and variable soils that make up the volcanic and surficial geological landscape
of the northern Andes. Results indicate that native species can grow in a variety of soil
conditions, and exhibit growth rates comparable to non-native species. However, our
results suggest native species are site restricted for best growth and should be planted on
particular soils. We make recommendations for reforestation for the species in this study.
& Matthew C. Bare
mattbare03@gmail.com
1
Yale School of Forestry and Environmental Studies, 360 Prospect Street, New Haven, CT 06511,
USA
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Keywords Restoration Tropical Andes Growth rates Alnus acuminata Quercus
humboltii Nitrogen fixation Smallanthus pyramidalis Soil fertility
Introduction
Worldwide, the area of degraded forest and abandoned agricultural land is growing, and
both passive and active forms of restoration have the potential to conserve biodiversity,
stabilize eroded landscapes, and sequester carbon (Silver et al. 2000). Across the tropics,
large areas of abandoned and marginal agricultural land have potential for establishment of
second-growth forest (Chazdon 2008), and restoration through enrichment planting (Millet
et al. 2013) or native tree plantations (Wishnie et al. 2007; Lamb 2011; Rodrigues et al.
2011). Such restoration activities can facilitate forest recovery and augment forest tree
diversity (Parrotta et al. 1997; Holl et al. 2000; Ashton et al. 2001; Lamb et al. 2005).
The tropical Andes biodiversity hotspot, stretching from Venezuela to Chile, is an
important ecological region with great potential for forest restoration (Conservation
International 2014). Within the tropical Andes, the northern Andean montane forests of
Colombia and Ecuador (Dinerstein et al. 1995) hold high rates of species richness and
endemism (Gentry 1992), but have lost significant areas of natural forest (Etter et al. 2008).
However, many areas of the northern montane forest are experiencing forest regrowth:
between 2000 and 2010, Colombia gained approximately 23,773 square kilometers of forest
and Ecuador 5867 square kilometers, both largely in the montane regions (Aide et al. 2013).
Worldwide studies find that approximately an equal amount of forest area is undergoing
reforestation or natural regrowth as is being deforested (200,000–300,000 km2 y-1), and
that much of the regrowth area is in hilly and mountainous regions on marginal soils and
steep slopes such as in the tropical Andes (Asner et al. 2009).
Within the northern Andean montane forest, conservation of native forest fragments and
forest restoration are conservation priorities (Conservation Internacional Colombia 2014).
Fragments and native tree plantings in these forests are found to be an important source of
plant and bird biodiversity (Kattan et al. 1994; Murcia 1997; Gilroy et al. 2014). One
commonly planted montane tree is Andean alder (Alnus acuminata Kunth.), a fast growing
nitrogen-fixing tree, useful for soil enrichment in silvo-pastoral systems. A comparison of a
native A. acuminata plantation with natural forest regeneration in the Colombian Andes
found that A. acuminata plantings are taller than natural forest re-growth with a similar
basal area, although natural forest regrowth had higher total plant richness (Murcia 1997).
Studies in southern Ecuador have found that A. acuminata can achieve fast growth rates,
even greater than exotics such as Eucalyptus saligna and Pinus patula, especially in gaps
(Weber et al. 2008; Günter et al. 2009).
Despite the importance of forest restoration in the northern Andes, few studies exist on
the growth rates of common native species in diverse sites. Most research examines the
growth of A. acuminata (Cornelius et al. 1996; Rı́os et al. 2004; Medina et al. 2008; Weber
et al. 2008; Günter et al. 2009); these studies test the growth of A. acuminiata of different
seed provenances, or different strains and application methods of the nitrogen-fixing
Frankia bacteria associated with Alnus. In southern Ecuador, a few studies have evaluated
the growth of other native species such as Heliocarpus americanus, Piptocoma discolor,
Cedrela montana, and Juglans neotropica in experimental plots; these studies find that
native early successional trees such as A. acuminiata, H. americanus, and P. discolor grow
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New Forests
fast in planted sites (Weber et al. 2008; Günter et al. 2009). These studies have also found
that seed selection, provenance, and quality are important determinants of planting success,
in addition to silvicultural treatments such as weed control (Stimm et al. 2008; Weber et al.
2008). In this site, Wilcke et al. (2008a) showed that tree growth is also affected by soil
fertility, altitude, and land use history; studies in other tropical montane ecosystems make
similar conclusions (Grubb 1977; Bautista-Cruz and del Castillo 2005). In the Neotropics
more generally, numerous studies have measured growth rates of commonly planted
lowland trees (Worbes 1999 in Venezuela; Hooper et al. 2002, Griscom et al. 2005, and
Wishnie et al. 2007 in Panama; and Haggar et al. 1997 and Piotto et al. 2003 in Costa
Rica). Elsewhere in the tropics, studies have shown that selected native species can achieve
growth rates comparable or superior to those of fast growing exotics (McNamara et al.
2006; Schneider et al. 2014).
Nevertheless, although a few studies provide information on growth of selected species
in experimental conditions, growth data from a wider range of field conditions and soil
nutrient concentrations is necessary for a better understanding of commonly planted species in the northern Andes. In the tropics generally, old and lowland tropical soils are P
limited whereas young, highland tropical soils are more likely to be N limited (Vitousek
and Farrington 1997; Davidson et al. 2004). In the northern Andes, however, soil conditions are highly variable, often a result of volcanic activity and landslides (Bussmann et al.
2008; Wilcke et al. 2008b). There is very little grey literature and no published data on
many tree species that have been more recently planted, such as Smallanthus pyramidalis
Triana., a fast growing Asteraceae tree commonly used for erosion control and live fences.
Another important tree of montane forest, both ecologically and for timber, is Andean oak
(Quercus humboltii Bonpl.). This tree is found in Panama, Venezuela, Colombia, and
Ecuador, and dominates montane forest across much of its range in Colombia (León et al.
2009), but few published data are available on its growth rates and soil affinities.
Restoration practice is growing in the tropical Andes, especially in Colombia and
Ecuador (Murcia et al. 2015). State ministries have directed large-scale reforestation
projects with exotic timbers since the middle twentieth century, and since the 1990s, nongovernmental organizations, international donors, and research institutions have become
engaged in numerous small projects focused on ecological restoration (CESA-Intercooperation Suiza 1992; Endo 1994; Meza et al. 2006; Andrade-Perez 2007; Farley 2007). Most
recently, private sector financing has become more available for restoration via payments
for watershed services, climate change mitigation, and mining offsets (Bare 2014).
However, while many agencies publish general guides, little specific data are available on
native tree plantings.
Colombia has recently prepared a national plan for restoration (Ospina Arango and
Vanegas Pinzón 2010), largely based on the Society for Ecological Restoration primer
(Society for Ecological Restoration 2004). This plan describes restoration of forest
ecosystems with goals of providing habitat connectivity, biodiversity, and ecosystem
functions like water provision, however, it offers little guidance on species selection and
background of established field projects in Colombia. In Ecuador, detailed information
exists about a study site in the southern Andes, but little information is available about
plantings elsewhere in the country.
The first objective of our study was to build on what little has been published and to
evaluate the growth performance of a range of native tree species planted in forest
restoration projects in the northern Andean montane forests. Our second objective is to
compare growth of the most commonly selected tree species in relation to soil nutrition on
reforestation sites.
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Methods
Study area
Sites were located in the montane forest of the northern region of the Tropical Andes,
which covers approximately 423,000 km2 (Dinerstein et al. 1995) (Fig. 1). The montane
forest is normally described as being from an elevation of around 1000 to 3200–3500 m,
where the forest transitions into high altitude grassland known as páramo (Hammen 1974;
Armenteras et al. 2003). In fact, some researchers describe the upper montane—páramo
boundary as human influenced (Sarmiento and Frolich 2002; Bakker et al. 2008). Lower
montane forests have an average annual temperature between 19 and 23 °C with an annual
precipitation ranging between 1500 and 1700 mm. Upper montane forests have an average
annual temperature between 9 and 16 °C, with an annual precipitation between 700 mm in
dry inter-Andean valleys to 3000 mm on slopes of the wetter Pacific-side (Olson et al.
Fig. 1 Map depicting study sites in Colombia and Ecuador
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New Forests
1995). Vegetation changes rapidly along the altitudinal gradient. Lower elevation forests
are dominated by palms (Arecaceae), and the angiospermous families Melastomataceae,
Lauraceae, Rubiaceae, Malvaceae, and Fabeaceae. Higher elevation forests transition to
Myricaceae, Fagaceae, Clusiaceae, Ericaceae, and Asteraceae, while palms and Melastomataceae remain common (Armenteras et al. 2003; Homeier et al. 2008). Much of the
higher montane forest on wet slopes in Colombia is dominated by Andean oak (Q. humboltii) (León et al. 2009). Higher elevation forests have lower total species richness but
normally higher rates of endemism, particularly among vascular epiphytes (Gentry 1992).
Most of the northern Andes as a whole are volcanic ash derived soils (Andisols). These
soils typically display high amounts of soil carbon, dense networks of micropores, high
water retention, and low bulk density (Tonneijck et al. 2010). Aluminum–humus complexes are common in acidic soils (Zehetner et al. 2003). Other areas in the Andes shaped
by erosion and landslides or that were not derived from volcanic ash deposits are classified
as Entisols or Inceptisols (Cambisols) (Wilcke et al. 2008b). Throughout much of the
northern Andes, landslides are common and play a significant role in the soil heterogeneity
and shaping forest vegetation (Bussmann et al. 2008).
The northern Andean montane ecosystem is the most densely settled area of Ecuador
and Colombia, and agriculture has been the primary driver of land use change over the past
several centuries (Sarmiento and Frolich 2002; Etter et al. 2008). In Colombia, approximately 75 % of the population lives in the Andean region; in Ecuador it is approximately
50 % (Colombia Censo General 2005; Ecuador en Cifras Resultados 2015). Land use
activity in the higher areas is most often associated with potato cultivation, and coffee and
fruit trees in the lower lying areas, although cattle pasture is common throughout the region
and is replacing some agricultural crops (Etter et al. 2006; Guhl 2008). Coffee cultivation
is focused on areas of better access and soil fertility, whereas cattle pasture and establishment of natural second-growth is more likely to occur on less fertile soils and on steep,
remote mountain areas (Etter et al. 2006; Asner et al. 2009; Aide et al. 2013). Across the
region, forest fragments are spread throughout the agricultural landscape (Etter et al. 2006;
Murgueitio et al. 2011; Lerner et al. 2014). Mining is practiced throughout the region, but
is a minor driver of forest clearing compared to agriculture (Etter et al. 2008).
While most forest clearing in the Andean montane ecosystem occurred over the past
centuries, some clearing continues today. In Colombia nationwide, Hansen et al. (2013)
calculate a rate of forest loss of 3.0 % from 2000 to 2012 or an average annual loss of
0.25 % (in the forest cover[25 % threshold). The areas with highest amounts of forest loss
were the departments of Caquetá, Meta, and Antioquia; all located primarily in montane—
lowland forest transition zones of the Andes. In Ecuador, Hansen et al. (2013) calculate a
2.7 % forest loss from 2000 to 2012 or 0.23 % average annual rate of forest cover loss. The
areas with the highest amounts of forest loss were the lowland Amazon and coastal regions,
although other studies find high continued rates of forest loss in montane regions of
southern Ecuador (Tapia-Armijos et al. 2015).
Site selection
Our study sites were focused on projects with a native forest restoration goal. Timber
plantations using exotic trees were excluded. Forest restoration projects were identified
using expert interviews and internet search, followed up with interviews with key informants. Project managers from various sectors (academic, government, NGO) were contacted for background information, project reports, and interviews. Seventy projects,
primarily in the montane region of the two countries, were identified and catalogued.
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Project data was triangulated when possible using written reports, interviews with project
managers, and third party interviews with other restoration practitioners in the region.
Of seventy projects catalogued as the most promising based on our initial survey and
interviews, sixteen were selected for field visits and data collection. These sites were
selected because they had an implementation record of [5 years (established prior to
2008), availability of information about date of planting and species planted, and a basic
record of site protection (not necessarily maintenance of the planted trees, but merely
protection of the site from fire or re-conversion to pasture or agriculture). Of the 16 sites
where data were collected, four were discarded after site survey because of site abandonment or unclear planting data; the remaining 12 were finally used for data analysis. The
goals of these restoration projects were for a mix of purposes including scientific research,
conservation and landscape connectivity, watershed protection, and agroforestry (live
fences, nutrient retention). Most sites were fenced to prevent cattle grazing, but not fertilized and only minimally weeded (see Appendix 1 for complete site details and
objectives).
Sampling design
Because sites were derived from a variety of sources, planting design and species varied
greatly. In the study sites, trees varied between 5 and 15 years of age and were spaced
between 2 and 5 m. Study sites were grouped into large ([2 ha) and small (\2 ha). Small
sites were sampled via census (all trees were measured); in large sites, three line transects
crossing the entirety of the planting site (50–500 m) were selected randomly, and all trees
within 5 m of the center line were measured. In all sites, planted trees with height greater
than diameter at breast height (dbh) (1.3 m) were identified to species, measured for dbh,
and ocular estimates of tree canopy height made to the nearest half meter, using a survey
rod for calibration. Data was collected in 2013 (see Appendix 1 for details).
Soil samples were collected from 3 to 5 random locations at each restoration site;
approximately 100 g were collected from the A horizon, approximately 2–4 cm below the
mineral soil surface. Composite samples from each site were analyzed in the field for
texture and then air dried and shipped to the U.S. for chemical analysis. Air-dried samples
were analyzed for pH at the Yale School of Forestry and Environmental Studies soil
laboratory (Greeley Memorial Laboratory). Soil carbon, organic matter, cation exchange
capacity, and additional nutrients (N, P, K, Na, Mg, and Ca) were analyzed at the
University of Georgia Department of Crop and Soil Sciences Lab for Environmental
Analysis. Dissolved carbon was determined using a Shimadzu TOC-5050A Total Organic
Carbon Analyzer. Analysis was based on loss of ignition (David 1988). All other elements
were determined by spectrophotometric methods and ion chromatography using a DIONEX DX500 modular system (University of Georgia University of Georgia Laboratory for
Environmental Analysis 2015).
Data analysis
Based on the data gathered, a total of seven species were identified for data anlysis: A.
acuminata Kunth. (Betulaceae, known locally as aliso, or Andean alder in English), B.
bogotensis Kunth. (Asteraceae, known locally as chilco), C. montana Moritz ex Turcz.
(Meliaceae, known locally as cedro de montaña), Myrica pubesens Humb. & Bonpl. ex
Willd. (Myricaceae, known locally as laurel de cera), Q. humboltii Bonpl. (Fagaceae,
known locally as roble, or Andean oak in English), S. nigra L. (Adoxaceae, known in
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English as elderberry, native to Europe), and S. pyramidalis Triana. (Asteraceae, known
locally as arboloco). Mean annual increment for height and diameter were calculated by
taking measurements in 2013 and averaging growth over the age of the tree. Two-way
analysis of variance (ANOVA) was performed to test significance of species, site, and
interaction effects on mean annual increments of diameters and height (MAI-d, MAI-h) of
the seven common species in the study. Mean annual increments were compared among
sites and among species for statistical significance using a Tukey test. Multiple regression
analysis (backwards stepwise, Minitab 16) was used on soil nutrient variables for the MAId and MAI-h of the two most commonly found trees, A. acuminata and Q. humboltii. Soil
texture, pH, organic matter, soil carbon, cation exchange capacity, aluminum, and site
elevation showed no significant effects and were removed from further analysis. Sampling
design and data analysis draw significantly on a similar study conducted by (Schneider
et al. 2014).
Results
A total of 802 trees were measured of 45 different species. Statistics were calculated on
the seven species most commonly found across the 12 sites. A. acuminata was by far the
most commonly planted species, being a popular restoration tree for its fast growth and
nitrogen-fixing ability. A. acuminata represented 44 % of all trees sampled across
reforestation sites, planted at seven sites. Q. humboltii was found at four sites and S.
pyramidalis, a fast-growing, short-lived Asteraceae tree common to disturbed areas, was
found at three sites. Mid-successional timber trees such as C. montana, Tabebuia rosea
(Bignoniaceae), J. neotropica (Juglandaceae), and Podocarpus spp. (Podocarpaceae)
were planted at several sites, but many individuals of these species had died due to
intense competition with pasture grass (see Appendix 2 for a partial list of species
planted).
Growth rates between species were significantly different, as were growth rates between
sites (Table 1). The interaction effect between site and species was significant, indicating
that species differed in their growth rates and changed ranking in relation to each other
across the different restoration sites and soils. Tukey studentized t test comparisons of
growth rates among species revealed A. acuminata had the greatest diameter growth,
averaging 1.81 cm y-1, along with S. pyramidalis at 1.63 cm y-1 (Fig. 2). Growth was
significantly greater in these two species compared to all other species measured except C.
Table 1 Two-way ANOVA of mean annual increment for diameter (cm) and height (m) by sites, species
and interaction between sites and species
Source
N
df
Mean
12
11
1.40
7
6
1.21
SD
R2 (adj)
F
p
0.47
5.303
\.0001
0.41
4.094
.001
2.944
.001
MAI-d (cm)
Site
Species
Site 9 species
17
.553
MAI-h (m)
Site
Species
Site 9 species
12
11
0.82
0.26
5.368
\.0001
7
6
0.71
0.32
8.504
\.0001
7.357
\.0001
17
.573
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Fig. 2 Mean annual increment of seven commonly planted species recorded. Gray bars show diameter
growth (mean annual increment) and hatched bars show height growth (mean annual increment). Error bars
depict standard errors. Letters indicate Tukey grouping: species that do not share a letter are significantly
different, for example, mean diameter increment in A. acuminata is statistically significantly different from
B. bogotensis but not from S. pyramidalis. See Appendix 2 for average mean annual increment of other
species measured
montana. C. montana showed a wide range of growth rates perhaps because of a small
sample size or its inherent variability in growth and site establishment. B. bogotensis, S.
nigra, and Myrica pubenscens are all small spreading trees and exhibited moderate to slow
diameter growth but high rates of canopy spread.
Smallanthus pyramidalis showed the highest mean annual increment for height at
1.21 m y-1, which was significantly greater than all other species (Fig. 2). A. acuminata
averaged 0.95 m y-1, not statistically different from B. bogotensis and C. montana, but
statistically different from the 0.56 m y-1 average height growth of Q. humboltii.
Two high elevation pasture sites exhibited the greatest MAI of diameter and height,
largely because these sites are dominated by fast-growing A. acuminata (Fig. 3). Reasons
for slow growth rates in certain sites include species selection and land use history; the
slowest growing site was a previous mine site, and the second-slowest site was a 16-year
monodominant plantation of Q. humboltii.
Regression analysis of A. acuminata and Q. humboltii, the two species found at more
than three sites, showed that diameter and height growth varied significantly in relation
to soil fertility (Table 2). Diameter of A. acuminata was positively correlated with
magnesium and potassium, and negatively correlated with nitrogen, sodium, phosphorous, and calcium. Q. humboltii diameter growth was positively correlated with magnesium and calcium, but height was positively correlated with only magnesium. Soil
nutrients explained between 34.18 and 44.60 % of the variation in growth rates for the
two species.
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Fig. 3 Mean annual increment of planted species at various restoration sites. Gray bars show diameter
growth (mean annual increment) and hatched bars show height growth (mean annual increment). Error bars
depict standard errors. See Appendix 1 for full site description
Table 2 Significant predictors of mean annual increment of diameter (MAI-d) and mean annual increment
of height (MAI-h) in two species found at more than three sites
Species
Degrees
of
freedom
Regression coefficient
N
Na
Mg
P
K
Ca
R2
adj
MAI-d
A. acuminata
6
-1.6**
-.045**
0.003**
-0.093**
0.002**
-0.001**
44.6
Q. humboltii
3
ns
ns
0.001*
ns
ns
0.0002*
34.18
MAI-h
A. acuminata
6
-0.624**
ns
0.001**
-0.039**
0.001**
-0.0003**
37.93
Q. humboltii
3
ns
ns
0.001**
ns
ns
ns
44.14
Significance levels ** p \ .001; * p \ .05
Discussion
Growth of native species
Compared with other studies of A. acuminata, average diameter growth across the present
sites in Ecuador and Colombia was about average (1.81 cm y-1) compared to that reported
for other studies elsewhere in the northern Andes and Costa Rica (e.g. 0.90–2.96 cm y-1;
Table 3). Many of these studies tested different provenances or experimental Frankia
bacteria inoculation treatments; most collected mean annual increment measurements
systematically over the first 6–24 months of plant growth as compared to this study that
evaluated much older plantings but inferred growth from time since planting. However, A.
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acuminata growth in our study was comparable to growth of other commonly planted
native and exotic plantation species in the Andean region (Table 3), see also (Günter et al.
2009).
Quercus humboltii averaged faster diameter growth compared to the literature
(Table 3), but the only literature available was from secondary forest with strong competition from other species, not a plantation where trees are purposefully spaced to provide
open growing space. S. pyramidalis showed similar rapid growth, but is short lived and less
valued for timber.
Table 3 Growth rates of A. acuminata and Q. humboltii in various restoration sites and trials in the
Tropical Andes and montane Neotropics, compared with exotics A. decurrens and P. patula. Measurements
from this study are in bold
Species
Location
Treatment
Diameter
growth
(cm)
Method
Source
A. decurrens
Colombia
(Caldas)
No treatment
1.83
During 15 months
Quiceno and
Medina (2006)
A. decurrens
Colombia
(Antioquia)
None
During 1 year
Medina et al.
(2008)
A. acuminata
Colombia
(Caldas)
No treatment
3.28
Daily growth during a
few months
extrapolated to year
Rı́os et al.
(2004)
A. acuminata
1780 m
Costa Rica
Plantation
2.96
Averaged over the life
of 9 years
Roque et al.
2009
A. acuminata
Turrialba
Costa Rica
Plantation
2.00
Over 40 months
Cornelius et al.
(1996)
A. acuminata**
Northern
Andes
(various)
Various
1.81
Averaged over the life
of several years
Present study
A. acuminata
Colombia
(Jardin,
Antiq)
Rhizospheric
organisms
1.64
Average of 6
treatments during
16 weeks
Molina et al.
(2008)
A. acuminata
Colombia
(Antioquia)
Rhizospheric
organisms
1.31
During 1 year
Medina et al.
(2008)
A. acuminata
Ecuador
(Loja)
Shade
1.13
During 24 months
Aguirre and
Weber (2007),
unpublished
A. acuminata
Colombia
(Antioquia)
None
0.88
During 1 year
Medina et al.
(2008)
Quercus
humboldtii**
Colombia (4
sites)
Plantation
0.99
Averaged over the life
of several years
Present study
Quercus
humboldtii
Colombia
16 year
secondary
forest
0.58
Averaged over the life
of several years
Becerra (1989)
Quercus
humboldtii
Colombia
2nd forest
0.21
Averaged over the life
of several years
León et al.
(2009)
P. patula
Colombia
4.5 year
plantation
2.11
During 3.5 years
Endo and Mesa
(1992)
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Soil nutrients
Regressions showed A. acuminata diameter and height growth was positively correlated
with magnesium and potassium concentrations and negatively correlated with nitrogen,
sodium, phosphorous, and calcium. Interestingly, our study suggests that magnesium and
calcium are strong positive and negative predictors respectively of tree growth for the two
species tested. This may be related to the large difference in fertility of northern Andean
soils of volcanic (often fertile, high pH, high cation exchange capacity, high calcium) and
non-volcanic glacial origin (often low fertility, low pH, low cation exchange capacity, low
calcium). In particular, the nitrogen fixing species A. acuminata did not grow as well on
soils richer in calcium and phosphorus (we suggest these soils are Andisols), perhaps
because they were less conducive to nitrogen symbiosis. We speculate that species growth
could also be negatively affected by other interacting site factors that we did not measure
such as wind, animal browse, site treatment (use of herbicides, weeding) or soil moisture
availability. In this study, sites practicing silvo-pastoral management protected planted
trees with fencing, but animal browsing still could have occurred from smaller native
herbivores.
The finding that A. acuminata is negatively associated with soil nitrogen is interesting,
as it is a nitrogen-fixing tree. In sites with dense stands of A. acuminata, one would expect
higher growth to correspond with higher soil nitrogen, not necessarily because the tree
responds to nitrogen fertility but because the tree enriches the soil with N fixation and
litterfall. However, it is also possible that A. acuminata grows slower in high nitrogen sites
because its association with nitrogen-fixing bacteria is absent (the symbiotic relation is not
necessary) and because of greater competition with grass and other surrounding nitrogendemanding vegetation, particularly when sites are not maintained (Davidson et al. 2004).
A. acuminata is also ectomycorrhizal, suggesting that it can grow well in low-nutrient
environments (Becerra et al. 2005). Similarly, a study of Alnus nepalensis in India found
that seedlings with mycorrhizal fungi grew slower in conditions of higher soil fertility (Jha
et al. 1993).
Quercus humboltii diameter growth was positively correlated with increased amounts of
soil magnesium and calcium. Height growth was correlated with magnesium. Again, like
Alnus, Quercus is an ectomycorrhizal genus. Other studies have shown that the symbiotic
plant-fungal relationship makes Quercus more nutrient-use efficient, particularly for
phosphorous and magnesium (Lehto and Zwiazek 2011; Simard et al. 2003). Other studies
have found that ectomycorrhizal presence is a stronger predictor of tree growth than soil
fertility (Zangaro et al. 2007), suggesting that parameters other than soil fertility (e.g. soil
water availability) could explain the growth of these species. Lastly, studies in the Andes
found that soil texture was an important predictor of plantation tree growth, specifically,
that trees grew better in clay loam (Henri 2001); while eroded soil significantly reduces
growth (Carpenter et al. 2004). In this study, soil texture was not correlated with growth of
planted species.
Finally, it is important to note that the height and diameter growth measured in this
study represents only one form of plant response to soil fertility. Growth allocation aboveand below-ground can differ among species. Early-successional species in fertile environments usually allocate growth to above-ground biomass, whereas mid and late-successional species often allocate more growth below-ground, especially in nutrient poor and
drought-stressed soils (Poorter 2001; Zangaro et al. 2007). In this study, elevation was not
found to be a significant predictor of tree growth, possibly because elevation effects were
123
New Forests
modified by species selection or site history. Some low elevation sites were slow growing
because they contained mid-successional trees instead of fast growing pioneers (sites 4 and
6 in Appendix 1), while some high elevation sites were fast growing because they contained fast growing A. acuminata (sites 8 and 9 in Appendix 1). Moreover, many low and
mid-elevation sites suffered a more intense land use history with greater erosion (sites 1, 2,
4, 10, and 12), whereas the high elevation sites experienced a lighter land use history of
low intensity pasture. Finally, an additional factor not evaluated in this study is the effect
of seed provenance and quality, as well as silvicultural treatments after planting, factors
which have been found to influence tree survival and growth (Stimm et al. 2008; Weber
et al. 2008).
Management applications
Not surprisingly, mid-successional species such as Q. humobltii and C. montana showed
slower diameter and height growth than pioneer species A. acuminata and S. pyramiadlis.
In this study, C. montana exhibited slow growth but with significant variability; other
studies that monitored plantings of the related Cedrela odorata in tropical lowland sites
of Central America report similar levels of variability (Wishnie et al. 2007). In this
study, other mid-successional species, Juglans neotropica, T. rosea, and Podocarpus
spp., were planted at five sites but all were \1 m in height and many were in poor
health, with few leaves and slow growth (personal observation). These slower-growing
species likely had trouble competing with the pasture grass present in almost all sites, a
factor that has been identified to inhibit tree recovery of J. neotropica and C. montana in
southern Ecuador (Günter et al. 2009), as well as for other mid-successional species in
other tropical montane sites (Aide and Cavelier 1994; Sarmiento 1997; Holl et al. 2000)).
Additionally, a study in one of the same field sites used in this study (Estación Cientı́fica
San Francisco, southern Ecuador) finds that lack of mycorrhizal association may be a
limiting factor for reforestation, and that inoculation can assist seedling establishment
(Urgiles et al. 2009).
In this study, short-lived pioneer trees such as S. pyramidalis, Verbesina crasirramea,
and Ochroma pyramidalis, as well as longer-lived A. acuminata may be effective at
facilitating site conditions for mid-successional species. Some site managers practice this
facilitation intentionally by first planting pioneers and later enrichment planting the midsuccessional species. Other site managers practice facilitation unintentionally by planting
all species at once, and letting the more rapidly growing pioneer trees facilitate site
conditions for the mid-successional species. In southern Ecuador, shrubs and ferns were
found to facilitate the growth of certain mid-successional species (Günter et al. 2009),
while in a meta-study of various restoration sites, facilitation has been found to assist
tree growth in mixed species plantings (Piotto 2008). Similarly, in this study, many sites
with dense infestations of the invasive leguminous shrub Ulex europaeus (gorse, or
retamo espinosa in Spanish, a species native to Europe but common throughout the
northern Andes) are treated with mechanical removal of gorse and broadcast seeding of
the bi-annual herbaceous plant Lupinus bogotensis to provide growing space and sunlight
for pioneer tree species and hopefully prevent re-colonization by the gorse. Use of nurse
plants such as Lupinus for restoration has been described widely in the literature
(Callaway and Walker 1997; Gómez-Aparicio et al. 2004; Blanco-Garcı́a et al. 2011;
Reyes and Rı́os 2011). Although it is practiced for site amelioration in areas of Ulex
123
New Forests
europeus colonization, some studies have found that nitrogen-fixing plants such as
Lupinus can actually facilitate weed invasion in habitats of native plants (Maron and
Connors 1996). Elsewhere, numerous researchers have recommended facilitation or site
amelioration using fast-growing species, either native or exotic (Brockerhoff et al. 2008;
Jacobs et al. 2015). In Costa Rica, Carpenter et al. (2004) recommend Pinus tecunumanii
to stabilize soil, provide habitat for seed dispersers, suppress weeds, and moderate
microclimate conditions, thus facilitating the establishment and growth of natives. In
Mexico, de la Luz Avendaño-Yáñez et al. (2015) find that P. patula plantations can
facilitate survival of native mid-successional trees (although inhibit growth). Parrotta
et al. (1997) and Holl et al. (2000) conclude that remnant pasture trees and fast-growing
pioneer trees are necessary to attract seed-dispersers and facilitate restoration. Similarly,
in sites with depleted soils or extreme microclimatic conditions (sun and wind), exotics
with wide ecological amplitudes may be necessary to ameliorate conditions for native
species with smaller niches (Calvo-Alvarado et al. 2007).
Other studies in the region have found nitrogen-fixing trees such as Inga spp. to be a
valuable means of site amelioration in degraded pasture in the Andes (Rhoades et al. 1998).
A. acuminata can be a valuable component of agroforestry systems, where it can serve as a
source of nitrogen fertilization for grass and as shade for cattle (Russo 1990). In southern
Ecuador, researchers have described the economic potential of agroforestry systems where
farmers rotate pasture and A. acuminata in order to reduce pressure on cutting of new
mature forest (Knoke et al. 2009). Similarly, groups in Colombia promote silvo-pastoral
systems with nitrogen-fixing A. acuminata and cattle fodder plants such as Leucaena
leucocephala, (Calle et al. 2009) as found in the sites of Pedro Palo and Rio Guacha in this
study.
Across the region, it should be noted that restoration sites observed in this study were
designed primarily for demonstration or research purposes and required significant
resource investments for planting and site maintenance. At the same time, much of the
region is undergoing a forest transition (Aide et al. 2013), where a significant amount of
land is returning from pasture and agricultural use back to forest. A recent study in
Colombia (Sánchez-Cuervo et al. 2012) found 28,000 km2 of area was reclaimed as second-growth from 2001 to 2010, approximately twice as much land as areas that had lost
vegetative cover (deforestation). Most of the reforested areas have occurred from agricultural abandonment, a finding consistent with analysis across Latin America (Aide and
Grau 2004; Rudel et al. 2009; Aide et al. 2013). Steep mountain pasture and coffee areas
are often the most marginal and are abandoned due to urbanization, low agricultural prices,
and/or rural violence (Etter et al. 2006, 2008). In a low-elevation montane forest region of
Ecuador, one study found increasing trends of spontaneous silvo-pastoral landscapes
(Lerner et al. 2014). In highly degraded sites with low nutrient levels such as the mines and
semi-urban areas observed in this study, active restoration may be needed. However, in the
mildly disturbed agricultural landscapes that comprise a significant area of the northern
Andean montane region, active restoration can be combined with agroforestry and silvopastoral systems, using fast growing species such as A. acuminata. These species provide
rapid nutrient inputs to degraded soil, and frequently have greater timber value than other
early-succession trees (Knoke et al. 2009). In most cattle pasture areas, re-vegetation with
native species occurs naturally, although active management can promote the introduction
123
New Forests
of more valuable timber species (Calle et al. 2009; Murgueitio et al. 2011). In the fragmented agricultural landscapes that compose much of the tropical Andes, we suggest these
types of agroforestry-oriented restoration activities in order to minimize costs while
facilitating landscape connectivity.
Conclusions
This study provides valuable baseline information on commonly planted native tree
species in montane forests of the northern Andes. Restoration projects in Ecuador and
Colombia, including the ones observed in this study, are largely focused on these
montane forests, and have multiplied in the last two decades (Bare 2014; Murcia et al.
2015). Many of these projects involve silvo-pastoral landscapes (Murgueitio et al.
2011), payments for watershed services (Goldman-Benner et al. 2012; Sáenz et al.
2014), and are driven by local or national governments (Bare 2014; Murcia et al.
2015). We show that native species, in particular Andean alder (A. acuminata), grows
fast in a range of restoration sites and soil conditions, but particularly those soils that
are relatively young and low in nitrogen. Our study contributes to a growing body of
literature that native species such as those studied can grow well on degraded sites in
the northern Andes (Murcia 1997; Günter et al. 2009).
Acknowledgments The authors are grateful for financial support received from the Tropical Resources
Institute at the Yale School of Forestry and Environmental Studies and the Gordon and Betty Moore
Foundation. Numerous colleagues have assisted with research planning, including Tina Schneider, Florencia
Montagnini, Eva Garen, Alicia Calle, and Gillian Bloomfield of the Yale School of Forestry and Environmental Studies and the Environmental Leadership and Training Institute. In Colombia and Ecuador, the
authors are grateful for the assistance of Carolina Murcia of CIFOR, Jose Ignacio Barrera of the Universidad
Javeriana, Orlando Vargas of the Universidad Nacional, Nikolay Aguirre of the Universidad de Loja, dozens
more experts in the fields of conservation and forest restoration, and dozens more project managers,
technicians, guides, ranchers, and farmers.
Appendix 1
See Table 4.
123
5
4
3
2
1
Bogotá
Cerros Occidentales,
Location
74.058302°W
4.604232°N,
Lat Lon
2700
Elevation
Colombia
Cordillera,
Eastern
Geography
West
Aspect
Loam
Soil
texture
2009
Date
established
Part of 34.5 ha
Size
Bogotá
Cerros Occidentales,
74.058428°W
4.603920°N,
2700
Colombia
Cordillera,
Eastern
West
Loam
2008
34.5 ha
Chisaca, Bogotá
74.172475°W
4.375763°N,
3160
Colombia
Cordillera,
Eastern
Flat
loam
Sandy
2006–2008
10 ha
Ebejico, Antioquia
75.760636°W
6.278767°N,
1700
Colombia
Cordillera,
Western
North
sand
Loamy
2007
enrichment, 100 ha of protection
100 ha of passive restoration, 100 ha of
Francisco, Loja,
Ecuador
Francisco
Estación Cientı́fica San
Cientı́fica San
Estación
79.085204°W
3.968652°S,
2340
Ecuador
Cordillera,
Eastern
South
loam
Silty
2003
4 ha
Context: abandoned pasture, managed by the local public land corporation. Restoration included planting (multiple species, scattered) but very little maintenance
Ebejico
CORANT—
scattered) and periodic weeding, but little enrichment planting
Nacional (Bogota), for the purpose of scientific study and public demonstration. Restoration includes mechanical removal of the invasive plant, native plantings (multiple species,
Context: site of a municipal water storage area, invaded by Ulex europaeus. Restoration is undertaken by the public water utility of Bogota in coordination with the Universidad
facilitation
Chisaca-
europaeus, native plantings (multiple species, scattered), continual maintenance and weeding, and continual enrichment plantings
Context: same as Cerros-Eucalyptus site, but the area was invaded by gorse (Ulex europaeus) during the 1990s and 2000s. Restoration activity includes mechanical removal of Ulex
Cerros-Gorse
areas of native montane forest. Restoration includes native plantings (multiple species, scattered), continual maintenance and weeding, and continual enrichment plantings
Context: site of a 100-year old Eucalyptus reforestation, currently undergoing restoration by the botanic garden of Bogota with public funds. Objectives are to create demonstration
Eucalyptus
Cerros-
Project name
Table 4 List of the twelve reforestation sites used for this study in Colombia and Ecuador
New Forests
123
123
9
8
7
6
Location
Lat Lon
Elevation
Geography
Aspect
Soil
texture
Date
established
Size
Cundimarca
Laguna Pedro Palo, Tena,
74.386229°W
4.685656°N,
2180
Colombia
Cordillera,
Central
Flat
Loam
1998
\5 ha
Cundimarca
Laguna Pedro Palo, Tena,
74.377331°W
4.685193°N,
2020
Colombia
Cordillera,
Central
Flat
Loam
2008
2–5 ha
Nono, Pichincha, Ecuador
78.608061°W
0.095844°S,
2820
Ecuador
Cordillera,
Western
East
loam
Sandy
2006
3 ha
Guasca, Cundimarca
73.914223°W
4.794627°N,
3200
Colombia
Cordillera,
Eastern
North
sand
Loamy
2007
\2 ha
in 2007 (one species, row plantings), with infrequent weeding
Context: land is a nature reserve, owned by a national NGO. The restoration project aims to restore a small area of the reserve that was previously in cattle pasture. Area was planted
Reserva Encenillo
abandoned pasture, in land managed by a public agency. Area is not maintained
Context: project was conducted by a national NGO with funding to conduct voluntary carbon offsets for international donors. Area was planted in rows (multiple species) on an
Profafor
species. Area is fenced from cows but not weeded
funded by various public agencies. Restoration included initial planting (multiple species, scattered) and enrichment planting of mid-successional species below the pioneer
Context: restoration objective is the establishment of silvo-pastoral system with live fences and ecological corridors; project is coordinated by a local citizen’s association and
corridors
Pedro Palo
public agencies. Restoration included initial planting (one species, row planting) but little maintenance; area is fenced to protect plantings from cows
Context: restoration objective is the enlargement of an oak forest originally found bordering a lake. Project is coordinated by a local citizen’s association and funded by various
Pedro Palo lake
area is fenced from cows but not weeded
Context: restoration is part of an ongoing scientific experiment operated between a local university, a national NGO, and donors. Plantings were done in rows with multiple species;
Project name
Table 4 continued
New Forests
12
11
10
Suesca, Cundimarca
Location
73.781451°W
5.404071°N,
Lat Lon
2600
Elevation
loam
Colombia
Silty
Soil
texture
clay
Flat
Aspect
Cordillera,
Eastern
Geography
2005–2013
mostly
Date
established
\2 ha along river corridor
Size
Rio Guacha area, Boyacá
73.090559°W
6.138158°N,
2000
loam
Colombia
Silty
clay
South
Cordillera,
Eastern
2008
\2 ha live fences
Cundimarca
OI Peldar, Zipaquira,
73.867447°W
5.067165°N,
2760
Colombia
Cordillera,
Eastern
Flat
loam
Sandy
2003
1 ha
establishment of soil (available on-site), and planting of multiple species (native and exotic), scattered
Context: restoration project is the rehabilitation of an abandoned sand mine; conducted by an environmental consulting firm for a mining company. Restoration involves re-
Zipa mine
by a national NGO in coordination with local landowners (on private land). Plantings are done in rows, maintenance is rare but plantings are fenced off from cows
Context: restoration objective is the establishment of a silvo-pastoral system with live fence and ecological corridors throughout a cattle pasture landscape; restoration is undertaken
Rı́o Guacha
functions. Area is continually weeded and enrichment planted with multiple species
Context: land is the riparian corridor (public right-of-way) of a small waterway. Restoration is performed by a local NGO. Restoration aims to prevent erosion and restore ecosystem
Rio Bogota
Project name
Table 4 continued
New Forests
123
New Forests
Appendix 2
See Table 5.
Table 5 Diameter growth rates of species planted in the 12 study sites (includes species with at least three
individuals planted)
n (trees sampled)
n (sites planted)
MAI—diameter (cm)
SD
Origin
1
A. decurrens
8
1
1.51
0.79
Non-native
2
A. melanoxlyn
6
1
1.02
0.63
Non-native
3
A. acuminata
356
7
1.81
0.74
Native
4
Oreopanax sp.
7
1
1.07
0.38
Native
5
B. bogotensis
39
3
1.31
0.34
Native
6
C. montana
6
3
1.07
0.47
Native
7
C. lusitanica
30
1
1.09
0.28
Mexico
8
Citharexylum sp.
4
2
1.04
0.16
Native
9
Escallonia sp.
12
1
0.63
0.18
Native
10
Eucalyptus sp.
21
1
1.31
0.63
Non-native
11
H. americanus
13
1
1.14
0.61
Native
12
Isertia sp.
5
1
0.61
0.14
Native
–
13
Lauraceae sp.
5
1
0.99
0.18
14
L. vulcanicola
23
2
1.16
0.26
Native
15
M. pubescens
24
3
0.58
0.17
Native
16
O. pyramidalis
17
1
1.36
0.69
Native
17
P. patula
15
2
1.87
0.78
Mexico
18
P. discolor
10
1
0.74
0.22
Native
19
Q. humboltii
53
4
0.99
0.42
Native
–
20
Rubiaceae sp.
6
1
1.52
0.30
21
S. nigra
8
3
1.13
0.18
Non-native
22
S. pyramidalis
52
3
1.64
0.53
Native
23
T. lepidota
24
2
0.93
0.22
Native
24
V. crasirramea
23
1
1.69
0.45
Native
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