Ecological Engineering 117 (2018) 50–61

Contents lists available at ScienceDirect

Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Active versus passive restoration: Recovery of cloud forest structure, T

diversity and soil condition in abandoned pastures
⁎
Alma L. Trujillo-Mirandaa, Tarin Toledo-Acevesa, , Fabiola López-Barreraa,
Patricia Gerez-Fernándezb
a
Instituto de Ecología A. C. Carretera antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, Mexico
b
Instituto de Biotecnología y Ecología Aplicada, Universidad Veracruzana, Veracruz, Mexico

A R T I C LE I N FO A B S T R A C T

Keywords: Tropical montane cloud forest is a priority ecosystem for restoration due to the diversity and ecosystem services
Biodiversity it provides and because it is under severe threat. Forest restoration can be achieved by active interventions and/
Disturbance or natural regeneration (passive restoration). However, there has been little comparison of the effectiveness of
Mixed plantation active versus passive restoration strategies and even fewer studies have monitored the long-term success of forest
Regeneration
restoration practices. We assessed the effectiveness of active (mixed plantation with native species) and passive
Resilience
Secondary forest
(areas adjacent and non-adjacent to mature cloud forest) restoration strategies implemented in pastures with
21 years of exclosure, and compared these to a mature cloud forest (reference system), in eastern Mexico. In the
mature forest and in the areas represented by each restoration strategy, ∼15 plots (200 m2) were established in
order to assess forest structure, tree diversity and soil properties as indicators of restoration success. Active
restoration proved more effective than passive restoration at recovering forest structure (e.g. higher basal area,
tree density and height). Adult tree diversity was similar across all restoration sites and the mature forest, while
composition differed greatly between the mature forest and each of the restoration sites, from which the
characteristic mature cloud forest tree species were mostly absent. The restoration sites presented very low tree
seedling density (0.39 individuals/m2) relative to the mature forest (1.68 seedlings/m2), probably due to the
higher cover of climbers, ferns, grasses and shrubs found in the understory of the restoration sites (∼78%),
compared to that of the mature forest (8%). In all of the restoration sites, soil pH was higher, and carbon content
in both the soil and litter was lower, than in the mature forest. This denotes a slow recovery of soil properties
after use of the land as cattle pasture. In general, the passive restoration site non-adjacent to the forest presented
the lowest recovery (lower canopy cover, composition similarity and seedling density), indicating the im-
portance of proximity to seed sources. Our results highlight the need, in both actively and passively restored
areas, for management practices such as enrichment planting, in order to assist tree seedling recruitment of key
species and recovery of forest attributes. Active and passive restoration strategies could be implemented as
complementary strategies for the restoration of cloud forest landscapes.

1. Introduction
Restoration has become a necessary response to the extensive loss
and degradation of tropical forests (Lamb et al., 2005; Meli et al.,
2017). One ecosystem of global priority is Tropical Montane Cloud
Forest (TMCF), which provides important ecosystem services but is
severely threatened by deforestation and degradation (Scatena et al.,
2010). Every year ∼1.1% of the global TMCF coverage is lost (Scatena
et al., 2010), mainly through land use change for livestock production
and agriculture (Aide et al., 2010). As a consequence, it was calculated
that only 28% of the original coverage of TMCF in Mexico remained in
2002 (Challenger and Dirzo, 2009). Faced with this scenario, the design
of appropriate strategies for TMCF restoration is of vital importance.
In order to recover the structure and functionality of degraded,
damaged or destroyed ecosystems, two general strategies of ecological
restoration are recognized: (1) passive restoration, which eliminates the
factors of disturbance and permits natural regeneration, and (2) active
restoration, which eliminates the source of disturbance and implements
strategies to accelerate recovery and to overcome obstacles to that re-
covery (Holl and Aide, 2011). Rates of natural regeneration through

⁎
Corresponding author.
E-mail addresses: almalucrecia90@gmail.com (A.L. Trujillo-Miranda), tarin.toledo@inecol.mx (T. Toledo-Aceves), fabiola.lopez@inecol.mx (F. López-Barrera),
pgerez@uv.mx (P. Gerez-Fernández).

https://doi.org/10.1016/j.ecoleng.2018.03.011
Received 6 January 2018; Received in revised form 19 March 2018; Accepted 21 March 2018
0925-8574/ © 2018 Elsevier B.V. All rights reserved.
A.L. Trujillo-Miranda et al.
passive restoration are highly variable and the process can be un-
successful (Aide et al., 2010) since it depends on multiple factors, in-
cluding the intensity and type of the previous land management, type of
surrounding landscape and resilience of the ecosystem (Guariguata and
Ostertag, 2001; Montagnini, 2008; Aide et al., 2010; Norden et al.,
2015). In particular, the factors reported as limiting natural regenera-
tion of tropical montane forests following conversion to grazing pas-
tures are: fire (Grau et al., 2010), competition with pioneer species (e.g.
grasses and ferns; Ortega-Pieck et al., 2011), decoupling of interactions
(e.g. high levels of herbivory and lack of mycorrhizae; Aide et al.,
2010), unfavorable microhabitat (e.g. high solar radiation, low fertility,
compaction and erosion of the soil; Holl, 1999) and absence of seed
dispersers and low propagule arrival rates (Aide and Cavelier, 1994).
Lower vegetation recovery has been reported with increased distance to
mature forests (Holl, 1999; Muñiz-Castro et al., 2006).
One alternative for accelerating regeneration and overcoming the
obstacles described above is active restoration through mixed planta-
tions (Holl et al., 2000). Plantations help to more rapidly develop a
canopy, which can inhibit the herbaceous plant stratum and improve
microhabitat conditions for establishment of a greater diversity of
woody plants, including species of more advanced successional stages
(Butler et al., 2008; Zahawi et al., 2013). The trees established in these
plantations can also catalyze recovery by attracting disperser fauna,
functioning as perches and providing food and refuge (Orozco-Zamora
and Montagnini, 2007). Moreover, plantations act to improve the soil
conditions below, conferring higher nutrient and organic material
contents and protection from erosion (Ruiz-Jaén and Aide, 2005a;
Montagnini, 2008).
The active restoration strategy requires much higher investment in
terms of cost and time compared to natural regeneration or passive
restoration (Holl and Aide, 2011; Chazdon et al., 2017). In some cases,
depending on the plantation characteristics (e.g. the identity and
number of species planted and the plantation management adopted;
Thijs et al., 2014), the successional trajectory of the restored forest can
be altered, thus modifying the composition (Holl and Aide, 2011). In
contrast, passive restoration can achieve recovery of the functions and
composition of the community through the seed bank and seed rain
(Guariguata and Ostertag, 2001). However, wide variation exists in the
recovery rates of secondary tropical forest, which is attributed to
multiple local and landscape factors that generate alternative scenarios
and trajectories (Norden et al., 2015). In a recent metanalysis for tro-
pical forests, Crouzeilles et al. (2017) report that natural regeneration is
more successful than active restoration in terms of biodiversity and
vegetation structure recovery, when four important factors are con-
trolled: forest cover, the time elapsed since restoration started, past
disturbance type and annual precipitation. According to the global re-
view of Meli et al. (2017), only 11 studies (7%) of restoration success in
both tropical and temperate forests report data pertaining to active and
passive restoration strategies evaluated at the same site, thus sharing
environmental and management conditions. Moreover, there are few
studies that evaluate the success of these strategies in relation to a re-
ference ecosystem (Ruiz-Jaén and Aide, 2005a; Wortley et al., 2013).
Such comparison would allow determination of whether the areas
under restoration are within the trajectory of recovery of the ecosystem.
Opportunities to evaluate active and passive restoration in the same
system can arise through restoration initiatives carried out by land-
owners, which have been little documented (Holl et al., 2003). Such
initiatives have disadvantages, such as the lack of initial characteriza-
tion of the system, absence of detailed information regarding the
practice of active restoration and lack of balanced experimental design.
Nevertheless, they are strategies implemented at large scale and pro-
vide a valuable opportunity to evaluate the long-term efficiency of
applied restoration practices (Holl et al., 2003).
Indicators of the vegetation structure, diversity and ecological
processes are used to evaluate the success of forest restoration, since
these characteristics reflect the capacity of the restored ecosystems for
51
Ecological Engineering 117 (2018) 50–61
regeneration and self-maintenance (Ruiz-Jaén and Aide, 2005b).
Structural variables, including canopy cover, basal area, height and
density of trees, are positively related to the recovery of ecosystem
services such as carbon capture, erosion control and provision of ha-
bitat for the fauna (Ruiz-Jaén and Aide, 2005b; Suganuma and Durigan,
2015). Species diversity and composition are indicators of successional
stage, dispersion mechanisms and ecosystem resilience (Wortley et al.,
2013). Furthermore, the density of seedlings and juveniles can in-
directly reflect ecological processes such as seed production, dispersion
and propagule germination and establishment. Measurements of soil
conditions can provide information about the nutrient cycling processes
that underpin ecosystem productivity and stability (Herrick, 2000).
There is increasing recognition of the linkage between above and be-
lowground ecosystem components and the importance of their in-
tegration for restoration ecology (Kardol and Wardle, 2010; Roa-
Fuentes et al., 2013).
In this study, we evaluate recovery in an area in which a mixed
plantation with native species (active restoration) was established
21 years ago, and areas from which livestock was excluded only (pas-
sive restoration adjacent and non-adjacent to a mature forest), com-
paring these to a mature TMCF as a reference system. We address the
following specific question: has active restoration been more effective
than passive restoration in terms of recovery of tree structure, diversity
and composition and soil conditions? This study will provide a frame-
work to incentivize practitioners to assess and report restoration out-
comes and evaluate the ecological benefits and potential trade-offs of
two different restoration approaches. Specifically, this study will con-
tribute to the adoption of criteria for defining and assessing ecological
success during the TMCF restoration process.
2. Methods
2.1. Study area
The study was conducted on the private ranch “Las Cañadas”
(19°11′23″ N, 96°59′11″ W; 1300–1500 m. a.s.l.; Fig. 1), Veracruz,
Mexico. Mean annual temperature is 19.1 °C and mean annual pre-
cipitation is 2100 mm. The original vegetation of the study zone is
TMCF and the soil type is umbric andosol (Geissert and Ibáñez, 2008).
Las Cañadas has a total area of 306.7 ha, of which 270.3 ha were de-
forested in 1950 for livestock production (0.66 head of cattle/ha), while
conserving a fragment of the mature forest. The exotic grasses Bra-
chiaria sp. and Cynodon sp. were introduced into the grazing pastures.
After 45 years, the livestock was excluded from the grazing areas and
different interventions were made in 1995 (Fig. 1). In this study, we
evaluated the following conditions present in four distinct sites:
a) Reference forest (mature forest; MF): fragment of 30 ha of TMCF,
maintained from before the year 1950, surrounded by secondary
TMCF.
b) Active restoration (mixed plantation; MP): In 36.56 ha, 39,256 trees
of native TMCF species were planted: Fraxinus uhdei (Oleaceae;
10,000 individuals), Juglans pyriformis (Juglandaceae; 5000 in-
dividuals), Liquidambar styraciflua (Hamamelidaceae; 3256 in-
dividuals), Platanus mexicana (Platanaceae; 1000 individuals),
Quercus sapotifolia and Quercus spp. (Fagaceae; 20,000 individuals).
All of these trees were acquired from nearby nurseries and were
approximately 1 to 1.5 m in height on transplantation. Manual
clearing was conducted prior to and two years after transplantation
in order to reduce competition with grasses. No subsequent main-
tenance was carried out. All of the species were planted in combi-
nation and at a random frequency, apart from Platanus mexicana,
which was planted at the edges of the river since it naturally forms
part of the riparian vegetation (Benítez et al., 2004). This site was
located at a distance of 735.4 ± 82.2 m (mean ± S.E.) from the
MF.
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

Fig. 1. Location of the study area in Veracruz, Mexico (above) and IKONOS image (2007; below) indicating the study area and sampling plots per site according to
the established ordering plan of “Las Cañadas”: MF = mature tropical montane cloud forest (circles), MP = active restoration mixed plantation (squares),
PA = passive restoration adjacent to the forest (diamonds), PNA = passive restoration non-adjacent to the forest (triangles), and MU = multiple use. The main land
use types around the study site were determined based on a Google Earth image (2017). Map elaborated by R. Landgrave.

c) Passive restoration adjacent to forest (PA): In 14 ha, livestock was edge.

excluded. This site is found adjacent to the fragment of MF, and was
located at a distance of 146.8 ± 26.6 m from the MF.
d) Passive restoration non-adjacent to forest (PNA): In 61.49 ha, live-
stock was excluded. This site was located at a distance of
907.5 ± 66.5 m from the MF.
2.2. Sampling design
In order to evaluate tree structure, diversity and composition, a
minimum of 13 plots of 10 × 20 m (200 m2) were established in each of
the four sites between March and May 2016. To select the location of
the plots, each site was subdivided on a map into rectangles of 200 m2.
A number was assigned to each rectangle and these were then randomly
selected. The plots were a minimum of 50 m apart and 30 m from the
In each plot, we recorded the slope with a clinometer and elevation
with GPS, the canopy cover at the start, middle and end of the plot (0 m,
10 m and 20 m) with a convex densiometer and the height of the three
tallest trees using visual estimation (da Silva et al., 2012). The species
and diameter at breast height (DBH) of all of the adult trees
(DBH ≥ 10 cm) were recorded. Juvenile trees (> 1.5 m in height
and < 10 cm DBH) were recorded in two 5 × 5 m (25 m2) subplots,
established in opposite corners of each 200 m2 plot. This category in-
cluded young individuals of canopy trees as well as small trees. Tree
seedlings (≥0.3 m and ≤1.5 m in height) were recorded in one
2.5 × 2.5 m (6.25 m2) subplot, established within each of the 25 m2
subplots. In each subplot, understory cover was estimated for the most
common groups: climbers, grasses, Piper, Pteridium and Selaginella. The
following cover categories were recorded: (1) 0%, (2) 1–25%, (3)

52
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

Fig. 2. Vegetation structure (mean ± 1 S.E.) in mature tropical montane cloud forest and in sites of active restoration (mixed plantation) and passive restoration
adjacent and non-adjacent to mature tropical montane cloud forest in Veracruz, Mexico. Basal area: X2 = 103.02, d.f. = 3, P < 0.001; tree height: F = 17.39,
d.f. = 3, P < 0.001; DBH: F = 11.44, d.f. = 3, P < 0.001; canopy cover: F = 27.23, d.f. = 3, P < 0.001; adult tree density: X2 = 25.47, d.f. = 3, P < 0.001;
sapling density: X2 = 7.75, d.f. = 3, P = 0.051; seedling density: X2 = 47.75, d.f. = 3, P < 0.001; understory cover: X2 = 68.46, d.f. = 3, P < 0.001. Means that do
not share a letter denote significant differences among sites (P < 0.05) using contrasts.

26–50%, (4) 51–75%, and (5) 76–100%.
2.3. Soil analysis
To characterize the upper layer of soil at each site, six randomly
selected plots were sampled. Three soil samples were collected from
each plot and soil samples from two plots were combined into one
compound sample, producing a total of three compound soil samples
per site for laboratory analysis. Samples of litter and soil from depth
0–10 cm were collected in October 2016. These litter and soil samples
were stored at 4 °C for less than a week prior to laboratory analysis to
determine pH, soil density, total carbon (C), total nitrogen (N), total
phosphorus (P), and calcium (Ca) and magnesium (Mg) contents. Total
C and N values were determined with the Dumas method (CHN ana-
lyzer, model 2400, Perkin Elmer ®). Total P was determined with per-
chloric acid: nitric acid digestion (1:2), and P content was determined
by the vanadomolybdate method with a spectrophotometer (Spectronic
21d, Milton Roy ®). Exchangeable Ca and Mg were analyzed with the
ammonium acetate method (Chapman, 1965). Bulk soil pH was mea-
sured in H2O at a 1:2 ratio (ISO 10390, 1994).
2.4. Data analysis
A general linear mixed model was used to determine the effect of

53
A.L. Trujillo-Miranda et al.
site on tree height, DBH and canopy cover (fixed factor: site, random
factor: plot). Canopy cover was arcsine-transformed in order to meet
the model assumptions. A generalized linear model was used to de-
termine the effect of site on the basal area and density of adult trees
(trees m−2), with Gamma (link function Inverse) and quasi-Poisson
(link function Log) distributions, respectively. Given that only one
measure of basal area and tree density was obtained per plot, only the
effect of site was assessed. To determine the effect of site on the density
of seedlings and saplings, a generalized mixed model was used (fixed
factor: site, random factor: plot) with Poisson distribution (link function
Log). For all of these analyses, all species were grouped. To determine
differences among sites in terms of the understory cover of climbers,
grasses, Piper, Pteridium and Selaginella, the median value for each ca-
tegory was used. The values for the different groups of plants were
added to obtain a total understory cover value for each 25 m2 subplot.
This value was analyzed with a generalized linear model (fixed factor:
site, random factor: plot) with Binomial distribution (link function
Logit). An ANOVA was used to evaluate differences in soil properties
among the four sites (fixed factor: site). Contrasts were used to de-
termine differences among sites (Crawley, 2013). All analyses were
carried out in R (RStudio Team 2016, version 1.0.44).
Given that the completeness of the adult tree species sampling was
unequal among sites and that comparisons of diversity are only ecolo-
gically valid at the same completeness (Chao and Jost, 2012), the inter-
and extrapolation (100 randomizations) method was used to estimate
the diversities of order 0 (0D = richness) and order 1 (1D = exponential
of the Shannon entropy) in order to make comparisons among sites at
the same sample coverage (92%). In order to determine the differences
in 0D and 1D among sites, 95% confidence intervals were used (Chao
et al., 2014). Values were calculated with the program iNEXT (Hsieh
et al., 2016).
To analyze similarity in tree species composition among sites, a
metric multidimensional scaling (mMDS) analysis with Bray-Curtis si-
milarity and Bootstrap was used. Since the stress value was 0.13 for
adult trees, the graphs were represented using two dimensions, which
made the interpretation reliable. To assess differences in species com-
position among sites, a PERMANOVA was used (site as a factor) for
adult trees. Values of probability were adjusted with Bonferroni cor-
rections. This analysis was performed in the program PRIMER
(v.7.0.13; Anderson et al., 2008).
3. Results
3.1. Forest structure
All of the structural characteristics presented higher values in the
Mature Forest (MF) than in the three restoration sites (Fig. 2,
Appendices A and B). With respect to the MF, the basal area of the
Mixed Plantation (MP) represented 44.4%, while the Passive Adjacent
(PA) and Passive Non-Adjacent (PNA) presented 28.1% and 26.7%,
respectively. The site MP also had values of basal area and height that
were higher than those of the passive restoration sites, as well as dia-
meter and canopy cover values that were similar to the PA. Density of
adult trees was the only structural variable that was similar among the
three restoration sites (Fig. 2). The sites PA and PNA only differed in
terms of the values of canopy cover, in which PNA presented the lowest
value (P < 0.05).
Density of juveniles (pooling all species together) did not differ
among any of the four sites evaluated. Seedling density was greater in
MF than in all of the three restoration sites (Fig. 2; Appendices A and B).
In particular, PNA presented the lowest density of seedlings.
The distribution of diametric classes (considering all of the species)
presented a greater density of individuals in smaller size categories in
all of the restoration sites. This density decreased with increasing value
of the diametric classes (Appendix C). Trees in the diametric
classes > 60 cm DBH were only recorded in MF. For the genus Quercus
54
Ecological Engineering 117 (2018) 50–61
in MF and MP, distribution of the diametric classes was continuous,
with individuals in all classes (Appendix C); this contrasts with the
passive restoration sites, where the distribution was discontinuous and
most of the diametric classes were unrepresented.
The total cover of climbers, grasses, Piper, Pteridium and Selaginella
in the understory was six to seven times higher in the restoration sites
than in MF (Fig. 2). There were no differences in the total cover of the
plants evaluated in the understory between the MP and passive re-
storation sites (Fig. 2; Appendices A and B). However, group-dependent
differences in the coverage among sites were recorded; in MP the cover
of grasses and of Piper was greater, while the passive restoration sites
presented a high cover of Selaginella and climbers. It should be high-
lighted that PNA presented the highest cover of the invasive fern Pter-
idium arachnoideum.
3.2. Diversity and composition of tree species
In total, 50 species of adult trees were recorded (Appendix D). The
sample coverage was: MF = 95.7%, MP = 93.96%, PA = 88.03% and
PNA = 92.44%. The observed richness was greater in MF and PA (26 in
each case) than in MP (23) and PNA (21). However, the estimated
richness was greater in PA than in MF and the diversity of the former
was greater than in all of the other sites (Fig. 3). The MP and PNA sites
presented estimated richness and diversity values that were similar to
those of the MF.
Species composition differed among sites (Pseudo-F = 10.14,
P ≤ 0.001; Fig. 4). The restoration sites differed from MF (Appendix E).
The MP presented a species composition that differed from the two
passive restoration sites, which did not differ from each other. The PNA
presented the least similarity of species with MF.
According to the Importance Value Index (IVI; Mueller-Dombois and
Ellenberg, 1974) in MF, the species of the genus Quercus presented the
highest values, followed by Beilschmiedia mexicana (Appendix D). In the
MP, L. styraciflua presented the greatest dominance. In general, across
the restoration sites, the pioneer species Myrsine coriacea and Trema
micrantha dominated the canopy. Most of the species presented IVI
Fig. 3. (A) Species richness and (B) Exponential of Shannon’s entropy index for
adult trees (≥10 cm DBH) estimates for a rarefaction and sample extrapolated
to 92% of sample coverage in mature tropical montane cloud forest, active
restoration mixed plantation, passive restoration adjacent and passive restora-
tion non-adjacent to mature tropical montane cloud forest in Veracruz, Mexico.
Differences occur where 95% confidence intervals do not overlap.
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

Fig. 4. Metric multidimensional scaling based on Bray Curtis similarity
(stress = 0.13) for adult tree (≥10 cm DBH) composition in mature tropical
montane cloud forest (circles), mixed plantation (active restoration: squares),
passive restoration adjacent (diamonds) and passive restoration non-adjacent
(triangles) to the mature tropical montane cloud forest in Veracruz, Mexico.
Shading denotes reliability averages estimated by Bootstrap and the black
symbols represent the centroids of the clouds.
values below 5% at all sites.
3.3. Soil properties
Soil analysis showed important differences between the MF and
restoration sites; with lower values in MF for pH, Ca, Mg and higher
total C (Table 1; Appendix F). The C and N concentrations in the litter
followed the same pattern, with higher values in the MF. In general, the
restoration sites did not differ among themselves in terms of the soil
variables analyzed. Soil and litter P presented variation but the mean
values were similar among sites.
4. Discussion
4.1. Structure
After 21 years, the passive restoration sites (PA and PNA) in this
study had developed a basal area that was ∼27% of that in the MF.
Other studies report that, following abandonment of grazing pastures,
basal area can take approximately 80 years to recover values similar to
those of mature forest (Hölscher et al., 2010; Muñiz-Castro et al., 2012).
The results of this study demonstrate that plantation of native trees in
former pastures can be effective in terms of accelerating the recovery of
TMCF structure (reaching 44% of the basal area of the MF). The
structure values suggest that the species utilized are suitable for re-
storation of TMCF in grazing pastures; approximately 41% of the adults
recorded in this site were represented by the species planted.
All of the restoration sites presented ∼65% of the density of adult
trees found in the reference forest. Other studies report greater, lesser
and equal tree densities in secondary forests compared to those of
mature forests (Aide and Cavelier, 1994; Hölscher et al., 2010). The
lower density of trees in this study could reflect the fact that, in grazing
pastures that have been active for ∼45 years, the seed bank has largely
been eliminated, along with the resprouts and seedlings of trees (Aide
and Cavelier, 1994; López-Toledo and Martínez-Ramos, 2011, but see
Sampaio et al., 2007). Moreover, the presence of sown grasses, such as
Cynodon plectostachyus, could impede recruitment from the seed bank
(Williams-Linera et al., 2016) and/or from the seed rain. Thus, the low
density of adult trees in the restoration sites could be the result of low
recruitment.
The three restoration sites presented low seedling densities com-
pared to the MF and to other TMCF with different degrees of dis-
turbance (Álvarez-Aquino et al., 2005; Ortiz-Colín et al., 2017). There is
wide variation in the regeneration of woody vegetation in tropical
forests, both in plantations and through natural regeneration (Butler
et al., 2008; Hölscher et al., 2010; Thijs et al., 2014). This is due to
multiple factors at microsite, habitat and landscape levels, which may
also present temporal variation (Norden et al., 2015). The main factors
that could explain the low density of seedlings found in the restoration
sites are: (1) low production of seeds, since the reduced density of
adults may limit propagule production; (2) low abundance of seed
dispersers (Aide and Cavelier, 1994); (3) high cover of climbers,
grasses, Piper, Pteridium and Selaginella that could limit seedling emer-
gence and establishment through competition for space, light and nu-
trients (Guariguata et al., 1997; Toledo-Aceves and Swaine, 2008;
Ortega-Pieck et al., 2011); (4) decoupling between seed production and
the microhabitat conditions. Given that canopy cover increases over the
course of succession, it is possible that the light conditions are un-
suitable for establishment of heliophyte species. While it has been re-
ported that obstacles to the dispersion of seeds in restored areas of
tropical forests change over time (Reid et al., 2015), the results indicate
that intervention (e.g. direct seeding, enrichment plantations, removal
of herbaceous vegetation, nucleation) is required in order to assist re-
generation.
Canopy cover is an important indicator of restoration success, given
that it presents a direct relationship with the recovery of biomass, as
well as exerting an influence in terms of generating microclimatic
conditions favorable to the establishment of species of advanced suc-
cessional stages and providing refuge for disperser fauna (Suganuma

Table 1
Soil and litter properties (mean ± 1 S.E.) in mature tropical montane cloud forest, mixed plantation (active restoration), passive restoration adjacent and passive
restoration non-adjacent to mature tropical montane cloud forest in Veracruz, Mexico. Means that do not share a letter differ significantly among sites (P < 0.05)
using contrasts (N = 3 for all variables, except bulk density N = 6).
Variable Mature forest Mixed plantation Passive adjacent Passive non-adjacent F P

Soil
pH 4.15a ± 0.10 5.22b ± 0.11 5.69b ± 0.17 5.50b ± 0.22 18.67 0.001
Bulk density (g cm−3) 0.40 ± 0.03 0.47 ± 0.04 0.53 ± 0.05 0.59 ± 0.06 2.89 0.103
C (%) 14.15a ± 0.78 10.80ab ± 0.95 10.46ab ± 2.12 7.51b ± 0.05 4.91 0.032
N (%) 1.02 ± 0.07 0.85 ± 0.06 0.96 ± 0.18 0.67 ± 0.02 2.12 0.176
P (%) 0.08 ± 0.00 0.07 ± 0.00 0.08 ± 0.00 0.08 ± 0.00 1.52 0.282
C/N 13.93 ± 0.78 12.84 ± 1.41 10.83 ± 0.35 11.18 ± 0.46 2.87 0.104
Ca (cmol kg−1) 1.46a ± 0.83 6.81ab ± 2.04 9.48b ± 1.87 8.58b ± 1.63 4.69 0.036
Mg (cmol kg−1) 0.69a ± 0.18 2.10b ± 0.68 4.01c ± 0.22 2.73b ± 0.24 12.32 0.002

Litter
C (%) 36.83a ± 2.54 23.74b ± 2.61 23.83b ± 3.10 17.89b ± 2.05 9.47 0.005
N (%) 2.37a ± 0.03 1.51bc ± 0.04 1.81b ± 0.16 1.32c ± 0.19 12.02 0.002
P (%) 0.06 ± 0.00 0.08 ± 0.01 0.08 ± 0.00 0.08 ± 0.00 0.96 0.456
C/N 15.56 ± 1.22 15.70 ± 1.69 13.06 ± 0.61 13.71 ± 0.67 1.35 0.325

55
A.L. Trujillo-Miranda et al.
and Durigan, 2015). The greater understory cover in all of the re-
storation sites, relative to the MF, supports that found in previous
studies (Aide and Cavelier, 1994; Holl, 1999). While we have no
knowledge of the microenvironmental heterogeneity prior to initiation
of restoration, the MP appears to have contributed to reducing the
coverage of the plants in the understory, as has been previously re-
ported (Ruiz-Jaén and Aide, 2005a; Zahawi et al., 2013), because the
shade generated by the canopy acts to inhibit the herbaceous cover
(Marrs and Watt, 2006). The lower canopy cover and seedling density
values in the PNA suggest that distance to the forest and other land-
scape factors (e.g. the presence of other propagule sources) may act in a
synergistic manner with factors that operate at a more localized level
(e.g. competition with vegetation in the understory).
4.2. Diversity and composition
The relatively rapid recovery of tree richness and diversity found
after 21 years in both active and passive restoration sites concurs with
the findings of Muñiz-Castro et al. (2012) in abandoned grazing pas-
tures in TMCF. In contrast, other studies in secondary tropical humid
forest report that tree richness did not reach values comparable to those
of mature forests after 20 years in Colombia and Venezuela (Saldarriaga
et al., 1988) and after 16–18 years in Costa Rica (Guariguata et al.,
1997). The paucity of available information regarding the intensity of
the previous use of the landscape matrix in other studies makes com-
parison difficult, but it is probable that the recovery of the richness is
due to the proximity of propagule sources (Guariguata and Ostertag,
2001). The greater richness and diversity estimated in the PA, com-
pared to that of the MF itself, may be due to the confluence of primary
and secondary species (Guariguata and Ostertag, 2001; Muñiz-Castro
et al., 2006). The greater availability of light at the beginning of suc-
cession favors colonization by pioneer species, and the proximity to the
MF could favor the arrival of seeds of species with intermediate or full
shade tolerance.
While all of the sites presented similar values in terms of the rich-
ness and diversity of species, there were important differences in
composition. It should be noted that the TMCF presents a high turnover
in the ensemble of tree species among fragments (Williams-Linera et al.,
2013). The MF was an isolated fragment when restoration interventions
began in 1995; nevertheless, the composition found is very similar to
that reported for other mature TMCF in the region (Williams-Linera
et al., 2013). Among the most dominant species found in the MF, Q.
lancifolia, Zanthoxylum melanostictum and Styrax glabrescens have been
reported as representative of mature TMCF in the region (Muñiz-Castro
et al., 2012). Species such as Beilschmiedia mexicana, Persea longipes, S.
glabrescens and Tapiriria mexicana, characteristic of TMCF (Rzedowski,
1996; González-Espinosa et al., 2011), have not appeared in the sec-
ondary forests and thus require specific interventions in order to assist
restoration of their populations. In contrast, all of the restoration sites
are dominated by the pioneer species Trema micrantha and Myrsine
coriacea. This pattern matches that reported by other studies in which
heliophyte species dominate during the first years of succession (Muñiz-
Castro et al., 2012). One of the causes of low similarity in species
composition of adult trees between the MP and the MF is that, of the
five species planted, Q. sapotifolia, Platanus mexicana, Juglans pyriformis
and Fraxinus uhdei were not recorded in the reference ecosystem. It is
likely that more time is required in order to determine the influence of
the MP on the recovery of the floristic composition.
Our results support the notion that distance to the edge of the forest
plays an important role in recovery of the composition. In general, seed
dispersion of species that are characteristic of mature forests decreases
with distance (Aide and Cavelier, 1994; Holl, 1999; Muñiz-Castro et al.,
2006). In the PNA site, the low similarity to the MF in terms of species
composition could be due to the fact that the established species come
from propagule sources other than those of the MF, such as shade trees
in coffee plantations, live fences or remnant trees present in the
56
Ecological Engineering 117 (2018) 50–61
landscape.
4.3. Soil properties
The succession could have also been limited by soil compaction and
nutrient loss due to the former use of land for cattle grazing (Aide et al.,
2010). While soil bulk density did not differ among sites, soil and litter
properties analyzed presented low recovery in all of the restoration
sites. In general, TMCF has been characterized by low nutrient-cycle
rates and extreme soil acidity (Bruijnzeel and Veneklaas, 1998;
Bautista-Cruz et al., 2012). A link between high soil and litter C and soil
acidity has been previously described, and suggests the presence of
recalcitrant components in the organic matter that act to slow decom-
position rates (Bautista-Cruz et al., 2012). High soil C in the forest also
reflects the accumulation of above and belowground organic matter
(Dixon et al., 1994). In contrast, the lowest soil and litter C values found
in the PNA could reflect the fact that the lowest basal area was found in
that site. The higher values of the soil C:N ratio in the MF, in com-
parison to the restoration sites, reflect lower N availability, which may
be due to longer leaf life-spans in the tree community (Bruijnzeel and
Veneklaas, 1998). Changes occur in plant strategies for acquisition and
use of resources along succession; in TMCF, soil conditions can become
more stressful for plants as succession progresses and a strong tolerance
to low soil nutrient availability is observed (Bruijnzeel and Veneklaas,
1998; Negrete-Yankelevich et al., 2007; Bautista-Cruz et al., 2012).
Tree plantations have been reported to improve soil conditions by
increasing organic matter input, reducing erosion and increasing soil
nutrients (Ruiz-Jaén and Aide, 2005a; Montagnini, 2008). However,
other studies have found reduced soil C in tree plantations occupying
former pastures with rainfall > 1500 mm per year (Rhoades et al.,
2000) and, in a meta-analysis, Guo and Gifford (2002) report that
broadleaf tree plantations in pastures did not affect soil C stocks. We
identified a tendency for the MP to present values closer to the MF,
while passive restoration sites displayed greater dissimilarities; how-
ever, no significant differences were found among the restoration sites
in general. This lack of significance was probably due to high variation
associated with the reduced number of samples and the high spatial
heterogeneity of the soil, which has been found to increase, temporally
and spatially, as a result of land-use change (Roa-Fuentes et al., 2013).
4.4. Implications for practice
Different TMCF restoration strategies can be integrated in a com-
plementary manner considering the high environmental and biotic
heterogeneity characteristic of this system (Williams-Linera et al.,
2013), as well as the restoration objectives, landscape matrix, micro-
habitat conditions and socioeconomic factors (Holl and Aide, 2011;
Ramírez-Soto et al., 2018). It can be inferred from our results that, in
zones more distant from the propagule sources, planting of native
species can be effective in terms of accelerating the recovery of the
structure and some species of TMCF. Furthermore, the active restora-
tion strategy can contribute to the recovery of functions such as carbon
capture, regulation of hydrological and nutrient cycles and the provi-
sion of food and refuge to the fauna. A less expensive approach to ex-
tensive plantations is to plant nuclei (islands) of trees (Ramírez-Soto
et al., 2018), this approach could be more effective in terms of in-
creasing recruitment at former pastures sites in Costa Rica compared to
passive restoration, at least during the first years after planting (Zahawi
et al., 2013). In zones adjacent to mature forests, recovery of some
structural and compositional characteristics can be achieved with the
simple exclusion of disturbance. While some characteristics demon-
strate greater recovery during the initial years (e.g. canopy cover), our
results indicate that recovery of soil fertility and processes such as tree
regeneration may require more time or could be limited, which could
affect the long-term self-maintenance of the ecosystem.
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

5. Conclusions Declarations of interest

Evaluation of restoration strategies implemented simultaneously in None.

the same system, with similar environmental and historical conditions,
shows that the establishment of mixed plantations (active restoration)
in grazing pastures with exclosure accelerated the recovery of the TMCF
vegetation structure relative to that of natural regeneration (passive
restoration). While both active and passive restoration matched the
values of richness and diversity of the reference mature forest, even
after 21 years, species composition remained very different. Low seed-
ling density was found in all of the restoration sites, for which reason
intervention is required in order to assist regeneration, particularly in
species that are rare and of more advanced successional stages. Passive
and active restoration can be implemented in the landscape in a com-
plementary manner, implying different costs and benefits. In the zones
furthest from sources of propagules and/or dominated by invasive
species, planting native species of different functional groups can be an
effective strategy for accelerating the recovery of the structure and of
certain species of the TMCF, while in the zones adjacent to mature
forests, recovery of some structural characteristics can take place with
the simple exclusion of disturbance. Under both strategies, long-term
monitoring is fundamental to providing a basis for subsequent inter-
ventions to assist the recovery of the processes and functions of the
system.
Acknowledgments
This work was funded by CONACYT (CB2014-01/238831), which
also provided an MSc scholarship to A. L. Trujillo-Miranda (No.
416522). Our thanks go to Ricardo Romero and the cooperative Las
Cañadas, for granting us permission and facilities to work on their
property. We thank INECOL A.C. for the use of their facilities. This work
would not have been possible without the assistance during fieldwork
of V. Tepatlán, R. López, M. Peralta, V. Vásquez, C. Gallardo and L.
Ríos. We are very grateful to C. Gallardo who identified the majority of
the tree species, and to F. Lorea, S. Valencia, M. Cházaro, J. Gutiérrez,
L. Rosales, E. Tinoco, J. Rojas, R. de Santiago, R. Cruz for species
identification. We thank S. Rocha for the soil analyses. We thank R.
Guevara and V. Sosa for their advice with statistical analysis and R.
Landgrave for producing maps for sites in which to collect field data. M.
Bonilla and R. Zahawi provided useful critique on the MSc thesis on
which this manuscript is based. We thank the two anonymous reviewers
for their helpful suggestions. K. Macmillan revised the English text.

Appendix A

Characteristics and vegetation structure (mean ± 1 S.E.) in sites of mature tropical montane cloud forest, active restoration (mixed plantation),
passive restoration adjacent and passive restoration non-adjacent to the mature forest in Veracruz, Mexico. Means with the same letter do not differ
significantly among sites (P > 0.05), using contrasts. Density of adult trees (≥10 cm DBH), saplings (> 1.5 m in height and < 10 cm DBH) and
seedlings (≥0.3 to 1.5 m in height) were analyzed in plots of 200 m2, 25 m2, 6.25 m2, respectively.

Variable Mature forest Mixed plantation Passive adjacent Passive non-adjacent

No. of plots 17 16 13 15
Slope (°) 55 ± 5.73 39.56 ± 5.30 43.23 ± 7.25 51.07 ± 3.86
Elevation (m. a.s.l.) 1425.6 ± 7.49 1348 ± 4.38 1396 ± 6.67 1363.3 ± 6.53
Adult tree density (tree ha−1) 614.7a ± 50.3 462.5b ± 31.8 350b ± 48.7 350b ± 38.1
Basal area (m2 ha−1) 44.27a ± 4.73 19.70b ± 2.10 12.44c ± 1.47 11.83c ± 1.30
Height (m) 24.52a ± 1.15 18.97b ± 1.18 14.10c ± 1.32 13.95c ± 1.22
DBH (cm) 24.65a ± 1.21 20.23b ± 0.89 17.96bc ± 0.79 17.02c ± 0.64
Canopy cover (%) 77.97a ± 1.28 70.91b ± 1.56 67.70b ± 1.86 57.40c ± 1.90
Sapling density (sapling m−2) 0.59 ± 0.04 0.38 ± 0.04 0.44 ± 0.05 0.43 ± 0.05
Seedling density (seedling m−2) 1.68a ± 0.15 0.60b ± 0.10 0.80b ± 0.10 0.30c ± 0.06
Understory cover (%) 8a ± 2.24 76.42b ± 4.34 75.15b ± 5.01 84.17b ± 4.22
Climbers (%) 0 0 7.96 ± 3.81 4.37 ± 1.24
Grasses (%) 0.36 ± 0.36 35.89 ± 3.78 19.33 ± 4.69 30.50 ± 2.59
Piper (%) 2.20 ± 0.83 17.39 ± 3.42 10.27 ± 4.25 6.48 ± 2.41
Pteridium (%) 0 1.15 ± 0.64 3.88 ± 2.19 13.77 ± 3.88
Selaginella (%) 5.56 ± 1.94 22.23 ± 3.53 33.83 ± 5.37 29.20 ± 4.15

Appendix B

Contrasts with which to assess differences in vegetation structure in sites of mature tropical montane cloud forest (MF), active restoration (mixed
plantation; MP), passive restoration adjacent (PA) and passive restoration non-adjacent (PNA) to mature forest in Veracruz, Mexico. Adult trees
≥10 cm DBH, and seedlings ≥0.3 to 1.5 m in height. Canopy cover was arcsine-transformed in order to comply with model assumptions.

MF – MP MF – PA MF – PNA MP – PA MP – PNA PA – PNA

Variable t P t P t P t P t P t P

Adult tree density 2.36 0.021 4.005 < 0.001 4.205 < 0.001 1.868 0.066 1.95 0.056 1.02E−09 1
Basal area 4.798 < 0.001 5.944 < 0.001 6.501 < 0.001 2.729 0.008 3.165 0.002 0.318 0.751
Height 3.356 < 0.001 5.941 < 0.001 6.287 < 0.001 2.74 0.009 2.944 0.005 0.084 0.932

57
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

DBH 2.936 0.005 4.604 < 0.001 5.537 < 0.001 1.895 0.065 2.902 0.005 0.907 0.369
Z P Z P Z P Z P Z P Z P

Canopy cover 3.5 < 0.001 4.646 < 0.001 8.948 < 0.001 1.32 0.459 5.46 < 0.001 3.881 < 0.001
Seedling density 5.42 < 0.001 3.65 < 0.001 7.81 < 0.001 1.52 0.34 2.86 0.01 4.17 < 0.001
Understory cover 8.508 < 0.001 7.762 < 0.001 9.642 < 0.001 0.291 0.987 1.491 0.365 1.698 0.258

Appendix C

Diameter distributions in adult trees (≥10 cm DBH) of (A) all species and (B) Quercus species in sites of mature tropical montane cloud forest,
mixed plantation (active restoration), passive restoration adjacent and passive restoration non-adjacent to mature tropical montane cloud forest in
Veracruz, Mexico.

Appendix D

Importance value index (%) of adult tree species (≥10 cm DBH) in sites of mature tropical montane cloud forest, active restoration (mixed
plantation), passive restoration adjacent and passive restoration non-adjacent to mature tropical montane cloud forest in Veracruz, Mexico.

Species Mature forest Mixed plantation Passive adjacent Passive non-adjacent

Acacia angustissima 1.00 3.79

Acacia pennatula 2.25 1.01
Alchornea latifolia 4.44 4.52
Annona cherimola 2.56
Beilschmiedia mexicana 7.54 1.44
Brunellia mexicana 2.13 3.78 7.25
Bunchosia sp1 2.36 2.68
Cestrum tomentosum 2.21
Cinnamomum effusum 2.13 1.51 0.93
Citharexylum sp1 5.63
Clethra alcoceri 0.76
Clethra sp1 3.46 3.72 9.93 8.78
Cojoba arborea 3.37

58
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

Eugenia mexicana 3.40

Frangula capreifolia 1.48 4.64 2.92
Fraxinus uhdei 2.48
Hampea integerrima 0.71 1.76
Hedyosmum mexicanum 1.11 0.98
Heliocarpus appendiculatus 0.61
Ilex sp1 3.86
Ilex tolucana 0.60
Juglans pyriformis 8.00
Lippia myriocephala 1.56 1.45 0.98
Liquidambar styraciflua 0.57 18.98 1.79 3.09
Lonchocarpus aff. hydrophilus 1.01
Lonchocarpus sp1 0.93
Meliosma alba 0.76 1.37
Myrsine coriacea 14.93 17.37 24.11
Ocotea psychotrioides 0.94
Persea longipes 0.52
Platanus mexicana 2.04
Quercus aff. xalapensis 0.77
Quercus insignis 9.42 0.86 3.14
Quercus lancifolia 11.34 5.76
Quercus paxtalensis 30.53 1.44
Quercus sapotifolia 11.04 9.78
Saurauia pedunculata 2.45 6.11
Sideroxylon aff. contrerasii 0.57
Siparuna sp1 0.72
Solanum nigricans 1.47 6.27 0.99
Styrax glabrescens 3.76
Symplocos limoncillo 1.06 1.11
Tapirira mexicana 0.56
Telantophora grandifolia 0.50 1.26
Toxicodendron striatum 0.55 4.10 2.66
Trema micrantha 0.72 15.61 14.09 11.96
Turpinia insignis 2.02 0.73
Vernonanthura patens 4.87
Vismia baccifera 1.42 0.73 1.08 2.03
Zanthoxylum melanostictum 3.98 1.70 3.48 3.23

Appendix E

Paired test to evaluate differences in adult tree (≥10 cm DBH) species composition among sites of mature tropical montane cloud forest, mixed
plantation (active restoration), passive restoration adjacent and passive restoration non-adjacent to mature tropical montane cloud forest in
Veracruz, Mexico. P values are Bonferroni adjusted.

Sites t P

Mature Forest-Mixed plantation 4.31 < 0.001

Mature Forest-Passive adjacent 3.39 < 0. 001
Mature Forest-Passive non-adjacent 4.35 < 0. 001
Mixed plantation-Passive adjacent 2.23 < 0. 001
Mixed plantation-Passive non-adjacent 2.40 < 0. 001
Passive adjacent – Passive non-adjacent 1.33 0.38

59
A.L. Trujillo-Miranda et al. Ecological Engineering 117 (2018) 50–61

Appendix F

Contrasts to determine differences in soil properties in sites of mature tropical montane cloud forest (MF), mixed plantation (MP), passive
restoration adjacent (PA) and passive restoration non-adjacent (PNA) to mature tropical montane cloud forest in Veracruz, Mexico.

MF – MP MF – PA MF – PNA MP – PA MP – PNA PA – PNA

Variable t P t P t P t P t P t P

Soil
pH 4.765 0.001 6.845 0.001 5.990 0.000 2.080 0.071 1.224 0.255 0.855 0.417
Ca 2.281 0.051 3.41 0.009 3.03 0.016 1.13 0.288 0.756 0.471 0.380 0.713
Mg 2.544 0.034 5.974 0.000 3.66 0.006 3.429 0.008 1.119 0.295 2.310 0.049
C 1.931 0.089 2.125 0.066 3.828 0.005 0.194 0.850 1.896 0.094 1.702 0.127
Litter
C 3.55 0.007 3.535 0.007 5.149 0.000 0.023 0.981 1.591 0.150 1.614 0.145
N 5.587 0.001 2.999 0.017 5.623 0.000 1.588 0.150 1.035 0.330 2.623 0.030

References
Aide, T.M., Cavelier, J., 1994. Barriers to lowland tropical forest restoration in the Sierra
Nevada de Santa Marta, Colombia. Restoration Ecol. 2, 219–229.
Aide, T.M., Ruiz-Jaén, M.C., Grau, H.R., 2010. What is the state of tropical montane cloud
forest restoration? In: Bruijnzeel, L.A., Scatena, F.N., Hamilton, L.S. (Eds.), Tropical
Montane Cloud Forests Science for Conservation and Management. Cambridge
University Press, Cambridge, UK, pp. 101–110.
Álvarez-Aquino, C., Williams-Linera, G., Newton, A.C., 2005. Disturbance effects on the
seed bank of Mexican cloud forest fragments. Biotropica 37, 337–342.
Anderson, M.J., Gorley, A.M.J., Clarke, K.R., 2008. PERMANOVA + for PRIMER: Guide
to software and statistical methods. PRIMER-E: Plymouth, UK. 214 p.
Bautista-Cruz, A., del Castillo, R.F., Etchevers-Barra, J.D., Gutiérrez-Castorena, M. del C.,
Báez, A., 2012. Selection and interpretation of soil quality indicators for forest re-
covery after clearing of a tropical montane cloud forest in Mexico. For. Ecol. Manage.
277, 74–80.
Benítez, G., Pulido-Salas, M.T.P., Equihua, M., 2004. Árboles multiusos nativos de
Veracruz para reforestación, restauración y plantaciones. Instituto de Ecología, A.C,
SIGOLFO, CONAFOR, Veracruz, Mexico. 288 p.
Bruijnzeel, L.A., Veneklaas, E.J., 1998. Climatic conditions and tropical montane forest
productivity: the fog has not lifted. Ecology 79, 3–9.
Butler, R., Montagnini, F., Arroyo, P., 2008. Woody understory plant diversity in pure and
mixed native tree plantations at La Selva Biological Station, Costa Rica. For. Ecol.
Manage. 255, 2251–2263.
Challenger, A., Dirzo, R., 2009. Factores de cambio y estado de la biodiversidad. En:
Capital natural de México vol. II: Estado de conservación y tendencias de cambio.
Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Mexico, pp.
37–73.
Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K., Ellison, A.M.,
2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling
and estimation in species diversity studies. Ecol. Monogr. 84, 45–67.
Chao, A., Jost, L., 2012. Coverage-based rarefaction and extrapolation: standardizing
samples by completeness rather than size. Ecology 93, 2533–2547.
Chapman, H.D., 1965. Cation exchange capacity. In: Black, C.A. (Ed.), Methods of
Analysis. Part 2. Agronomy 9. American Society of Agronomy, Madison, Wisconsin,
pp. 891–901.
Chazdon, R.L., Bodin, B., Guariguata, M., Lamb, D., Walder, B., Chokkalingam, U., Shono,
K. 2017. Partnering with nature: The case for natural regeneration in forest and
landscape restoration. FERI Policy Brief. Montreal, Canada.
Crawley, M.J., 2013. The R Book. second ed., John Wiley and Sons Ltd, pp. 1076.
Crouzeilles, R., Ferreira, M.S., Chazdon, R.L., Lindenmayer, D.B., Sansevero, J.B.B.,
Monteiro, L., Iribarrem, A., Latawiec, A.E., Strassburg, B.B.N., 2017. Ecological re-
storation success is higher for natural regeneration than for active restoration in
tropical forests. Sci. Adv. 3, E1701345.
da Silva, G.F., Curto, R.D.A., Soares, C.P.B., Piassi, L.C., 2012. Evaluation of height
measurement methods in natural forests. Revista Arvore 36, 341–348.
Dixon, R.K., Brown, S., Houghton, R.E.A., Solomon, A.M., Trexler, M.C., Wisniewski, J.,
1994. Carbon pools and flux of global forest ecosystems. Science 263 (5144),
185–189.
Geissert, D., Ibáñez, A., 2008. Calidad y ambiente físico-químico de los suelos. In:
Manson, R.H., Hernández-Ortiz, V., Gallina, S., Mehltreter, K. (Eds.), Agroecosistemas
Cafetaleros de Veracruz Biodiversidad, Manejo y Conservación. Instituto de Ecología
A. C., Instituto Nacional de Ecología (INE-SEMARNAT), pp. 213–222.
González-Espinosa, M., Meave, J., Lorea-Hernández, F.G., Ibarra-Manríquez, G., Newton,
A.C. (Eds.), 2011. The Red List of Mexican Cloud Forest Trees. Fauna and Flora
International, Cambridge, UK, pp. 148.
Grau, H.R., Carilla, J., Gil-Montero, R., Villalba, R., Araoz, E., Masse, G., de Membiela, M.,
2010. Environmental history and forest regeneration dynamics in a degraded valley
of north-west Argentina’s cloud forests. In: Bruijnzeel, L.A., Scatena, F.N., Hamilton,
L.S. (Eds.), Tropical Montane Cloud Forests Science for Conservation and
Management. Cambridge University Press, Cambridge, UK, pp. 597–604.
Guariguata, M.R., Chazdon, R.L., Denslow, J.S., Dupuy, J.M., Anderson, L., 1997.
Structure and floristics of secondary and old-growth forest stands in lowland Costa
Rica. Plant Ecology 132, 107–120.
Guariguata, M.R., Ostertag, R., 2001. Neotropical secondary forest succession: changes in
structural and functional characteristics. For. Ecol. Manage. 148, 185–206.
Guo, L.B., Gifford, R.M., 2002. Soil carbon stocks and land use change: a meta-analysis.
Global Change Biol. 8, 345–360.
Herrick, J.E., 2000. Soil quality: an indicator of sustainable land management? Appl. Soil
Ecol. 15, 75–83.
Holl, K.D., 1999. Factors limiting tropical rain forest regeneration in abandoned pasture:
seed rain, seed germination, microclimate, and soil. Biotropica 31, 229–242.
Holl, K.D., Aide, T.M., 2011. When and where to actively restore ecosystems? For. Ecol.
Manage. 261, 1558–1563.
Holl, K.D., Loik, M.E., Lin, E.H.V., Samuel, I.A., 2000. Tropical montane forest restoration
in Costa Rica: overcoming barriers to dispersal and establishment. Restoration Ecol.
8, 339–349.
Holl, K.D., Crone, E.E., Schultz, C.B., 2003. Landscape restoration: moving from gen-
eralities to methodologies. BioScience 53, 491–502.
Hölscher, D., Köhler, L., Kappelle, M., Leuschner, Ch., 2010. Ecology and use of old-
growth and recovering montane oak forests in the Cordillera de Talamanca, Costa
Rica. In: Bruijnzeel, L.A., Scatena, F.N., Hamilton, L.S. (Eds.), Tropical Montane
Cloud Forests Science for Conservation and Management. Cambridge University
Press, Cambridge, UK, pp. 610–617.
Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: an R package for interpolation and extra-
polation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456.
ISO 10390, 1994. Soil quality—determination of pH.
Kardol, P., Wardle, D.A., 2010. How understanding aboveground–belowground linkages
can assist restoration ecology. Trends Ecol. Evol. 25 (11), 670–679.
Lamb, D., Erskine, P.D., Parrotta, J.A., 2005. Restoration of degraded tropical forest
landscapes. Science 310, 1628–1632.
López-Toledo, L., Martínez-Ramos, M., 2011. The soil seed bank in abandoned tropical
pastures: source of regeneration or invasion? Revista Mexicana de Biodiversidad 82,
663–678.
Marrs, R.H., Watt, A.S., 2006. Biological flora of the British Isles: Pteridium aquilinum (L.)
Kuhn. J. Ecol. 94, 1272–1321.
Meli, P., Holl, K.D., Rey-Benayas, J.M., Jones, H.P., Jones, P.C., Montoya, D., Mateos,
D.M., 2017. A global review of past land use, climate, and active vs. passive re-
storation effects on forest recovery. PLoS ONE 12, 1–17.
Montagnini, F., 2008. Management for sustainability and restoration of degraded pastures
in the Neotropics. In: Myster, R.W. (Ed.), Post-Agricultural Succession in the
Neotropics. Springer, New York, USA, pp. 265–295.
Mueller-Dombois, D., Ellenberg, H., 1974. Aims and Methods of Vegetation Ecology.
Wiley, New York 547 p.
Muñiz-Castro, M.A., Williams-Linera, G., Benayas, J.M., 2006. Distance effect from cloud
forest fragments on plant community structure in abandoned pastures in Veracruz,
Mexico. J. Tropical Ecol. 22, 431–440.

60
A.L. Trujillo-Miranda et al.
Muñiz-Castro, M.A., Williams-Linera, G., Martínez-Ramos, M., 2012. Dispersal mode,
shade tolerance, and phytogeographical affinity of tree species during secondary
succession in tropical montane cloud forest. Plant Ecol. 213, 339–353.
Negrete-Yankelevich, S., Fragoso, C., Newton, A.C., Heal, O.W., 2007. Successional
changes in soil, litter and macroinvertebrate parameters following selective logging
in a Mexican Cloud Forest. Appl. Soil Ecol. 35, 340–355.
Norden, N., Angarita, H.A., Bongers, F., Martínez-Ramos, M., Granzow-de la Cerda, I.,
Van Breugel, M., Lebrija-Trejos, E., Meave, J.A., Vandermeer, J., Williamson, G.B.,
Finegan, B., Mesquita, R., Chazdon, R.L., 2015. Successional dynamics in neotropical
forests are as uncertain as they are predictable. Proc. Natl. Acad. Sci. U.S.A. 112,
8013–8018.
Orozco-Zamora, C., Montagnini, F., 2007. Lluvia de semillas y sus agentes dispersores en
plantaciones forestales de nueve especies nativas en parcelas puras y mixtas en la
Estación Biológica La Selva, Costa Rica. Recursos Naturales y Ambiente (Costa Rica)
49, 131–140.
Ortega-Pieck, A.A., López-Barrera, F., Ramírez-Marcial, N., García-Franco, J.G., 2011.
Early seedling establishment of two tropical montane cloud forest tree species: the
role of native and exotic grasses. For. Ecol. Manage. 261, 1336–1343.
Ortiz-Colín, P., Toledo-Aceves, T., López-Barrera, F., Gerez-Fernández, P., 2017. Can
traditional selective logging secure tree regeneration in cloud forest? Iforest 10,
369–375.
Ramírez-Soto, A., Lucio-Palacio, C.R., Rodríguez-Mesa, R., Sheseña-Hernández, I., Farhat,
F.N., Villa-Bonilla, B., Landa Libreros, L., Gutiérrez Sosa, G., Trujillo Santos, O.,
Gómez Sánchez, I., Ruelas Inzunza, E., 2018. Restoration of tropical montane cloud
forests: a six-prong strategy. Restoration Ecol. 26, 206–211.
Reid, J.L., Holl, K.D., Zahawi, R.A., 2015. Seed dispersal limitations shift over time in
tropical forest restoration. Ecol. Appl. 25, 1072–1082.
Rhoades, C.C., Eckert, G.E., Coleman, D.C., 2000. Soil carbon differences among forest,
agriculture, and secondary vegetation in lower montane Ecuador. Ecol. Appl. 10,
497–505.
Roa-Fuentes, L.L., Martínez-Garza, C., Etchevers, J., Campo, J., 2013. Recovery of soil C
and N in a tropical pasture: passive and active restoration. Land Degrad. Dev. http://
dx.doi.org/10.1002/ldr.2197.
RStudio Team, 2016. RStudio: Integrated Development for R. RStudio, Inc., Boston. URL
61
Ecological Engineering 117 (2018) 50–61
http://www.rstudio.com/.
Ruiz-Jaén, M.C., Aide, T.M., 2005b. Restoration success: how is it being measured?
Restoration Ecol. 13, 569–577.
Ruiz-Jaén, M.C., Aide, T.M., 2005a. Vegetation structure, species diversity, and ecosystem
processes as measures of restoration success. For. Ecol. Manage. 218, 159–173.
Rzedowski, J., 1996. Análisis preliminar de la flora vascular de los bosques mesofilos de
montaña de México. Acta Bot. Mex. 35, 25–44.
Saldarriaga, J.G., West, D.C., Tharp, M.L., Uhl, C., 1988. Long-term chronosequence of
forest succession in the upper Río Negro of Colombia and Venezuela. J. Ecol. 76,
938–958.
Sampaio, A.B., Holl, K.D., Scariot, A., 2007. Does restoration enhance regeneration of
seasonal deciduous forests in pastures in central Brazil? Restoration Ecol. 15,
462–471.
Scatena, F.N., Bruijnzeel, L.A., Bubb, P., Das, S., 2010. Setting the stage. In: Bruijnzeel,
L.A., Scatena, F.N., Hamilton, L.S. (Eds.), Tropical Montane Cloud Forests Science for
Conservation and Management. Cambridge University Press, Cambridge, UK, pp.
3–13.
Suganuma, M.S., Durigan, G., 2015. Indicators of restoration success in riparian tropical
forests using multiple reference ecosystems. Restoration Ecol. 23, 238–251.
Thijs, K.W., Aerts, R., Van de Moortele, P., Musila, W., Gulinck, H., Muys, B., 2014.
Contrasting cloud forest restoration potential between plantations of different exotic
tree species. Restoration Ecol. 22, 472–479.
Toledo-Aceves, T., Swaine, M.D., 2008. Effect of lianas on tree regeneration in gaps and
forest understory in a tropical forest in Ghana. J. Vegetation Sci. 19, 717–728.
Williams-Linera, G., Toledo-Garibaldi, M., Hernández, C.G., 2013. How heterogeneous
are the cloud forest communities in the mountains of central Veracruz, Mexico? Plant
Ecol. 214, 685–701.
Williams-Linera, G., Bonilla-Moheno, M., López-Barrera, F., 2016. Tropical cloud forest
recovery: the role of seed banks in pastures dominated by an exotic grass. New
Forests 47, 481–496.
Wortley, L., Hero, J.M., Howes, M., 2013. Evaluating ecological restoration success: a
review of the literature. Restoration Ecol. 21, 537–543.
Zahawi, R.A., Holl, K.D., Cole, R.J., Leighton, R., 2013. Testing applied nucleation as a
strategy to facilitate tropical forest recovery. J. Appl. Ecol. 50, 88–96.