|

Received: 14 February 2017    Accepted: 14 July 2017

DOI: 10.1111/1365-2664.12976

RESEARCH ARTICLE

Planting accelerates restoration of tropical forest but assembly

mechanisms appear insensitive to initial composition

Lanping Li1,2,3 | Marc W. Cadotte2,4  | Cristina Martínez-Garza5  | 

Marinés de la Peña-Domene5  | Guozhen Du3

1
State Key Laboratory of Plateau Ecology
and Agriculture, College of Agriculture and Abstract
Animal Husbandry, Qinghai University, Xining, 1. Central to the success of restoration is how applied activities influence community
Qinghai, China
2
assembly mechanisms. Phylogenetic and trait-based approaches to community
Biological Sciences, University of Toronto-
Scarborough & Ecology and Evolutionary ecology are increasingly being used to test for non-random community assembly
Biology, University of Toronto, Toronto,
and are now being applied to assessments of habitat restoration. A critical question
Ontario, Canada
3 for the restoration of tropical forests is how plantings influence the recruitment of
State Key Laboratory of Grassland
Agroecosystems, School of Life Sciences, new species, and specifically the phylogenetic and functional diversity of restored
Lanzhou University, Lanzhou, Gansu, China
habitats.
4
State Key Laboratory of Biocontrol, Key
Laboratory of Biodiversity Dynamics 2. We examined 8 years (2006–2014) of tropical-forest recruitment in two restora-
and Conservation of Guangdong, Higher tion planting compositions (12 animal-dispersed and 12 wind-dispersed tree spe-
Education Institutes, College of Ecology and
Evolution, Sun Yat-sen University, Guangzhou, cies), with a control (no planting) in 24 plots in Los Tuxtlas, Mexico. Specifically, we
China assessed the influence of plantings on newly arriving individuals’ phylogenetic,
5
Centro de Investigación en Biodiversidad functional, taxonomic diversity, abundance and the change of these measures
y Conservación, Universidad Autónoma del
Estado de Morelos, Cuernavaca, Morelos, ­during early succession.
Mexico 3. The recruiting individuals’ phylogenetic, functional, taxonomic diversity and abun-
dance increased through succession. Both animal-dispersed planting and wind-
Correspondence
Marc W. Cadotte dispersed planting appeared to accelerate forest succession more than controls
Email: mcadotte@utsc.utoronto.ca
(natural succession), and diversity in the animal-dispersed plantings was marginally
Funding information higher after 8 years. We did not find any difference in recruiting individuals’ phylo-
TD Bank; Division of Environmental Biology,
genetic and functional dispersion (measured as standardized effect sizes) in any
Grant/Award Number: 0516259; University
of Illinois at Chicago; Universidad Autónoma given year, or when measured as turnover between successive pairs of years,
del Estado de Morelos (UAEM); NSF, Grant/
measuring planting composition and control plots.
Award Number: 0516259; Canada Foundation
for Innovation; Ontario Research Fund; 4. Recruiting individuals were phylogenetically clustered during early forest restora-
Natural Sciences and Engineering Research
tion regardless of treatment. At the same time, the recruits transitioned from ap-
Council of Canada, Grant/Award Number:
386151; International Science & Technology pearing randomly constructed to clustering according to functional traits, which
Cooperation Program of China, Grant/Award
suggests an increase in recruits’ functional similarity during early succession.
Number: 2015DFG31870
5. Synthesis and applications. Both the animal and wind-dispersed plantings acceler-
ated the increase of recruiting individuals’ phylogenetic, functional, taxonomic di-
versity and abundance during early succession. However, planting treatment did
not appear to alter community assembly mechanisms of recruiting individuals. Our
findings support restoration planting by showing that planting trees with animal
dispersal syndrome could accelerate forest restoration more than unassisted forest
regeneration. Furthermore, communities appeared to be phylogenetically and

986  |  wileyonlinelibrary.com/journal/jpe

© 2017 The Authors. Journal of Applied Ecology J Appl Ecol. 2018;55:986–996.
© 2017 British Ecological Society
LI et al. Journal of Applied Ecology |
      987

functionally clustered during early succession regardless of initial planted composi-

tion. Thus, while overall diversity increased with planting, if a restoration goal is to
maximize phylogenetic or functional dispersion, the planting composition tested did
not provide means to achieve this goal, at least during early succession.

KEYWORDS
community assembly, deterministic processes, forest regeneration, functional diversity,
phylogenetic diversity, planting, restoration ecology

1 | INTRODUCTION Functional and phylogenetic measures can also provide insights

Planting of young trees is a well-­known strategy to accelerate forest
recovery (de la Peña-­Domene, Martínez-­Garza, & Howe, 2013; Lamb,
Erskine, & Parrotta, 2005). Plantings may ameliorate local microcli-
matic conditions to enhance growth and survival of recruits, improve
the availability of soil resources that favour further recruitment (Roa-­
Fuentes, Martínez-­Garza, Etchevers, & Campo, 2015), attract animal
seed dispersal vectors (Reid, Holl, & Zahawi, 2015; Wunderle, 1997),
and might protect new recruits from grazing (de la Peña-­Domene,
Martínez-­Garza, Palmas-­Pérez, Rivas-­Alonso, & Howe, 2014; Padilla
& Pugnaire, 2006). It is well known that the selection of species for
restoration planting has important repercussions for further forest
succession and recovery (de la Peña-­Domene et al., 2013). To try to
maximize restoration success and to achieve certain goals, restoration
ecologists make decisions about the type of species to be transplanted
and the initial diversity and spatial patterning. For example, studies
have shown that the planting native vs. exotic species (Lugo, 1997),
the use of nurse species (Gómez-­Aparicio et al., 2004) and including
late-­successional species (Martínez-­Garza & Howe, 2003) all influence
restoration outcomes. Also, different planting methods or composi-
tions have been used, such as establishing monocultures, mixed plant-
ings (Lugo, 1997), to start with uniformly planted distribution or to
have plantings in aggregations (Holl, Zahawi, Cole, Ostertag, & Cordell,
2011). Traditionally, restoration success has been assessed with tax-
onomic diversity, but increasingly, restoration goals have expanded
to include other ecosystem properties and measures of biodiversity,
including phylogenetic and trait-­based measures (Barber et al., 2017;
Cadotte, Carscadden, & Mirotchnick, 2011; Hipp et al., 2015).
Functional traits have been used to predict species performance in
forest restoration (Guzmán-­Luna & Martínez-Garza, 2016; Martínez-­
Garza, Bongers, & Poorter, 2013; Martínez-­Garza, Peña, Ricker,
Campos, & Howe, 2005), but often within the context of taxonomic
restoration goals and measures that focus on the recruitment rate of
species or individuals (taxonomic diversity). Forest restoration goals
have expanded to include the restoration of ecosystem function and
services, and so functional and phylogenetic measures are thought
to better represent community resource use and overall contribution
to ecosystem function (Aerts & Honnay, 2011; Mori, Lertzman, &
Gustafsson, 2017). Thus, to assess multiple restoration goals, multi-
faceted measures of biodiversity need to be investigated.
into the relative importance of deterministic (Levine & HilleRisLambers,
2009) and stochastic (Hubbell, 2001) processes that influence com-
munity assembly. Deterministic or non-­random functional or phyloge-
netic patterns are generally thought to result from abiotic and biotic
filters. Specifically, abiotic filters promote the co-­occurrence of similar
species (functional or phylogenetic clustering), and biotic filters (e.g.
interspecific competition) result in the co-­occurrence of dissimilar
species (functional or phylogenetic overdispersion; Cavender-­Bares,
Kozak, Fine, & Kembel, 2009; Vandermeer, 1972; Webb, Ackerly,
McPeek, & Donoghue, 2002). However, linking patterns to mecha-
nisms is notoriously complicated (Cadotte & Tucker, 2017; Kraft et al.,
2015; Mayfield & Levine, 2010). For example, competitive exclusion
could also drive phylogenetic and functional clustering, by excluding
related or functional similar species with low competitive abilities
(Mayfield & Levine, 2010). Stochastic processes including unpredict-
able disturbance, dispersal limitation and stochastic demography pre-
dict no consistent pattern of co-­occurring species (Chase & Myers,
2011; Zhou & Zhang, 2008). Detecting these patterns matters for
restoration because goals, such as maximizing diversity, are highly de-
pendent on the dominant mechanism and how we measure diversity.
Most previous studies have found that phylogenetic or functional
clustering decreases as succession proceeds (Letcher et al., 2012;
Letten, Keith, & Tozer, 2014; Li et al., 2015; Mo, Shi, Zhang, Zhu, & Slik,
2013; Norden, Letcher, Boukili, Swenson, & Chazdon, 2011; Purschke
et al., 2013; Whitfeld, Kress, Erickson, & Weiblen, 2012). This suggests
that either abiotic filters select for similar species or, perhaps more
appropriately, similar species having correlated fitness responses to
environmental conditions during early succession (Cadotte & Tucker,
2017). However, some studies have observed the opposite succes-
sion pattern, with overdispersion in the Neotropics (Letcher, 2010) or
random patterns in desert ecosystems during early succession (Verdú,
Rey, Alcántara, Siles, & Valiente-­Banuet, 2009). Furthermore, most of
the previous studies used chronosequence comparisons of different
successional states rather than succession within a longitudinal study
of a single plot through time, and the lack of time series can result in
incorrect inferences of mechanisms (Li et al., 2015). Here, we traced
the changes in the phylogenetic and functional diversity of commu-
nities undergoing restoration and the recruiting species over 8 years
and assessed the influence of initial planting composition on tropical-­
rainforest restoration.
 |Journal of Applied Ecology
988       LI et al.
In this paper, our goal was to examine how transplanted species
influence phylogenetic and functional diversity of recruited commu-
nities and to determine if the composition of plantings influences
community assembly mechanisms during early succession. If plant-
ings alleviate abiotic filters (e.g. facilitation) for recruiting species or
increase seed dispersal, there should be more co-­occurring recruits in
the plots with plantings. How these effects could influence phyloge-
netic and functional patterns of the recruits and communities under-
going restoration depends on the dominant structuring mechanism.
If the availability of soil resources is improved by plantings and local
resource competition for recruits is alleviated, then we should expect
less phylogenetic or functional overdispersion of recruiting species.
Conversely, if the environment selects for species possessing similar
traits during early succession, then plantings, which alleviate abiotic
stress, might reduce clustering of recruits. However, plantings may
also strengthen phylogenetic or functional clustering and slow the
phylogenetic or functional turnover of recruiting species due to nega-
tive interspecific interactions (e.g. size-­asymmetric light competition)
or by reproducing large numbers of offspring.
Using 8 years of recruitment data from plots planted with 12
animal-­dispersed tree species, 12 wind-­dispersed tree species, or un-
planted controls (natural succession) in Los Tuxtlas, Mexico, we ask:
F I G U R E   1   Experimental design of 24 30 × 30m restoration plots
arranged in a 8 × 3 grid within a 12-­ha pasture at Los Tuxtlas, Mexico.
Vegetation at the plots is shown for three different years (2003,
2012 and 2014). Plots marked with green were planted with animal-­
dispersed species, plots marked with blue were planted with wind-­
dispersed species and plots marked with red were left unplanted.
Distances from the plots to the closest vegetation forest and the
University Reserve are drawn in straight lines from the corners of the
grid to the forest patches. All digital images were taken from Google
Earth 7.1.8.3036, access date: 1/17/2017
(1) if there is any influence of composition of plantings on commu-
nity phylogenetic or functional diversity (with and without plantings)
during early succession; (2) if plantings alter the observed dominant
pattern (e.g. from clustered to overdispersed) of the recruiting individ-
uals and the restoration communities (all individuals), and (3) if plant-
ings influence the functional and phylogenetic turnover over time.
We predict that plantings might accelerate the restoration of forest
communities in terms of species richness (SR) compared to natural
succession, but we do not have specific predictions about the influ-
ence of plantings on the observed dominant structuring mechanism of
recruiting individuals.
2 | MATERIALS AND METHODS
2.1 | Study site
This study was conducted in pastures close to the Los Tuxtlas
Biological Station, part of the Los Tuxtlas Biosphere Reserve, Veracruz,
Mexico (18°05′N and 18°45′N; 94°35′W and 95°30′W; see Figure 1
for study location). The reserve harbours a tropical moist evergreen
forest and mean annual rainfall at the station (measured from 1997
to 2007) was 4,275 ± 404 mm, with a dry season from March to May.
The soil is sandy loam originating from basalt and andesite mixed with
volcanic ash; the texture is mainly clay (48.5%) with an acidic pH (4.9;
González-­Soriano, Dirzo, & Vogt, 1997). Forest at the site was cleared
more than 30 years ago and the remaining vegetation was burned,
and corn was planted for one season together with native (Axonopus
compressus and Paspalum conjugatum) and exotic (Cynodon dactylon,
Brachiaria brizantha, Brachiaria decumbens and Panicum spp.) grasses.
The current pastures are under intensive cattle ranching and manage-
ment; cutting, use of herbicide or fire is applied to eliminate all natural
forest regeneration. We used a list of 400 woody species as the pool
of candidate species for this research based on previous studies of the
forest reserve next to the research site (Bongers, Popma, del Castillo,
& Carabias, 1988; de la Peña-­Domene et al., 2013; Martínez-­Garza &
González-­Montagut, 1999).
2.2 | Experimental design
The experimental design is described in detail in de la Peña-­Domene
et al. (2013), but briefly, 24 fenced 30 × 30 m plots separated by 35 m
of active cattle pasture arranged in a 3 × 8 grid were established in
2006. Eight plots were planted with 12 native animal-­dispersed tree
species, and eight plots with 12 native wind-­dispersed tree species.
A total of 144 seedlings (12 seedlings per species) were planted at a
spacing distance of 2 × 2 m. Seedlings were 4–7 months old at plant-
ing. Eight unplanted plots were left as fenced controls for natural
succession to take place. To alleviate the negative effects of com-
petition with grasses, vegetation within 50 cm of planted seedlings
was removed until saplings were taller than surrounding grass (about
1.5 m high). Within each plot, individuals of all species were planted
in mixed stands in a highly regular arrangement to maximize the dis-
tance between individuals of the same species. Recruits >10 cm high
LI et al.
(both trees and shrubs) were recorded 1–3 times every year from
2007 to 2014. The census data in May, June or July (except for 2014,
when census was in January) were used to estimate species’ yearly
recruitment.
2.3 | Functional traits
In this study, we used seven continuous functional traits for species
observed during succession: maximum plant height, maximum diam-
eter at breast height (DBH), maximum canopy cover, leaf area (LA),
leaf mass per unit area (LMA), leaf dry matter content (LDMC) and
seed mass; and three categorical functional traits: growth form, seed
dispersal mechanism and successional status for our analysis. All trait
data were obtained from previous studies in this system (Guzmán-­
Luna & Martínez-Garza, 2016; Martínez-­Garza, Bongers et al., 2013;
Martínez-­Garza, Tobon, Campo, & Howe, 2013) and the TRY data-
base (Kattge et al., 2011). Few species’ traits were obtained from
congeneric relatives (genus level) which included two species’ maxi-
mum DBH and maximum canopy cover, three species’ maximum plant
height and LDMC, five species’ seed mass, six species’ LA and eight
species’ LMA. Growth form was coded with two levels (shrub and
tree), seed dispersal with two levels (animal and wind) and succes-
sional status with two levels (pioneers and non-­pioneers). The seven
functional traits were chosen to represent species multidimensional
functions associated with competitive ability, resource allocation, dis-
persal ability, and successional strategy (Cornelissen et al., 2003). We
used Gower’s distance (Gower, 1971), which allows for missing data
and categorical data in quantifying distances, to generate a functional
distance matrix that represented the functional similarity between
species. In order to apply the analytical methods, we constructed a
functional trait dendrogram to serve as an analogue to a phyloge-
netic tree by using the Gower distance matrix and UPGMA clustering
(Petchey & Gaston, 2002).
2.4 | Community phylogeny
We collected three sequences from GenBank: two plastid DNA
genes (rbcL and matK) and one nuclear DNA gene (ITS, contain-
ing ITS1, 5.8s and ITS2) for 400 species representing the regional
species pool for phylogenetic analyses. Of the 400 species, 232
had at least one gene represented in GenBank and we used the
sequences from congeneric relatives as proxies for the remaining
168 species. From the 168 species, 10 species were only identi-
fied to the genus level. We also used two species representative
of early diverging in seed plant evolution—Amborella trichopoda
and Cycas revoluta—to serve as outgroup species. Concatenated
sequences were aligned using MUSCLE (Edgar, 2004) and the best
nucleotide substitution model (GTR+G+I) was identified using
jModeltest (Posada, 2008).
We generated a maximum likelihood phylogeny using PHYML with
a BIONJ starting tree (Guindon & Gascuel, 2003). Nodal support was
estimated using approximate likelihood-­ratio test scores, and a semi-
parametric rate-­smoothing method (Sanderson, 2002) was applied to
Journal of Applied Ecology |
      989
transform the phylogeny to an ultrametric tree using the r package ape
(Paradis, Claude, & Strimmer, 2004).
2.5 | Phylogenetic, functional and taxonomic
diversity
We used Faith’s PD to measure the phylogenetic diversity and
Petchey and Gaston’s FD to measure the functional diversity for
recruiting individuals and all individuals (recruits and transplants)
in each plot. Faith’s PD is defined as the sum of the branch lengths
of the phylogeny connecting all species in a plot (Faith, 1992), and
Petchey and Gaston’s FD is defined as the sum of the branch length
in a trait dendrogram connecting all species in a plot (Petchey &
Gaston, 2002).
We used the standardized effect size of the observed mean pairwise
phylogenetic distance (SES.MPD) and mean nearest phylogenetic taxon
distance (SES.MNTD) among species to evaluate the phylogenetic
local dispersion of recruiting individuals and all individuals in each plot
(Cadotte & Davies, 2016). Positive standardized effect sizes indicate a
higher observed value than expected and are referred to as overdis-
persed, and negative values indicate a lower observed value than ex-
pected, representing clustering (Cadotte & Davies, 2016; Webb et al.,
2002). We used three commonly employed null models in our analysis:
null model 0: shuffle species labels across distance matrix; null model 1:
randomize community matrix by drawing species from species pool; null
model 2: randomize community matrix by drawing species from phylog-
eny or trait dendrogram pool (Cadotte & Davies, 2016). Compared with
null model 1, null models 0 and 2 may focus on the chance that species
occur in a community, and null model 1 better captures interspecific in-
teractions in communities. The null models returned qualitatively similar
results and so null model 1 is ­reported in the text.
Identical measures were applied to explore functional local dis-
persion of recruiting individuals and all individuals in each plot using
the trait dendrogram. The analogous standardized effect sizes of
functional local dispersion were termed SES.MFD for the mean pair-
wise functional distance and SES.MNFD for the mean nearest taxon
functional distance (e.g. Li et al., 2015). We calculated the SES.MPD,
SES.MNTD, SES.MFD and SES.MNFD for recruiting individuals and
all individuals in each plot in every year; all dispersion metrics were
abundance weighted.
To assess the phylogenetic and functional turnover during early
succession, we calculated phylogenetic and functional dissimilar-
ity between the recruiting species in pairs of plots sampled over
different ages with two metrics. The first metric is a calculation
of the mean pairwise phylogenetic (βMPD) and functional (βMFD)
distance between communities, and the second metric is a cal-
culation of mean nearest taxon phylogenetic (βMNTD) and func-
tional (βMNFD) distance between communities (Cadotte & Davies,
2016). The turnover metrics of βMPD (or βMFD) and βMNTD (or
βMNFD) represent a basal and terminal dispersion of the assem-
blage, respectively (Swenson et al., 2012). And we focused on the
standardized effect size of these metrics (SES.βMPD, SES.βMNTD,
SES.Βmfd and SES.βMNFD) which provides us with phylogenetic
 |Journal of Applied Ecology
990       LI et al.

and functional turnover dispersion. We also used SR and the abun-
dance of recruiting individuals to describe the taxonomic local di-
versity and the recruitment dynamics for each plot. Recruitment
data overlap with de la Peña-­Domene et al. (2013, 2014). All the
analyses were performed using the Picante r package (Kembel
et al., 2010) in the r environment (http://www.R-project.org).
difference of recruits’ diversities (phylogenetic, functional and taxo-
nomic diversity) and abundance among plantings plots and control
plots increased through time and in the eighth year they were max-
imally different (Figure 2). The abundance of recruits in the animal-­
dispersed plantings was two times and four times greater than in the
wind-­dispersed plantings and control plots, respectively (Figure 2d).

2.6 | Statistical analysis 3.2 | Phylogenetic and functional dispersion during

We used mixed effects models to evaluate the effect of planting
and succession time on recruiting individuals’ phylogenetic, func-
tional, taxonomic diversity and abundance using lmerTest package
(Bates, Maechler, Bolker, & Walker, 2014; Kuznetsova, Brockhoff, &
Christensen, 2016) in r. Treatment (plots containing animal-­dispersed
tree species, wind-­dispersed tree species and control plots) and suc-
cession time (entered as a linear or quadratic term) were used as fixed
factors and the eight plots nested within each treatment were con-
sidered as random effects. The best-­fit model and second-­fit model
were selected based on Akaike’s information criterion (AIC) among
models including intercept only, treatment and succession time alone,
together, and their interaction. We calculated the delta AIC between
the best-­fit model and second-­fit model; only the details of the best-­
fit model are shown in the results.
3 |  RESULTS
3.1 | The change in community diversity during early
succession
The model that included treatment (control and the two planting com-
positions), succession time and their interactive effects was the best at
explaining variation in phylogenetic, functional, taxonomic diversities
and also the abundance of recruiting individuals (Table 1). The meas-
ures of recruits’ diversity increased over time (Figure 2, Table S1). The
early succession
The model containing only succession time was the best predictor
of community phylogenetic dispersion (SES.MPD and SES.MNTD;
Table 1). The model including both linear and quadratic terms of suc-
cession time was the best predictor of functional local dispersion (SES.
MFD and SES.MNFD; Table 1), which suggested that treatment was
not an effective explanation for variation in recruits’ phylogenetic and
functional local dispersion. The values of SES.MPD and SES.MNTD
ranged from −0.084 to −1.320 and −0.077 to −0.910, respectively
(Figure 3a,b), indicating a consistently clustered phylogenetic pat-
tern. The influence of succession time on phylogenetic local disper-
sion (SES.MPD and SES.MNTD) of recruiting individuals was quite
weak (Figure 3a,b, Table S2). While the functional local dispersion
(SES.MFD and SES.MNFD) significantly changed through time: the
values of SES.MFD decreased from 0.655 to −1.206 and SES.MNFD
decreased from 0.741 to −0.792, which indicates that functional
clustering became stronger during early succession (Figure 3c,d). The
results of phylogenetic clustering during early succession and increas-
ing functional clustering were consistent across different null models
(Figures S1 and S2).
In contrast to the phylogenetic and functional local dispersion
of the recruits, we found that phylogenetic and functional local dis-
persion of all individuals (which includes both recruits and plantings)
were significantly affected by treatment and the interaction of time
and treatment (except the SES.MNTD of all individuals in plots with

T A B L E   1   Best-­fit models and the second-­fit models that model the effect of treatment and succession time on recruiting individuals’
phylogenetic, functional, taxonomic diversity and abundance identified based on Akaike’s information criterion (AIC) through linear mixed
effects models. Treatment (plots with animal-­dispersed species, wind-­dispersed species, and no-­transplant control plots) and succession time
were used as fixed factors and the eight plots nested within each treatment were considered as random effects

Best-­fit model Second-­fit model Delta AIC Figure

2
PD ~Treatment + Time + Treatment * Time + (1|Plot) ~Time + Time + (1|Plot) 2.244 Figure 2a
FD ~Treatment + Time + Treatment * Time + (1|Plot) ~Time + (1|Plot) 4.575 Figure 2c
2
SR ~Treatment + Time + Treatment * Time + (1|Plot) ~Time + Time + (1|Plot) 3.06 Figure 2b
Individual ~Treatment + Time + Treatment * Time + (1|Plot) ~Time + Time2 + (1|Plot) 2.468 Figure 2d
SES.MPD ~Time + (1|Plot) ~Treatment + Time + (1|Plot) 0.689 Figure 3a
SES.MNTD ~Time + (1|Plot) ~Treatment + Time + (1|Plot) 0.808 Figure 3b
2
SES.MFD ~Time + Time + (1|Plot) ~Time + (1|Plot) 6.980 Figure 3c
SES.MNFD ~Time + Time2 + (1|Plot) ~Time + (1|Plot) 0.687 Figure 3d
SES. βMPD ~1 + (1|Plot) ~Treatment + (1|Plot) 1.017 Figure 5a
SES. βMNTD ~1 + (1|Plot) ~Treatment + (1|Plot) 0.683 Figure 5b
2
SES. βMFD ~Time + Time + (1|Plot) ~Treatment + (1|Plot) 1.367 Figure 5c
SES. βMNFD ~1 + (1|Plot) ~ Time + (1|Plot) 0.112 Figure 5d
LI et al. Journal of Applied Ecology|
      991

(a) (b)

PD

SR
(c) (d)

Abundance
FD

F I G U R E   2   Phylogenetic (PD), functional

(FD), taxonomic diversity (SR) and
abundance for recruiting individuals in plots
with animal-­dispersed plantings (red), wind-­
dispersed plantings (black) and unplanted
control plots (grey) through 8 years. Bars
represent means ±SE Year Year

(a) (b)
SES.MPD

SES.MNTD

(c) (d)
SES.MNFD
SES.MFD

F I G U R E   3   Phylogenetic and functional

local dispersion for recruiting individuals
in plots with animal-­dispersed plantings
(red), wind-­dispersed plantings (black) and
unplanted control plots (grey) through
8 years. Bars represent means ±SE Year Year
 | Journal of Applied Ecology
992       LI et al.
animal-­dispersed trees, Table S3, Figure 4). The influence of succes-
sion time on the phylogenetic and functional local dispersion for all
individuals was also weak (Table S3). The SES.MPD of all individuals in
plots with plantings (both animal-­and wind-­dispersed trees) was much
more clustered than the control plots (Figure 4a). For SES.MNTD, only
plots with wind-­dispersed trees were more clustered than control
plots (Figure 4b). The functional local dispersion (SES.MFD and SES.
MNFD) confirmed that all individuals in both plantings (including both
planted and recruiting individuals) were more clustered than individu-
als found in the control plots (Figure 4c,d).
3.3 | Phylogenetic and functional turnover
dispersion during early succession
The phylogenetic turnover dispersion (SES.βMPD and SES.βMNTD) of
recruiting species across all plots was below 0 (Figure 5a,b), indicat-
ing lower turnover than expected, and there was no significant dif-
ference between plantings and control plots (Table 1, Table S2). The
functional turnover dispersion (SES.βMPD and SES.βMNTD) for the
recruiting species appeared random (no significant trends) and they
also did not differ among treatments (Figure 5c,d; Table S2), though
SES.βMFD appears to show a negative trend for the animal dispersed
and control plots and the wind-­dispersed treatment was temporally
quite dynamic.
4 |  DISCUSSION
We found that recruiting species phylogenetic, functional, taxonomic
diversities and abundance increased as succession unfolded and
plantings accelerated the increases of these measures. The recruits’
phylogenetic local dispersion changed little over the first 8 years of
succession, but the functional local dispersion transitioned from ap-
pearing random to being clustered. This result implies the trend of
recruits to be functional similar during early tropical-­forest restoration
which might shape further community structure.
Plantings did not affect the recruits’ phylogenetic and functional
local and turnover dispersion; and the recruits’ phylogenetic and func-
tional turnover dispersion did not significantly change during the first
8 years of succession. While the phylogenetic and functional diver-
sity of all individuals in each plot (including transplanted species) were
significantly influenced by transplanted species themselves: when we
look at both recruiting and transplanted species, the phylogenetic
and functional local dispersion in those plots were much more clus-
tered than in control plots (except the SES.MNTD of all individuals in
plantings of animal-­dispersed species). Here, we uniquely addressed
the influence of planting composition on recruits’ phylogenetic and
functional diversity, which may help us understand the mechanisms
structuring community composition during early forest restoration.
These results can help temper the expectations about diversity change
in forest restoration, and that while choosing species mixes that can
accelerate forest restoration rate, functional and phylogenetic dis-
persion might not be greatly affected. We posit that the mechanisms
structuring early forest succession create functionally and phylogenet-
ically clustered communities regardless of planting regime.
4.1 | The influence of succession time and
transplanted species on forest restoration
The recruits’ phylogenetic, functional, and taxonomic diversity, as well
as abundance, all increased over time and this result was consistent
with previous studies (de la Peña-­Domene et al., 2013; Purschke et al.,
2013). Both animal-­dispersed and wind-­dispersed species plantings
accelerated forest restoration. From these results (e.g. Figure 2), there
appears to be a lag, taking between 3 and 4 years for these increases
to be observed. This seems reasonable as the influence of the trans-
planted species and early colonists on local environmental conditions
and soil properties should increase over time; also, early successional
transplants and recruits started to reproduce after 3–4 years. For ex-
ample, 4 years after planting, 12 transplants from five species were
reproducing, whereas 1 year later, 67 transplants from 11 tree species
were reproducing. As these different aspects of biodiversity increase,
we should also expect this restored forest to provide more ecosys-
tem services (Cadotte et al., 2011; Srivastava, Cadotte, MacDonald,
Marushia, & Mirotchnick, 2012). For example, flower resources for
pollinators, reduced soil erosion and, in general, habitat for many
animals.
4.2 | Mechanisms driving early succession produce
clustered communities
Despite the overall increase in diversity (Figure 2), the recruiting in-
dividuals were more related to each other than expected from ran-
dom assembly during early succession (Figure 3a,b). Previous studies
have also shown that early successional communities tend to be com-
posed of ecological similar or closely related species (Letcher et al.,
2012; Li et al., 2015; Mo et al., 2013; Norden et al., 2011; Purschke
et al., 2013; Whitfeld et al., 2012). In contrast, we observed in-
creased functional clustering of recruiting individuals after the fourth
successional year (Figure 3c,d), suggesting that early successional
communities’ recruits increased in functional similarity—a result also
observed in a longitudinal study of forest succession in temperate
deciduous forests (Li et al., 2015). This result might be caused by the
extinction of recruits that are functionally dissimilar to the species
present in these plots (presumably increasing size-­asymmetric light
competition, ill-­suited to local conditions or selective predation) or
more colonization of tree species that are functionally similar to the
residents (Li et al., 2015). In the first 4 years, the functional local dis-
persion of recruiting individuals was quite random and then changed
to being clustered. These results imply that either stochastic pro-
cesses might play a more important role during the first few succes-
sional years or these long-­lived species require several years for the
assembly mechanisms to be observed.
We did not find an influence of planting composition on the re-
cruits’ phylogenetic and functional local dispersion which might sug-
gest that planting composition did not affect the mechanisms that
LI et al. Journal of Applied Ecology|
      993

(a) (b)

SES.MPD

SES.MNTD
(c)
SES.MFD (d)

SES.MNFD
F I G U R E   4   Phylogenetic and functional
local dispersion for all individuals in plots
with animal-­dispersed plantings (red), wind-­
dispersed plantings (black) and unplanted
control plots (grey) through 8 years. Bars
represent means ±SE Year Year

(a) (b)
SES.βMPD

SES.βMNTD

(c) (d)
SES.βMFD

SES.βMNFD

F I G U R E   5   Phylogenetic and functional

turnover dispersion for recruiting
individuals in pairs of plots with animal-­
dispersed plantings (red), wind-­dispersed
plantings (black) and unplanted control
plots (grey) through 8 years. Bars represent
means ±SE Year Year
 | Journal of Applied Ecology
994       LI et al.
structure community composition during this early tropical-­forest
restoration. An alternative is that recruits produced by plantings
drive phylogenetic and functional clustering, but it is impossible for
us to distinguish between locally produced recruits and those origi-
nating from the primary forest. The potential effect of local recruits
strengthened over time, from the five species recorded reproducing
4 years after planting, only one species was recorded as a recruit, but
by 2014, four of the species transplanted were recorded as recruits.
Despite that there were more recruits in the plots with plantings, their
phylogenetic and functional local and turnover dispersion were not
different from those recorded in the plots under natural succession. It
may be because the species of seeds dispersed by both animals and
wind were similar to the species that dispersed to plots under natural
succession, even though there were more seeds and species falling
in the plantings (see Popoca-­Ortega, 2016). Regardless, the ability to
accelerate forest restoration might depend on the increase of seed
dispersal by fruit-­eating animals (de la Peña-­Domene et al., 2014), the
recruits produced by the plantings and the increased survival rate of
new recruits.
We observed a discrepancy between phylogenetic and functional
turnover patterns and the mismatch is not surprising given that there
are not strong phylogenetic signals in the seven continuous traits
(Table S4). Phylogenetic turnover was slower than that expected, but
functional turnover was no different than random expectations. The
low phylogenetic turnover might imply the limitation of colonists or
the importance of long-­lived species in community assembly during
restoration. If the plantings survive and limit new recruitment, or if the
recruits are generally closely related to the earlier recruits, then we
should expect that the phylogenetic turnover will be low. While the
new recruits’ functional turnover was random, they remained function-
ally clustered, and we should expect the community pattern to change
only if turnover was non-­random (Li et al., 2016). Consistent with the
result of recruits’ phylogenetic and functional local dispersal, there was
no difference in the recruits’ phylogenetic and functional turnover dis-
persal between the plantings and control plots. These results serve as a
reminder of the complex nature of community assembly and difficulty
in uncovering the mechanisms that maximize functional and phyloge-
netic diversity (Grman, Bassett, & Brudvig, 2013; Letten et al., 2014).
4.3 | Management implications
Global initiatives related to habitat restoration include the Aichi bio-
diversity targets (CBD, 2010), the Bonn Challenge (Bonn-­Challenge,
2014) and for the Americas, the Initiative 20 × 20 (Initiative-­20x20,
2014), and such initiatives benefit from restoration strategies that
maximize recovery rate and probability of success. Further, the global
initiative REED+ supplies targets which aim to maximize carbon se-
questration, and these goals are related to restoration outcomes.
However, none of these ambitious global and regional initiatives in-
clude suggestions about how to restore ecosystems. Further, few
of the countries that partner with these initiatives actually have na-
tional restoration plans (reviewed for Latin America, Méndez-­Toribio,
Martínez-­Garza, Ceccon, & Guariguata, 2017).
Minimal restoration intervention includes actions to remove
chronic disturbance so natural succession may take place; this is also
referred to as “passive” restoration (Zahawi, Reid, & Holl, 2014) or un-
assisted forest regeneration (Chazdon & Guariguata, 2016); whereas
maximal intervention (Guzmán-­Luna & Martínez-Garza, 2016), also
called assisted succession (Chazdon & Guariguata, 2016), involves
restoration plantings. Minimal intervention is suggested for land-
scapes with existing seed sources and resulting communities should
ultimately resemble the original communities (Latawiec et al., 2016);
this approach is cheaper and is therefore easier to implement at larger
scales (Chazdon & Guariguata, 2016), although some hidden costs
have been identified (Zahawi et al., 2014). On the other hand, even
when restoration plantings are expensive, they may decrease spe-
cies loss (Martínez-­Garza & Howe, 2003) by favouring the establish-
ment of vulnerable tree species (de la Peña-­Domene, Minor, & Howe,
2016). Further, when diverse initial compositions are used, restored
areas may better reflect the natural diversity and variability observed
in original communities (Howe & Martinez-­Garza, 2014). Our study
reveals that the influence of transplanted species on tropical-­forest
restoration success depends on how success is defined, thus on the
restoration goals. Even though the planting compositions tested did
not increase phylogenetic or functional dispersion of these early suc-
cessional assemblages, diversities in the animal-­dispersed plantings
are greater than other plantings and natural succession. Therefore,
restoration plantings resulted in faster increases in the different diver-
sity measurements.
Moreover, in most plots with plantings, all individuals appeared to
be phylogenetically and functionally clustered relative to what is ex-
pected from the neighbouring intact forest, with no apparent shifts in
the dominant structuring mechanism. This is likely caused by the short
timeframe of the study, the species selected for planting, and the fact
that the dominant dispersal mechanism selected a clustered subset of
species from the regional species pool.
Maximizing diversity is one approach to enhancing ecosystem
function, and it is possible to achieve desired ecological services by
selecting appropriate assemblages (Lamb et al., 2005) since trans-
planted species will shape the restoration community during early
succession. For example, practitioners can transplant fast growing
seedlings to supply certain functions or goods or we can plant seed-
lings with specific dispersal syndromes to accelerate biodiversity
restoration. We recommend transplanting species that can attract
animal seed dispersal vectors to accelerate forest restoration as sup-
ported by the higher diversity in animal-­dispersed plantings compared
with the diversities of recruits in plots with wind-­dispersed plantings
after 8 years (Figure 2), and these differences might become more
pronounced through time. If maximizing species dissimilarity is a
stated restoration goal, then perhaps transplanting maximally diverse
species would be advisable. Further, if certain species are likely to
disperse into the restoration site, then biasing the initial composition
to species with low dispersal ability could ultimately maximize local
diversity.
Our findings might be used to design appropriate restoration
strategies, regarding assisted or unassisted forest regeneration, even
LI et al.
though the exact mechanisms are not yet understood. Our results
revealed that negative interspecific interactions between the recruits
and transplanted were likely weak, at least during early succession.
Further, while initial plantings did not increase recruits’ dissimilarity,
they did increase overall diversity. Thus, initial planting composition
should be considered one possible tool to achieve certain restoration
goals, but other tools should be employed to achieve other goals.
ACKNOWLE DGE ME N TS
We are grateful to Luz María Ayestarán for expert field assistance.
C.M.G. and M.d.D. gratefully acknowledge financial and logistical
support from the University of Illinois at Chicago, the Universidad
Autónoma del Estado de Morelos (UAEM), the Director and
staff of the Los Tuxtlas Biological Station (Universidad Nacional
Autonoma de México), NSF (DEB # 0516259 to Henry F. Howe
and C.M.G.) and National Geographic Society for the maintenance
of the fences. M.W.C. was supported by the TD Professor of
Urban Forest Conservation and Biology chair, Canada Foundation
for Innovation, the Ontario Research Fund and Natural Sciences
and Engineering Research Council of Canada (#386151). L.L. was
supported by the International Science & Technology Cooperation
Program of China (2015DFG31870). We thank the TRY database
for providing functional traits data (http://www.try-db.org). The
TRY initiative and database is hosted, developed and maintained by
J. Kattge and G. Bönisch (Max Planck Institute for Biogeochemistry,
Jena, Germany).
DATA ACCE SSI BI LI TY
Data available from the Dryad Digital Repository https://doi.
org/10.5061/dryad.sh0v5 (Li et al., 2017).
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S U P P O RT I NG I NFO R M AT I O N
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How to cite this article: Li L, Cadotte MW, Martínez-Garza C, de
la Peña-Domene M, Du G. Planting accelerates restoration of
tropical forest but assembly mechanisms appear insensitive to
initial composition. J Appl Ecol. 2018;55:986–996. https://doi.
org/10.1111/1365-2664.12976