Post on 09-Apr-2023
Fast-growing pioneer tree stands as a rapid and
effective strategy for bracken elimination in the
Neotropics
David Douterlungne1*, Evert Thomas2 and Samuel I. Levy-Tacher3†
1El Colegio de la Frontera Sur, Carretera Panamericana y Perif�ericos Sur S/N, PO Box 29299, Maria Auxiliadora,
San Crist�obal de Las Casas, Chiapas, Mexico; 2Bioversity International, Regional Office for the Americas,
Recta Cali-Palmira Km 17 – CIAT, PO Box 6713, Cali, Colombia; and 3El Colegio de la Frontera Sur, ECOSUR, Carr.
Panamericana y Periferico Sur s/n Barrio Ma. Auxiliadora, C.P. 29290, San Cristobal de las Casas, Chiapas, Mexico
Summary
1. Large areas of agricultural land around the world are degraded as a consequence of domi-
nance by bracken fern (Pteridium spp.). Tropical production systems based on shifting culti-
vation and cattle breeding are particularly vulnerable to invasion of this species. In spite of
this, effective methods for tropical bracken control are limited.
2. Fast-growing tree species have been used successfully to out-compete aggressively coloniz-
ing heliophytes and trigger natural succession. Drawing on a traditional Mayan management
technique, we evaluate the potential of the pioneer tree balsa (Ochroma pyramidale) to con-
trol Pteridium caudatum in Chiapas, Mexico. We tested different bracken cutting frequencies
and balsa propagation methods in a factorial randomized block experiment. Eighteen months
later, we quantified bracken biomass under the young balsa canopy.
3. Living bracken rhizome biomass correlated significantly with balsa basal area, leaf litter
biomass and understorey light intensity. While bracken rhizomes persisted in control plots, it
was completely eradicated in plots with a minimum balsa basal area of 11 m2 ha�1. This
threshold value was reached in less than 18 months with any of the tested propagation meth-
ods (seed broadcasting, direct sowing or nursery seedlings), on the condition of at least
monthly bracken cutting during the first six months.
4. The ability of fast-growing broad-leaved pioneer trees like balsa to quickly out-compete
bracken fern offers opportunities for large-scale application in tropical rural areas where eco-
nomic and technical resources are scarce.
5. Synthesis and applications. Mayan subsistence farmers traditionally use balsa to out-
compete invasive weeds, including bracken fern. Here, we highlight the usefulness of this
method for quick and effective bracken control in southern Mexico. This approach, in combi-
nation with balsa’s short rotation cycle, creates opportunities to rapidly convert bracken land
into forest stands with commercial potential, thus providing local income and increasing the
likelihood of adoption by rural people. We encourage further research to test the potential of
balsa and other fast-growing pioneer trees species for controlling bracken and similar weeds.
Key-words: balsa, biological control, ecological restoration, forest succession, Lacandon
tropical rainforest, Mexico, Ochroma pyramidale, Pteridium caudatum
Introduction
Bracken fern (Pteridium spp., Dennstaediaceae) is one of
the most persistent weeds world-wide, due to a combina-
tion of an ancestral global distribution dating back to the
Oligocene (~23�8 million years ago), and an effective dis-
persal and colonization capability (Der et al. 2009; Roos,
R€odel & Beck 2011). Bracken’s competitive advantage
relates to aggressive rhizomatous and aerial growth (Marrs,
Johnson & Duc 1998a), allelopathic and toxic effects on
competing species and grazing animals, respectively (Marrs
et al. 2000; Alonso-Amelot & Avendano 2002; Calder�on
*Correspondence author. E-mail: daviddouter@hotmail.com†Correction added after online publication 15 July 2013; S. I.
Levy-Tacher added as co-author.
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society
Journal of Applied Ecology 2013, 50, 1257–1265 doi: 10.1111/1365-2664.12077
Tobar et al. 2011), tolerance to fire (Gliessman 1978;
Da Silva & Silva Matos 2006), extreme weather events
(Roos et al. 2010) and the cutting of its fronds (Pakeman
et al. 2002; Roos, R€odel & Beck 2011). Furthermore, the
accumulation of slowly decomposing bracken fronds
(Frankland 1976) depletes seed and seedling banks, con-
strains natural recruitment (Da Silva & Silva Matos 2006;
Ghorbani et al. 2006) and can delay natural succession for
decades to centuries (Marrs et al. 2000; Roos, R€odel &
Beck 2011). Bracken typically colonizes open fields after
disturbance events, resulting in loss of land for crop or ani-
mal husbandry (Schneider & Goeghegan 2006) and hence
affecting people’s economies and well-being. In Great Brit-
ain, bracken was estimated to cover 7�3% (c. 17 100 km2)
of the land surface (Pakeman et al. 1996), representing an
estimated reduction in the land’s capital value of 5�5 billion
USD (Robinson 2008). Prior to the introduction of control
measures on the island of S~ao Miguel (Azores), bracken-
induced bladder cancer in one cattle breed was estimated to
cause an annual economic loss of 16�2 million USD, as
18% of the slaughtered animals and 13�5 million litres of
milk did not pass sanitary control (Pinto et al. 2001). In
Chiapas, Mexico, where this study took place, at least
360 km² (about 0�5% of the state territory) is dominated by
bracken (Suazo 1998).
Control of bracken is extremely difficult, and many
strategies have been tested without achieving complete
bracken elimination (Marrs, Johnson & Duc 1998b;
Pakeman et al. 2002; Le Duc, Pakeman & Marrs 2003;
Stewart et al. 2008; Roos, R€odel & Beck 2011). Most
literature on restoration of bracken land concerns strate-
gies targeted to temperate climates (but see Roos, R€odel
& Beck 2011) and can be classified in three main groups.
The first type is based on physically damaging the fronds
or rhizomes, often through the use of heavy machinery,
such as tractors and bulldozers (e.g. Le Duc, Pakeman &
Marrs 2003; Ghorbani et al. 2006). A second group of
treatments relies on chemical substances, such as
ASULAM (e.g. Pakeman et al. 2002; Stewart et al. 2008).
Both strategies are unlikely to be applied in poor rural
contexts as they require substantial financial and/or
labour investments during prolonged periods of time
(often exceeding 10 years; Marrs, Johnson & Duc 1998b;
Ghorbani et al. 2006). The third type of control measures
takes advantage of ecological processes such as competi-
tion and natural succession (e.g. Pakeman et al. 2002;
Slocum et al. 2006), and may be better tailored to the
tropical rural context as they are less resource-intensive.
In tropical ecosystems, pioneer tree species are of par-
ticular interest for biological bracken control of bracken,
owing to their ability to out-compete aggressively coloniz-
ing light-demanding weeds, and trigger forest succession
(Lamb, Erskine & Parrotta 2005). The Lacandon and
Ch’ol Mayan ethnic groups from the southern Mexican
rainforest have longstanding experience with the use of
key tree species to assist natural regeneration of tropical
evergreen forest on abandoned slash and burn plots. They
sow or tolerate balsa or Ochroma pyramidale (Cav.
ex Lam.) Urb., Malvaceae, a neotropical broad-leaved
pioneer tree species, on their fallows to accelerate soil
recovery (Diemont & Martin 2009). Balsa thrives on
abandoned agricultural soils with minimal maintenance
labour. Survival rates of 90% or more and mean heights
of 6–7 m have been registered after the first growth year
(Douterlungne 2005). Furthermore, from the second
growth year onwards, abundant balsa litter increases soil
organic matter (Diemont et al. 2006), while understorey
shade constrains the establishment and growth of light-
demanding weeds (D. Douterlungne, unpublished data).
When located in the vicinity of old-growth forest, balsa’s
big white flowers attract seed-dispersing fauna, especially
bats (Tschapka 2005) and insects, which in turn attract
small tree-climbing mammals (D. Douterlungne, personal
observation). Both balsa and bracken are amply distrib-
uted across the Neotropics (Lamprecht 1989; Der et al.
2009) and share similar habitat preferences for recently
burnt (Vazquez-Ya~nes 1974; Gliessman 1978) or disturbed
vegetation on well-drained soils (Kammesheidt 2000).
Establishment success and growth performance of balsa
in bracken land have been the topic of a previous publication
(Douterlungne et al. 2010). Here, we focus on the potential
of balsa plantations to effectively eliminate Pteridium cauda-
tum (L.) Maxon (previously Pteridium aquilinum var. cauda-
tum). We scrutinize the relationship between living bracken
biomass and three different balsa attributes: basal area, leaf
litter production and understorey light intensity.
Materials and methods
SITE DESCRIPTION
Our experiment was carried out in Lacanj�a Chansayab, Chiapas,
Mexico (16˚46′08″N, 91˚08′12″W). The study area borders the
largest undisturbed tropical rainforest area in Mesoamerica and
is located at 350 m above sea level, with an annual precipitation
between 2300 and 2500 mm, and a mean annual temperature of
25 °C (INEGI 1988). Predominant soils are humic acrisols
(Muench 1978). The landscape is characterized by a mosaic of
tropical evergreen forest –the local climax vegetation (Miranda
1998)– interspersed with secondary forest, crop fields and fallows
nearby settlements. The experimental plots were laid out within a
bracken infested area of c. 0�85 ha. Plots were impenetrable with-
out the use of a machete, with dead bracken fronds forming a 0�5–1 m thick layer and living fronds reaching up to more than two
metres high. According to local Lacandon farmers, on site
bracken domination dated back more than thirty years.
EXPERIMENTAL DESIGN
In October 2005, we set up a fully factorial randomized block
experiment of 2304 m², divided in four equal blocks of 576 m².
Each block was separated by a two metre access trail and
included nine adjacent plots of 8 9 8 m², where three balsa estab-
lishment methods were crossed with three bracken cutting
frequencies. Control plots (without balsa trees) for each of the
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
1258 D. Douterlungne, E. Thomas & S.I. Levy-Tacher
three cutting frequencies were not included in the original design,
but located in homogenous bracken land in the direct vicinity
(<10 m) of the four blocks. For statistical analyses, we included
each of the respective control plots in the nearest block.
Local Lacandon participants manually cleared (machete) and
burned the experimental area prior to establishing balsa trees.
As a first planting method, we mimicked the traditional Lacan-
don method of randomly broadcasting c. 5000 balsa seeds per
plot, which resulted in patchy distributions of emerging seed-
lings. The second and third method consisted of directly sowing
seeds and transplanting two-month-old nursery seedlings at
2 9 2 m spacing. No thinning was carried out during the exper-
iment. The minimum cutting frequency entailed only initial
clearing of the site prior to planting or sowing, without any
posterior cutting. The intermediate- and high-intensity treat-
ments consisted of cutting all bracken fronds every four and
two weeks, respectively, during the first six months of the exper-
iment. Survival and growth rates are reported in Douterlungne
et al. (2010).
Eighteen months after experiment initiation, balsa dominated
all plots where bracken was cut. We quantified remaining
bracken as: (i) visually estimated cover; (ii) weight of air-dried
fronds; and (iii) weight of air-dried rhizomes, considering living
and dead rhizomes separately. We quantified bracken rhizome
and frond biomass in three randomly assigned 0�25-m2 subplots
in the central 36 m2 of each plot, excavating holes as deep as the
deepest rhizome (>0�5 m deep). However, given the similar statis-
tical patterns observed for all bracken variables, we focus on liv-
ing rhizome biomass. The carbohydrate reserves in bracken
rhizomes are the fern’s primary means for regrowth (Watt 1940),
even after elimination of all of its fronds (Walker & Boneta
1995). Therefore, living rhizome biomass is considered the most
adequate predictor for assessing success of long-term bracken
control (Marrs, Johnson & Duc 1998a). We measured light inten-
sity with a linear photosynthetically active radiation (PAR) sen-
sor or ceptometer (Decagon, Pullman Washington, US) at four
random locations in the same central plot area, at noon of cloud-
less days, above the bracken vegetation and under the balsa can-
opy, where relevant. To quantify balsa performance, we weighed
all air-dried balsa leaf litter available in the bracken rhizome sub-
plots and calculated basal area based on the nine trees from the
central 36 m2 of each plot according to the following
formula: plot-based basal area ¼ 1000036 �P9 center plot trees
i¼1 ðdiameter
tree=2Þ2 � p. We measured tree diameter 10 cm above-ground
level, as several trees were smaller than 130 cm and would be
excluded in breast height-based basal area calculations.
STATIST ICAL ANALYSIS
We used an iterative modelling process (following Zuur et al.
2009) to identify variables that significantly contributed to
explaining plot-averaged bracken rhizome biomass. We started
with linear mixed effects (LME) models of different complexities
to address the spatial autocorrelation in our dataset and com-
pared these with a generalized least squares (GLS) model (fixed
component containing up to second-order interaction terms).
Aikake’s information criteria (AIC) and likelihood ratio tests
(Zuur et al. 2009) indicated no significant random (block or plot)
effect, and therefore, we retained the more parsimonious GLS
model. To resolve heterogeneity in the normalized residuals, we
applied exponential variance structures for basal area and leaf
litter, while an additional square root transformation of the
response variable ensured normality of residuals (verified with
Q-Q plot and Shapiro–Wilkinson normality test: W = 0�96,P = 0�16). After model simplification and removal of one influen-
tial data point, we retained the minimum adequate model. We
calculated an approximate r2-value by comparing the variation in
data explained by the GLS model with that of a null model
(Crawley 2007).
To compare uncorrelated effect sizes of the individual contribu-
tions of correlated balsa attributes to bracken reduction, we calcu-
lated a partial correlation matrix of the standardized covariance
matrix. We tested multivariate normality with a Shapiro–Wilkinson
test for multivariate samples (Looney 1995) and evaluated condi-
tional independence using t-test statistics (Marchetti, Drton &
Sadeghi 2012).
Next, we examined individual relations between balsa perfor-
mance variables and living rhizomes biomass, applying a similar
iterative approach as above and maximizing the restricted log-
likelihood. Additionally, we interpreted the biological meaning of
the curves of predicted model values before deciding whether and
which transformation to apply. Reported model equations are
based on standardized data to help biological interpretation
(Grace & Bollen 2005). We included control plots to evaluate the
contribution of different bracken cutting intensities to bracken
control in plots with no balsa trees.
We used ANOVA to evaluate the impact of cutting frequencies
and balsa establishment methods on bracken rhizome biomass.
Mixed models and ANCOVA were discarded using the same itera-
tive decision-making process described previously. Factor levels
without in-between significant differences were merged to
improve model fit and coefficient estimation. We ordered the dif-
ferent management treatments based upon Tukey honest signifi-
cant differences with 95% confidence intervals. All analyses were
performed in R, version 2.14.1 (R Development Core Team
2011) with associated packages ggm (Marchetti, Drton & Sadeghi
2012), ggplot2 (Wickham 2009a), gridExtra (Auguie 2012), nlme
(Pinheiro et al. 2011), mvnromtest (Jarek 2012), plyr (Wickham
2009b) and reshape (Wickham 2007).
Results
BALSA PERFORMANCE AND BRACKEN CONTROL
All balsa attributes correlated significantly with biomass
of living bracken rhizomes (Fig. 1), and our overall model
explains 87% of the observed variation (see Table S1,
Supporting Information). Also bracken frond biomass
(r2 = �0�70; P < 0�001; F1,46 = 106�6) and frond cover
(r2 = �0�81; P < 0�001, F1,46 = 201�6) correlated nega-
tively with balsa basal area. We observed only dead rhi-
zomes and fronds in plots with balsa basal areas above
11 m2 ha�1, with the exception of two plots that had less
than 80 g m�2 of living, but clearly exhausted rhizomes
(Fig. 1a). In the same plots, mean above-ground bracken
cover dropped in 18 months from 100 � 0% to 17 � 15%,
corresponding to 256 � 292 g m�2 of mainly dehydrated
and dead fronds. By contrast, in plots with lower balsa per-
formance (basal area <10 m2 ha�1), living rhizomes
remained abundant (2995 � 1576 g m�2), maintaining
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
Using succession for complete bracken elimination 1259
5728 g m�2of living frond biomass on average and covering
91 � 21% of plot surface areas.
Threshold values for complete bracken elimination were
less straightforward for light intensity or balsa leaf litter
(Fig. 1b,c). However, living bracken rhizomes tended to
completely disappear in intensely shaded plots (<500 lmol
m�2 s�1) and plots containing more than 80 g m�2 of
balsa leaf litter on average. Not surprisingly, all balsa
performance variables were correlated, and plots with
increasing balsa basal area had stronger understorey
shade and accumulated more leaf litter (Fig. 2). Indepen-
dent effect size of balsa basal area on living bracken rhi-
zome biomass was twice as high as for balsa leaf litter or
understorey light intensity, which yielded comparable
effect sizes (Table 1).
MANAGEMENT METHODS
Bracken rhizome biomass varied significantly between dif-
ferent combinations of balsa establishment methods, cut-
ting frequencies and their interactions, whereas the
control treatments (without balsa) held significantly higher
levels of rhizome biomass under all cutting frequencies
0
2000
4000
6000
8000ln(y) = −0·88 x
r2 = 0·77
(a)
(b)
(c)
0 5 10 15 20 25
Balsa basal area (m2 ha−1)
0
2000
4000
6000
8000sqrt(y) = 0·84 x
0 500 1000 1500 2000 2500
PAR (µmol m−2 s−1)
0
2000
4000
6000
8000sqrt(y) = −4·18 sqrt(x)
0 50 100 150 200 250
Balsa leaf litter (g m−2)
Livi
ng b
rack
en r
hizo
mes
(g
m−
2 )
r2 = 0·63
r2 = 0·79
Fig. 1. Univariate regressions of living bracken rhizome biomass
vs. (a) balsa basal area (F1,45 = 172�3); (b) understorey light intensity(measured as photosynthetically active radiation) (F1,45 = 78�04);and (c) balsa leaf litter biomass (F1,45 = 175�2). All points corre-
spond to plot-averaged values sampled in 18-month-old balsa
stands. The red line and shaded zone represent back-transformed fit-
ted values and 95% confidence intervals, respectively. All models
and coefficients are significant at a 5% level. Equations are based on
standardized data centred on the mean. Shade projected by over-
hanging trees of adjacent plots produced the outlier in the extreme
left part of (b). The same overhanging trees also deposited litter in
plots with low values of balsa basal area, explaining the outliers on
the right hand side of (c).
0
100
200
300 y = 0·85 ln(x)
r2 = 0·56B
alsa
leaf
litte
r (g
m−
2 )
0
500
1000
1500
2000
2500
ln(y) = −0·65 ln(x)
0 5 10 15 20 25
0 5 10 15 20 25
Balsa basal area (m2 ha−1)
PA
R (
µmol
m−
2 s−
1 )(a)
(b)
r2 = 0·4
Fig. 2. Univariate regressions of plot-averaged basal area of
18-month-old balsa stands vs. (a) balsa leaf litter biomass
(F1,34 = 43�32); (b) understorey light intensity (photosynthetically
active radiation), where higher values represent higher light inten-
sity (F1,33 = 22�01.). The red line and shaded zone represent back-
transformed fitted values and 95% confidence interval of the
model, respectively. All models and coefficients are significant at
a 0�01% level. Equations are based on standardized data centred
on the mean.
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
1260 D. Douterlungne, E. Thomas & S.I. Levy-Tacher
(S2). Biweekly and monthly cutting frequencies during the
first six months did not result in differences in living
bracken rhizome biomasses regardless of the balsa estab-
lishment method used (Fig. 3).
Discussion
ECOLOGICAL TRAITS UNDERLYING BRACKEN
CONTROL
As opposed to other studies where complete bracken
eradication by above-ground treatments was considered
unrealistic or even impossible (Pienkowski et al. 1998;
Roos, R€odel & Beck 2011), our 18-months-old balsa
stands completely out-competed the 30-year-old bracken
vegetation in plots with basal areas above 11 m² ha�1.
Several ecological traits underlie balsa’s potential to
weaken bracken’s competitive dominance. Of the three
measured balsa attributes, basal area presented the largest
independent effect on bracken reduction, suggesting a
strong competitive effect for available light, water and soil
nutrients. Balsa is one of the fastest growing pioneer trees
in the lowland Neotropics, and its canopy rapidly over-
tops aggressively competing heliophytes. Ochroma yielded
the highest growth volumes out of more than 70 tested
species on degraded lands in Costa Rica (Butterfield
1996). In our bracken land, one-year-old balsa trees
reached mean heights of over six metres and closed their
canopies (Douterlungne et al. 2010).
In the tropics, reduced light intensity alters bracken’s
balance between stored rhizome carbohydrates and newly
assimilated frond photosynthates (Le Duc, Pakeman &
Marrs 2003). Light competition as a bracken control
mechanism has been suggested, but can be costly without
guaranteeing success (Walker & Boneta 1995; Humphrey
& Swaine 1997; Gaudio et al. 2011). Also in our plots,
light competition alone was not sufficient for complete
bracken control, as demonstrated by partial correlation
analysis. Furthermore, bracken persisted in most plots
with low balsa basal area, despite their relatively low light
intensities compared with control plots. In Ecuador,
Roos, R€odel & Beck (2011) were unable to completely
eradicate bracken after a combination of cutting and cover-
ing vegetation with black plastic sheets during almost two
years, exposing it not only to strong shade, but also water
and heat stress. Similarly, bracken biomass remained con-
stant after reducing incoming sunlight with an 80% black
nylon mesh for one year at a site nearby the current experi-
ment (Pe~naolsa-Guerrero 2008).
Table 1. Partial correlation matrix of living bracken rhizome bio-
mass and balsa attributes. Values express the expected change in
a dependent variable associated with one standard deviation
change in a given predictor while controlling for the correlated
effects of other predictor variables, similar to path- or structural-
ized equation analysis. All pairwise comparisons fulfil conditional
independence at 0�001 confidence levels (t-tests; d.f. = 43)
Balsa
basal
area
Understorey
light intensity
Balsa
leaf
litter
Bracken
rhizomes
Balsa basal
area
1�000 �0�114 0�169 �0�591
Understorey
light
intensity
1�000 �0�403 0�241
Balsa leaf
litter
1�000 �0�296
Bracken
rhizomes
1�000
Control Seeds Traditional Seedlings
0
2000
4000
6000 a aa a bb a bb a bb
0 1 2 0 1 2 0 1 2 0 1 2
Monthly bracken cutting events
Livi
ng b
rack
en r
hizo
mes
(g
m−
2 )
Fig. 3. Differences in living bracken rhizomes due to different bracken cutting frequencies and balsa establishment methods (sampled
18 months after experiment set-up). Panels refer to different balsa establishment methods; Control: without balsa trees; Seeds: manually
introducing seeds in the ground; Traditional: manually broadcasting large quantities of seeds; and Seedlings: transplantation of nursery
seedlings. All plots were cleared from all above-ground vegetation before experimental set-up. Different letters indicate significantly dif-
ferent bracken cutting treatment means within each balsa establishment method (post hoc Tukey test with a 95% confidence interval).
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
Using succession for complete bracken elimination 1261
Balsa leaf litter demonstrated a similar independent effect
size as understorey shade. Leaf laminas can be extremely
large in young balsa individuals (0�429 � 0�070 m2, n = 50,
Douterlungne 2005), and leaf litter accumulates rapidly and
abundantly under young balsa stands (Diemont et al.
2006), blocking incoming light at ground level and possibly
obstructing the development of young emerging fronds
(Fig. 4). Probably, the combination of an extremely rapid
growth and a high production and turnover rate of big leafs
contributes to balsa’s ability to successfully out-compete
bracken.
Cutting of fronds clearly has a negative impact on
bracken performance. However, cutting alone was insuffi-
cient to eliminate bracken in our experiment, as none of
the cutting frequencies suppressed bracken in our control
plots. In British heathlands, Marrs, Johnson & Duc
(1998a) cut fronds of P. aquilinum every six months dur-
ing 18 consecutive years and suppressed bracken effec-
tively during the first years but failed to further reduce
and permanently eradicate the fern. Their results of
shorter cutting treatments suggest also bracken regrowth
in the long term. Le Duc, Pakeman & Marrs (2003) com-
pared the results of several British bracken control experi-
ments and concluded that cutting bracken twice a year
was the most successful treatment. However, they consid-
ered it to be ineffective in highly productive bracken
lands, such as tropical lowland bracken with an all-year
growth season. In Ecuador, the most successful treatment
out of series of tested strategies consisted of six consecu-
tive cutting events of P. arachnoideum, reducing its above-
ground fresh weight to c. 30% of reference levels (Roos,
R€odel & Beck 2011). All mentioned studies failed to con-
trol bracken completely but recommend bracken cutting
in combination with follow-up treatments, such as the
establishment of a closed forest canopy.
LONG-TERM BRACKEN ELIMINATION AND
SUCCESSIONAL PATHWAYS
Conventional invasive species control methods based on
damaging plant tissue such as through cutting or burning,
or applying herbicides often result in reinvasion of the
target species, or colonization by novel invasive plants,
jeopardizing return on investment (Kettenring & Adams
2011). In the UK, bracken recolonized sites 10 (Pakeman
et al. 2000) to 18 years (Marrs et al. 2000) after control
treatments. In contrast, under shaded balsa canopies,
recolonization by bracken is very unlikely in the absence
of living rhizomes, while leaf litter covering the soil pre-
vents new spores from germinating (Gliessman 1978;
Walker & Boneta 1995).
Initiating natural successional processes, such as the
ecological interactions under our balsa stands, can be
expected to be more effective to achieve long-term
bracken control and in general to unblock arrested suc-
cessional pathways in degraded lands (Marrs et al. 2000;
Slocum et al. 2006). The impact of artificial interventions
may on the contrary cease or even be reversed once the
intervention ends. Although natural succession may not
always be a desired outcome after bracken elimination
and most conventional control methods often constrain
forest succession (Pakeman et al. 2000). Blocking incom-
ing light, applying chemical substances or removing and
compacting soil with heavy machinery can severely
reduce seed and seedling banks (Ghorbani et al. 2003;
Roos, R€odel & Beck 2011) or deteriorate micro-
conditions for plant growth (Tirada-Corbal�a & Slater
2010). Instead, fast-growing pioneer trees like balsa typi-
cally jumpstart natural succession in clearings (Kammes-
heidt 2000; Van Breugel, Bongers & Mart�ınez-Ramos
2007), reducing even more the physical space, nutrients
and light available for bracken. Three years after balsa
establishment on a corn fallow located at less than 2 km
from our experimental area, recruited tree juveniles
reached an average density of 3�4 stems m�2, representing
51 different species (D. Douterlungne, unpublished data).
Slocum et al. (2006) obtained promising results to control
montane Dicranopteris pectinata fern thickets in the
Dominican Republic by a combination of manually clear-
ing and planting seedlings of woody plants. Three years
after initial clearing, fern cover was reduced to 16%,
while 28% of the planted trees were taller than two
metres, and spontaneously recruited tree juveniles
(>20 cm tall) reached a mean density of 2�3 �1�5 stems m�2 (Slocum et al. 2006). Once bracken or
other aggressive colonizing ferns are suppressed, trees can
be recruited without human intervention. In Sri Lanka,
seedlings of pioneer shrubs and trees were found in
Dicranopteris linearis fernlands after soil disturbance
(Cohen, Singhakumara & Ashton 1995). In Great Britain,
P. aquilinum was cut to increase incoming sunlight for
oak seedlings, which responded with an increase in total
biomass and leaf area (Humphrey & Swaine 1997). Fur-
thermore, Betula pendula and B. pubescens saplings
invaded a 2-m wide pathway cut into dense P. aquilinum
areas, and Pinus silvestris seedlings established in sparse
bracken (Marrs et al. 2000).
BALSA ESTABLISHMENT AND MANAGEMENT
Using balsa to control aggressively dominating species is
not a magic bullet solution and further long-term research
is necessary to fully assess the potential of this method for
large-scale bracken control. Using pioneer plantations to
out-compete bracken requires a successful tree establish-
ment and growth. While balsa thrives on well-drained soils,
it performs poorly in compacted soils such as in recently
abandoned pastures (Douterlungne & Ferguson 2012). Fur-
thermore, prolonged droughts can provoke massive balsa
leaf senescence (D. Douterlungne, personal observation),
resulting in increased light penetration and possible new
emergence of bracken fronds. Therefore, the method may
be less effective at the dry end of balsa’s realized niche
where similar broad-leaved fast-growing pioneer trees could
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
1262 D. Douterlungne, E. Thomas & S.I. Levy-Tacher
be tested as alternative solutions for bracken control.
Slocum et al. (2006) showed that tree growth and survival
rates in fern thickets vary with different environmental con-
ditions. Also, site-specific conditions like proximity of for-
est seeds, presence of remaining isolated trees, the age of
the bracken population, herbivore activity, etc. may affect
the effectiveness of bracken elimination and forest regener-
ation (Marrs, Johnson & Duc 1998b; Marrs et al. 2000).
The method of tree establishment can indirectly affect
the success of bracken control. All tested methods had pros
and cons. Direct seeding ensured efficient use of germ-
plasm, but exposed seeds to seed predators and leaching
out by heavy rains. The traditional method required large
amounts of seeds and resulted in an irregular distribution
of balsa trees with local unshaded patches where bracken
persists as potential re-infestation nuclei. Planting nursery
seedlings was more expensive but ensured higher survival
rates (but not necessarily growth rates). Ninety-two per
cent of transplanted seedlings survived their first growth
year in bracken vegetation without any post-establishment
cutting (Douterlungne et al. 2010).
Ideally, optimal number and frequency of bracken cut-
ting should strike a balance between the cost of treatment
and its effect. The lack of differences in rhizome biomass in
our biweekly and monthly cutting treatments suggest that
there is still margin to further reduce the minimum amount
and frequency of bracken cutting events to achieve least-
effort eradication of P. caudatum. Although cutting clearly
improved establishment and growth of transplanted balsa
seedlings in bracken land (Douterlungne et al. 2010), our
results suggest that bracken could also be controlled with-
out any additional cutting events after successful balsa
establishment; it may only take longer to accomplish. The
fact that bracken rhizome biomass was only slightly lower
in uncut plots with surviving balsa trees as compared to the
control plots is probably explained by the relatively short
time between rhizome sampling and belated balsa canopy
closure. Somewhat surprisingly, uncut control plots con-
tained significantly higher rhizome biomass as uncut plots
with no surviving balsa trees. This can be related to a nucle-
ation effect whereby shade from overhanging branches of
trees in successful plots limits bracken performance in
uncut plots without balsa trees, in spite of the two- to four-
metre wide bufferstrips between our sampling areas. As
control plots were surrounded by healthy untreated
bracken, they are not influenced by possible border effects.
Future experimental set-ups should use broader buffer
zones between sample areas to minimize potential border
effects.
SOCIO-ECONOMIC ASPECTS AND THE IMPORTANCE OF
TRADIT IONAL ECOLOGICAL KNOWLEDGE FOR
ECOLOGICAL RESTORATION
Success probability and adoption rate of ecosystem resto-
ration strategies in rural tropical regions increases when
initial (monetary) investments are kept minimal, and short
or medium-term possibilities for return on investment are
realistic (Aronson, Milton & Blignaut 2007). Establishing
dense balsa stands in post-disturbance conditions is an
affordable practice for contemporary small-scale farmers
in southern Mexico as it is part of the local traditional
swidden agriculture (Nulman, Levy & Montes de Oca
2005; see Douterlungne & Ferguson 2012 for detailed cost
estimation). Investment in follow-up treatments is
expected to be unnecessary after balsa canopy closure and
initiation of natural tree recruitment. Commercial exploi-
tation of balsa wood can provide income and can be com-
bined with swidden cultivation as the tree′s rotation
period of 5–8 years coincides with common fallow periods
(Lamprecht 1989). Furthermore, the recovery of land
suitable for agricultural or agroforestry use can boost
local economies (Turner et al. 2003; Schneider & Goeghe-
gan 2006), whereas alternative sources of income may be
obtained from Payment for Ecosystem Services programs
(Alexander et al. 2011).
Our research highlights the potential of traditional
ecological knowledge (TEK) as an important inspiration
source for efficient forest restoration strategies in rural
(a)
(b)
Fig. 4. Pteridium caudatum control experiment using Ochroma
pyramidale stands in southern Mexico. (a) Four-month-old balsa
stands (back) and regrowth of bracken in control plots (front).
(b) Ten-month-old balsa stands almost completely out-competed
bracken, and balsa leaf litter starts to accumulate.
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
Using succession for complete bracken elimination 1263
areas. In spite of the growing call in literature to incor-
porate local knowledge in the design of reforestation and
restoration programs (e.g. Higgs 2003; Ramakrishnan
2007; Martin et al. 2010), until today, few examples of
their integration in mainstream restoration practice exist.
The fulfilment of local people’s basic needs largely
depends on their ability to sustainably manage or restore
available resources in their living environments. Restora-
tion approaches based on naturally occurring processes
with restoration potential are more likely to be recog-
nized, adopted and adjusted by inhabitants of natural
ecosystems. Future participatory field experiments with
local people should therefore test the usefulness and
applicability of TEK for designing or improving
restoration.
Acknowledgements
The present study was financed by research grants of the Fondo Sectorial
CONACYT-CONAFOR (2005-S0002-14647), the National Institute of
Ecology of Mexico (INE), and the Consejo de Ciencia y Tecnolog�ıa of
Chiapas (CHIS-2006-C06-44603). Special thanks are due to the Lacandon
people of Lacanh�a Chansayab: Manuel Castellanos Chank�ın, his family
and Adolfo Chank�ın for sharing their knowledge, experience and home.
We are grateful to Antonio S�anchez Gonz�alez and Francisco Rom�an
Da~nobeytia for collaboration during fieldwork. We are indebted to Dun-
can Golicher, Bruce Ferguson and Karen Holl for commenting on earlier
drafts of this paper.
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Received 19 December 2012; accepted 19 February 2013
Handling Editor: Quentin Paynter
Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Table S1. Multivariate regression model of balsa attributes con-
tributing to bracken control.
Table S2. Multivariate ANOVA of balsa establishment and bracken
cutting treatments effects on living bracken rhizomes.
© 2013 The Authors. Journal of Applied Ecology © 2013 British Ecological Society, Journal of Applied Ecology, 50, 1257–1265
Using succession for complete bracken elimination 1265