Fast-growing pioneer tree stands as a rapid and effective strategy for bracken elimination in the...

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: [email protected]†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


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.



(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).



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



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.



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.



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