strategies for restoring tree seedling recruitment in high conservation value tropical montane...

Applied Vegetation Science 18 (2015) 121–133

Strategies for restoring tree seedling recruitment inhigh conservation value tropical montane forestsunderplantedwith cardamom

Balram Dhakal, Michelle A. Pinard, I.A.U. Nimal Gunatilleke, C.V. Savitri Gunatilleke &David F.R.P. Burslem

Keywords

Cardamom cultivation; Forest restoration;

Forest understorey cultivation; Knuckles forest;

Natural regeneration; Restoration strategies;

Tree seedlings

Abbreviations

KFR = Knuckles Forest Reserve;

GLMM = generalized linear mixed models;

NMS = non-metric multidimensional scaling

Nomenclature

Dassanayake & Clayton (1997); Dassanayake &

Fosberg (1980)

Received 21 April 2014

Accepted 21 July 2014

Co-ordinating Editor: Martin Hermy

Dhakal, B. (corresponding author,

[email protected]),

Pinard, M.A. ([email protected]) &

Burslem, D.F.R.P. ([email protected]):

Institute of Biological and Environmental

Sciences, University of Aberdeen, Cruickshank

Building, 23 St Machar Drive, Aberdeen, AB24

3UU, UK

Gunatilleke, I.A.U.N. ([email protected]) &

Gunatilleke, C.V.S. ([email protected]):

Department of Botany, University of

Peradeniya, Peradeniya 20400, Sri Lanka

Abstract

Question: What strategies are most appropriate for restoring tree seedling

recruitment whilst avoiding the spread of invasive plant species in high conser-

vation value tropical forests disturbed by planting a shade-demanding crop?

Location: Knuckles Forest Reserve, Sri Lanka (7°210–7°240 N, 80°450–80°480 E).

Methods: An experiment was conducted to test the effects of clipping or

removal of established cardamom plants on recruitment of native tree seedlings

and spread of non-native plants in a tropical montane forest with abandoned

cardamom stands in the understorey. The number and composition of tree seed-

ling emergents, the cover of herbaceous plants and the recovery of cardamom

were assessed for 3 yr.

Results: Tree seedling recruitment was higher in plots from which above-

ground cardamom biomass had been removed through slashing (mean � SE

per 5 m2; 28.9 � 2.70) and those where cardamom plants had been removed

completely through uprooting (32.2 � 3.17), or when dead cardamom leaves

and stems were removedwith small-scale extraction of pods (22.5 � 2.16), than

in unmanipulated control plots (16.6 � 1.13) over 15 mo. The species composi-

tion of tree seedling emergents did not differ in response to removal of carda-

mom. However, the cover of herbaceous plants, including the non-native

invasive Ageratina riparia, increased in response to removal of cardamom.

Recovery of cardamomwas higher when the plants had been slashed thanwhen

entire plants were uprooted and removed.

Conclusion: Slashing or uprooting cardamom plants is a potential strategy for

restoring tree seedling recruitment in forests with abandoned cardamom stands

in the understorey, but these interventions would need to be repeated annually

over many years to be successful, and they risk promoting expansion of the

cover of herbaceous plants, including non-native species. Hence, this approach

would be labour-intensive and costly. An alternative approach to promoting tree

seedling emergence and establishment is to clear dead cardamom leaves and

stems, and to encourage small-scale extraction of pods from the residual carda-

mom plants. Harvesting pods reduces the likelihood that the crop will be sus-

tained in situ through natural regeneration, and supplies an income to local

communities, which would enhance the social acceptability of the intervention.

Introduction

Many tropical forests globally have been underplanted

with shade-demanding cash crops such as cardamom and

coffee (Kumar et al. 1995; Perfecto et al. 1996; Bhagwat

et al. 2008). Cultivation within forests is an important

means of generating income for many communities living

close to forest margins (McNeely & Schroth 2006). How-

ever, the cultivation and management of crops in forests

may involve the selective removal of canopy trees,

121Applied Vegetation ScienceDoi: 10.1111/avsc.12129© 2014 International Association for Vegetation Science

persistent removal of understorey vegetation, including

seedlings and saplings of canopy trees, and fertilizer appli-

cation, which may impact tree regeneration processes

(Ashton et al. 2001; Reyes et al. 2006) andmodify the spe-

cies composition and size structure of the tree community

(Parthasarathy 1999; Ashton et al. 2001; Dhakal et al.

2012). In addition, herbaceous plants including non-native

species may become dominant in response to disturbance

during cultivation and exert negative effects on tree seed-

lings (Aide et al. 1995; Hall et al. 2011). When the planta-

tions are abandoned, the residual agricultural crop,

together with disturbance-responsive understorey plants,

may compete with tree seedlings for resources such as soil

moisture, nutrients and light, and thus hinder tree seedling

establishment (Aide et al. 1995; Holl et al. 2000; Zimmer-

man et al. 2000; Slocum et al. 2006; G�omez-Aparicio

2009). Consequently, forests may fail to recover naturally

(Aide et al. 2000), and interventions to restore regenera-

tion processes then become necessary (Lamb et al. 2005).

However, detailed studies on techniques for restoring for-

ests disturbed through cultivation of understorey crops are

lacking, despite a major focus on restoration of abandoned

deforested lands and pastures (Aide et al. 1995; Hooper

et al. 2005; Slocum et al. 2006; Holl et al. 2011). A sound

understanding of the constraints to tree seedling recruit-

ment in these human-modified forests is critical for devis-

ing management options that will enhance forest

conservation and the sustained delivery of ecosystem ser-

vices.

Removal of shrubs, herbs and lianas has been shown to

enhance the regeneration of tree species in many diverse

contexts (Hartman & McCarthy 2004; Royo & Carson

2006; Minden et al. 2010; Kettenring & Adams 2011). For

example, removal of the fern Dicranopteris pectinata Willd

enhanced tree seedling regeneration in a degraded forest

in the Dominican Republic (Slocum et al. 2004, 2006),

and clearance of the shrub Acanthus pubescens Thomson ex

Oliv. increased growth of planted tree seedlings in a logged

forest in Uganda (Duclos et al. 2013). By analogy, it can be

postulated that removal of the relict crop from a forest un-

derstorey may facilitate natural regeneration of the resid-

ual tree community. The simplest method of removal

would be slashing or uprooting the crop to release emer-

gent tree seedlings from competition for light, soil moisture

and nutrients. In addition, the soil disturbance associated

with uprooting the cropmay further enhance regeneration

by burying recently dispersed seeds, to protect them from

surface-active predators and pathogens, and to unearth

seeds that are buried beyond the reach of germination trig-

gers (Pearson et al. 2003; Gallery et al. 2007). The addition

of the trash obtained from slashing and uprooting the crop

may contribute to a substantial pool of organic matter or

nutrients on the forest floor and/or create a physical

barrier to seedling emergence, but no data are available to

evaluate these components of the intervention.

Removal of a residual abandoned crop from a forest un-

derstorey may trigger tree seedling recruitment, but only if

the recovery of the crop is kept in check. Crop plants may

recover by germination of seeds buried in the soil or by re-

sprouting from stumps. In addition, soil disturbance and

increased light availability, which are consequences of the

intervention, may provide opportunities for non-native

species to colonize or spread (Pascarella et al. 2000), as

many such species preferentially colonize disturbed sites

(Bellingham et al. 2005). In turn, colonization by

non-native species may result in profound changes to the

understorey vegetation. Therefore the assessment of strate-

gies for restoring tree seedling recruitment requires a con-

sideration of these wider impacts on development of the

forest understorey community after manipulations that

eliminate the abandoned residual crop.

In this study we established an experiment to examine

strategies to restore recruitment of tree seedlings in a high

conservation value tropical montane forest in Sri Lanka

that is affected by long-term cultivation, followed by plan-

tation abandonment, of the high-value, shade-tolerant

perennial spice crop, cardamom (Elettaria cardamomum

L. Maton). We hypothesized that the abandoned stands of

cardamom would impose barriers to tree regeneration and

therefore that removal of cardamom would restore tree

regeneration. The following specific questions were

addressed.

1. Does the active removal of entire cardamom plants,

and/or just above-ground leaf and stem material, enhance

the number of tree seedling emergents?

2. Does removal of cardamom biomass change the species

composition of emergent woody plant seedlings?

3. Does the recovery of cardamom and/or colonization by

other herbaceous plants increase in response to removal of

cardamom biomass and emerge as potential barriers to tree

seedling recruitment inmanipulated stands?

Methods

Study site

This study was conducted from January 2008 to June 2011

in the Knuckles Forest Reserve (KFR) of central Sri Lanka

(7°210–7°240 N, 80°450–80°480 E; Balasubramaniam 1988;

Appendix S1a). The KFR extends over an area of

21,000 ha and contains a range of natural vegetation types

as well as patches of human-induced grasslands, areas of

shifting cultivation and plantations of Pinus caribaea Mor-

elet (IUCN 1994). It is floristically very rich and also serves

as an important watershed, providing water for irrigation

and hydropower generation. The study site was located in

lower montane rain forest at 1032–1274 m a.s.l. close to

Applied Vegetation Science122 Doi: 10.1111/avsc.12129© 2014 International Association for Vegetation Science

Restoration strategies for cardamom plantations B. Dhakal et al.

Riverston (7°310 N, 80°440 E) in the northeastern part of

KFR. The 10-yr average annual rainfall at the study site is

3381 mm and the mean monthly temperature is 18–26 °C(MSP 2009). The most abundant tree species in natural

lower montane forests are Calophyllum spp., Hortonia flori-

bunda Wight ex Arn., Ilex walkeri Wight, Macaranga indica

Wight andMaesa indica Roxb. (Dhakal 2011).

Cardamom (Zingiberaceae) is a perennial herbaceous

crop bearing a pseudo-stem that extends up to 2–3-m in

height, with pods (harvested as a spice) at ground level

(Appendix S1b). It grows in a cool and humid climate and

has a productive life of 10–15 yr (Dhakal 2011). Official

records show that about 3000 ha of forest in KFR have

been cultivated with cardamom (IUCN 1994). However,

during 3 yr of fieldwork in the KFR we observed very little

natural forest without planted cardamom; hence this fig-

ure is likely to be a significant underestimate of the total

area under cultivation. Cardamom cultivation in the

greater part of the KFR, including our study sites, started

more than a century ago (Gurusinghe 1988) and contin-

ued until 1985. After that, managed plantations were

abandoned because the area was incorporated within the

Knuckles Conservation Area (17500 ha), which has pro-

tected status that prohibits cardamom cultivation (IUCN

1994). The KFR is now part of the Central Highlands of Sri

Lanka World Heritage Site, and there is current interest in

developing management interventions to enhance the

conservation value of forests underplanted with carda-

mom in the past.

Plot establishment and experimental manipulations

In order to examine the options for restoring tree regenera-

tion, an experiment was established in March 2008 in

eight blocks of land possessing forests with abandoned car-

damom. Mean (�SE) density of cardamom plants in these

abandoned plantations was 6098 � 500 ha�1 and the

basal area of trees (≥5 cm DBH) was 30.8 � 3.20 m2 ha�1

(Dhakal et al. 2012). In each block, six 10-m 9 10-m plots

were established in random locations but separated by a

minimum distance of 4 m (Appendix S1c) to accommo-

date the following treatments: (1) cardamom stems cut/

slashed at ground level and removed from the plots (SL);

(2) cardamom stems cut at ground level and cardamom

biomass (trash) placed uniformly across the cleared plots

(ST); (3) cardamom stems uprooted and removed entirely

from the plots (UP); (4) cardamom stems uprooted and

cardamom biomass (trash) placed uniformly across the

cleared plots (UT); (5) plots managed by removal of dead

cardamom stems and leaves (cleaning) every 3 mo and

pods harvested every 3 mo according to conventional

methods for the area (CL); and (6) abandoned cardamom

stands retained in an unmanipulated state (AB). The treat-

ments were allocated randomly to the plots within each

block.

Before the treatments were applied, the DBH of trees

≥5 cm on all plots was measured and all trees were identi-

fied by comparison with voucher specimens in the

National Herbarium at Peradeniya (PDA). One 1-m 9 5-m

seedling emergence quadrat was then established in a

random location in each 5-m 9 5-m quadrat of all

10-m 9 10-m plots in the study (total 192 seedling quad-

rats). Experimental treatments were imposed in March

2008 and seedlings were censused fortnightly in each seed-

ling emergence quadrat between April 2008 and June

2009. All newly emerged seedlings were tagged, given a

unique number and identified to morphotype. A photo-

graph of each new seedling was taken to establish a refer-

ence digital archive. For all morphotypes, specimens were

collected from outside the experimental plots and voucher

specimens were identified with the assistance of botanists

at the University of Peradeniya and by reference to

specimens in the National Herbarium (PDA). The extent of

cardamom recovery, i.e., new cardamom seedlings on all

plots and sprouts from cut stems and rhizomes that had

been dug up and then left in situ on plots fromwhich stems

had been slashed or uprooted, was measured in each seed-

ling emergence quadrat in March 2009, 1 yr after the

treatments had been applied. All new cardamom plants in

the plots were then removed by slashing or uprooting

immediately after completing this enumeration.

In March 2009 the cover of all live herbs (<1-m tall),

including new cardamom plants, was measured in each

seedling emergence quadrat using a 20-cm 9 50-cm

frame. Each plot was divided into five 1 m 9 1 m sections

and cover was measured in ten 20-cm 9 50-cm sub-quad-

rats in each section. After manipulation, the non-native

species Ageratina riparia (Regel) R. M. King & H. Rob.

(native to Mexico and Central America), an aggressive

invader of forest understorey environments, started to

colonize some plots. Therefore, the percentage of the

A. riparia cover was estimated separately in the plots using

the same procedure. In February 2009, a hemispherical

photograph was taken at the centre of each seedling

emergence plot at seedling height (15-cm) using a Nikon

Coolpix 995 camera and FC-E8 0.21 9 Nikon fisheye lens

(Nikon Corp., Tokyo, Japan).

In June 2011, 39 and 27 mo after the first and second

applications of experimental cardamom removal treat-

ments, respectively, the number and height of all living

seedlings (both those from the inventories in 2008/9 and

the new recruits establishing during the interval 2009–

2011) were recorded in each seedling emergence quadrat.

The extent of cardamom recovery was measured in each

seedling emergence quadrat on plots exposed to cardamom

removal treatments in 2009, although it was not possible


B. Dhakal et al. Restoration strategies for cardamomplantations

to distinguish new seedlings from re-sprouts on this occa-

sion. The cover of herbaceous plants and A. riparia were

estimated separately by implementing the same proce-

dures as in previous inventories.

Data analysis

To account for the nesting of plots within blocks of the car-

damom plantation, generalized linear mixed models

(GLMM) implemented using the glmmPQL function in the

MASS package (Venables & Ripley 2002) of R v. 1.11.1 (R

Foundation for Statistical Computing, Vienna, AT) were

used to analyse seedling emergence (cumulative over

15 mo and final densities at the 2009 and 2011 censuses),

herbaceous plant cover, A. riparia cover and cardamom

recovery data. Graphical methods were used to assess how

well the models fit the data.

Cumulative counts of seedlings emergence over 15 mo

(April 2008–June 2009) were obtained by summing across

the four 5 m2 seedling emergence quadrats nested in each

plot. Two models were fitted to data on counts of seedling

emergence in the experimental treatments with treatment

considered a fixed effect, and plot nested within block and

blocks as random effects. In the first model, seedling counts

were compared among four treatments i.e. plots in unma-

nipulated abandoned cardamom plantation (AB), plots in

which cardamom stands were cleaned through removal of

dead cardamom stems and leaves (CL), and plots in which

all cardamom biomass had been removed to ground level

by slashing (SL) or removed entirely by uprooting (UP),

with removal of the cardamom trash in both cases. The

model was initially fitted with treatment AB (unmanipu-

lated cardamom plantation) as a baseline to generate con-

trasts with the three other treatments, and then the order

of terms was switched and the model refitted in order to

generate all possible pair-wise contrasts among treatments

(Table 1). The second model fitted data on counts of seed-

ling emergence to the factorial combination of cardamom

removal treatments (slashing vs uprooting) and fate of

dead cardamom plant material after manipulation

(removal vs retention on plots) using a two-way structure

that included the interaction of these factors.

The final density (per quadrat) of seedlings at the cen-

suses in 2009 and 2011, the recovery of cardamom (seed-

lings and sprouts separately) in 2009, the cover of

herbaceous plants in 2009 and 2011 and the mean height

of seedlings per seedling emergence plot were analysed

using analogous models with appropriate probability

Table 1. Summary of the output of GLMM models comparing densities of emerged woody plant seedlings across treatment plots in 2009 and 2011 in

Knuckles Forest Reserve, Sri Lanka. The treatments in the experiment were: abandoned cardamom stands retained in an unmanipulated state (AB); plots

managed by removal of dead cardamom stems/cleaning and removal of pods (CL); cardamom stems were slashed at ground level and removed (SL); carda-

mom stems were slashed at ground level and cardamom trash placed uniformly across the plots (ST); cardamom stems were uprooted and removed

entirely from the plots (UP); cardamom stems were uprooted and cardamom trash placed uniformly across the plots (UT). In Model 2, data were combined

to test the two-way interaction between treatments with removal (SL + UP) or retention (ST + UT) of trash and slashing (SL + ST) or uprooting (UP and UT).

In all models, treatment was considered a fixed effect, and plots nested within blocks and blocks as random effects.

Model terms Contrasts df Cumulative number of

seedlings

Densities of seedlings

in 2009

Densities of seedlings

in 2011

Coefficients P Coefficients P Coefficients P

Model 1: AB vs CL, SL, UP Intercept 99 2.81 <0.01 3.71 <0.01 2.01 <0.01

Treatment AB vs CL 22 0.29 0.11 0.17 0.43 0.17 0.26

Treatment AB vs SL 22 0.53 <0.01 0.22 0.14 0.05 0.74

Treatment AB vs UP 22 0.64 <0.01 3.01 <0.01 �0.04 0.81

Model 1: CL vs AB, SL, UP Intercept 99 3.09 <0.01 1.79 <0.01 2.19 <0.01

Treatment CL vs AB 22 0.29 0.11 �0.79 0.43 �0.13 0.26

Treatment CL vs SL 22 0.24 0.16 0.11 0.48 �0.12 0.41

Treatment CL vs UP 22 0.35 0.04 0.59 0.01 �0.21 0.18

Model 1: SL vs AB, CL, UP Intercept 99 3.34 <0.01 2.25 <0.01 2.07 <0.01

Treatment SL vs AB 22 �0.53 0.01 �0.26 0.14 �0.01 0.94

Treatment SL vs CL 22 �0.23 0.16 �0.12 0.48 0.12 0.43

Treatment SL vs UP 22 0.11 0.49 0.34 0.06 �0.09 0.57

Model 1: UP vs AB, CL, SL Intercept 99 3.44 <0.01 2.59 <0.01 1.97 <0.01

Treatment UP vs AB 22 �0.64 <0.01 �0.59 <0.01 0.08 0.63

Treatment UP vs CL 22 �0.35 0.04 �0.46 0.01 0.21 0.19

Treatment UP vs SL 22 �0.11 0.49 �0.39 0.06 0.09 0.57

Model 2: Removed vs retained +

Uprooted vs slashed +

two-way interaction

Intercept 96 3.39 <0.01 4.11 <0.01 1.91 <0.01

Removed vs retained (Rr) 21 �0.06 0.29 0.31 0.26 0.22 0.29

Uprooted vs slashed (Us) 21 �0.04 0.45 �0.07 0.60 0.15 0.45

Rr 9 Us 21 0.17 0.27 0.03 0.59 �0.32 0.27



distributions. The survival of seedlings (the seedlings that

were tagged during 2009 and survived until the 2011 cen-

sus) at the plot level was analysed using glmmPQL models

with a binary response variable (survived vs died) follow-

ing Crawley (2008). To account for the large number of

zero records in the cardamom recovery and A. riparia

cover data in 2011, zero-inflated models were imple-

mented using the zeroinf1 function in the pscl package of

R (Zuur et al. 2009). The associations among densities of

tree seedlings, new cardamom seedlings, cardamom re-

sprouts and cover of all herbaceous plants and A. riparia

were analysed separately using Pearson’s product moment

correlation coefficients.

Hemispherical photographs were analysed using the

software Winphot 5.0 (ter Steege 1996) to determine a

value of canopy openness for each plot. Canopy openness

was assessed among treatments using glmmPQL models,

withmean percentage of canopy openness in each plot cal-

culated from the canopy openness measured in each seed-

ling emergence plot as a response variable, but differences

in canopy openness among plots and the effect of introduc-

ing canopy openness as an additional covariate in GLMM

models were non-significant. The relationships between

canopy openness, and herbaceous growth and seedling

density per quadrat were examined using the Pearson’s

product moment correlation coefficient. The patterns of

seedling community composition and its association with

canopy openness were visualised using non-metric multi-

dimensional scaling (NMS) using the software PC-ORD 5

(McCune & Grace 2002). The NMS ordinations were con-

ducted using the Sørensen distance measure with 50 runs

of real data and 50 runs of randomized data to generate a

Monte Carlo test of significance (McCune & Grace 2002).

Random starting configurations were used with a maxi-

mum of 200 iterations for each run. A three-dimensional

solution was chosen for the final iterative ordination, and

the best end point in the preliminary analysis was used as

the starting point in the final run. In order to reduce the

‘noise’ from infrequent species, species that were observed

only once or twice were excluded from the NMS analysis.

Results

Effect of cardamom eradication treatments onwoody

plant seedling recruitment and species composition

The manipulations imposed on the treated plots in aban-

doned cardamom plantations generally increased seedling

emergence of woody plants over 15 mo relative to unma-

nipulated plots (Fig. 1a, Table 1). Cumulative emergence

of seedlings over 15 mo from which just dead cardamom

stems and leaves had been removed (CL) was not differ-

ent, but was significantly higher on plots where the carda-

mom plants had been cleared to ground level (SL; +74%)

or uprooted and removed entirely (UP; +93%) than on

unmanipulated plots (AB). However, the cumulative

number of seedlings was not different in the plots where

cardamom stems were cleaned and the plots where carda-

mom stems were removed either by slashing or uprooting.

There was no difference between the treatments that

removed just the above-ground cardamom biomass (SL)

or the entire plants (UP), and no effect of adding (ST and

UT) or removing (SL and UP) the cardamom trash in the

plots, on cumulative emergence of seedlings over 15 mo

(Fig. 1a, Table 1). A similar pattern of response to treat-

ments was obtained for seedling density on plots in 2009,

except that in this case clearing the above-ground carda-

mom biomass alone had no effect on seedling density,

whereas uprooting the entire cardamom plants increased

mean seedling density by 10% relative to the unmanipu-

lated control plots (Fig. 1b). By the time of the census in

June 2011, 27 mo after the last application of cardamom

removal treatments, differences in the density of seedlings

among treatments had disappeared (Fig. 1b). This equal-

ization of mean density of seedlings among treatments

between the censuses in 2009 and 2011 occurred because

percentage seedling survival during this interval was sig-

nificantly lower in response to the removal of cardamom

above-ground biomass (mean � SE per 5 m2 plot:

14 � 0.6%) or entire plants (8.0 � 2.3%) than on the

unmanipulated control plots (16 � 2.1%; Appendix S6).

Mean seedling height did not differ among treatments in

either 2009 or 2011 (Appendix S6).

A total of 664 live seedlings were recorded in the plots

during the census in June 2009, with 83% (53 out of 64)

of morphotypes identified to species (Appendix S2). A total

of 1531 seedlings were recorded on the plots at the final

census in June 2011, and 86% (56 out of 65) of the mor-

photypes were identified to species (Appendix S2). Ordina-

tion with NMS of the communities of seedling emergents

suggested that removal of cardamom did not affect species

composition in either 2009 or 2011 (Appendix S3a,b). Glo-

chidion coriaceum and Rauvolfia densiflora (in 2009) and Psy-

chotria nigra and R. densiflora (in 2011) were the most

abundant germinants, although Actinodaphne elegans and

Symplocos cochinchinensis were the common species of over-

storey trees ≥5 cmDBH on the plots (Table 2a,b).

Cover of herbaceous plants and Ageratina riparia after

experimental cardamommanipulations

The cover of herbaceous plants in March 2009, 1 yr after

treatments were first applied, was lower on plots that had

been treated by removal of dead cardamom stems and

leaves than on plots of the unmanipulated control treat-

ment. However, mean cover of herbaceous plants was

higher by 16% and 20%, respectively, on plots where the



cardamom had been cleared to ground level or removed

entirely than on plots that had not been manipulated

(Fig. 2a, Appendix S4). Cover of herbaceous plants did not

differ between the two types of cardamom removal treat-

ment nor in response to the removal or return of the carda-

mom trash to the plots (Fig. 2a). By June 2011, the cover

of herbaceous plants had equalized across all treatments

(Fig. 2a). The cover of herbaceous plants in March 2009

was positively correlated with seedling density

(r [n = 190] = 0.41, P < 0.01), and canopy openness

(r [n = 190] = 0.21, P = 0.04), but in June 2011 herba-

ceous plant cover was not correlated with seedling density

(r [n = 190] = 0.17, P = 0.36) or the density of new

cardamom plants on plots where they had previously been

removed (r [n = 126] = �0.10, P = 0.59).

The cover of Ageratina ripariawas highly variable within

and among treatments at the censuses in 2009 and 2011

(Fig. 2b). Generalized linear mixed models on the data

from March 2009 failed to detect consistent differences

among treatments (Appendix S4), while zero-inflated

models fitted to the data from June 2011 to account for the

high frequency of zero counts in the data set suggested that

A. riparia cover did differ among treatments. Inspection of

mean values suggests that removal of entire cardamom

0

5

10

15

20

25

30

35

40

AB CL SL ST UP UT

Mea

n cu

mul

ativ

e num

ber o

f se

edlin

gs p

er(5

m2 )

seed

ling

emer

genc

e pl

ot

Treatments over 15 mo

0

5

10

15

20

AB CL SL ST UP UT AB CL SL ST UP UT

2009 2011

Mea

n se

edlin

g de

nsity

per

(5 m

2 ) se

edlin

g em

erge

nce p

lot

Treatments in two census periods

b

b

b

ab

aa

a

ab

(a)

(b)

Fig. 1. Mean � SE (a) cumulative number of tree seedlings that emerged over the first 15 mo following the establishment of the experiment, and (b)

mean tree seedling density per 5-m2 quadrat in June 2009 and June 2011 in a montane forest in Knuckles Forest Reserve, Sri Lanka. Cardamom stands were

either abandoned and retained in an unmanipulated state (AB); managed by removal of dead cardamom stems/cleaned (CL); slashed at ground level and

cardamom trash removed (SL); slashed at ground level and cardamom trash placed uniformly across the plots (ST); cardamom stems uprooted and

removed entirely from the plots (UP); or cardamom stems uprooted and cardamom trash placed uniformly across the plots (UT). Lowercase letters denote

significant (P < 0.05) differences among treatments AB, CL, SL and UP (1a and 1b in 2009); treatments ST and UT were not significantly different from SL

and UP for total cumulative emergence or density of seedlings in 2009, and no plots differed among treatments in 2011 for 1b (Table 1).



plants by uprooting stimulated an increase in A. riparia

cover, although variance among plots of this treatment

remains high (Fig. 2). There was no evidence that return-

ing the cardamom trash to the plots after slashing or

uprooting influenced A. riparia cover. Ageratina riparia

cover in March 2009 was not correlated with seedling

density (r [n = 190] = 0.03, P = 0.68), but was positively

correlated with the cover of other herbaceous plants

(r [n = 190] = 0.30, P < 0.01) and canopy openness

(r [n = 190] = 0.49, P < 0.01). In June 2011, A. riparia

cover was negatively correlated with woody plant seedling

density (r [n = 190] = �0.61, P < 0.01), but positively

correlated with the cover of other herbaceous plants

(r [n = 190] = 0.51, P < 0.01) and canopy openness

(r [n = 190] = 0.49, P < 0.01).

Cardamom recovery after manipulation

The mean density (�SE) of cardamom stems per

10-m 9 10-m plot at the time the experiment was estab-

lished in the abandoned cardamom plantation was 65 � 9

plot�1. The density of new cardamom seedlings in March

2009was about 300% and 800%higher in plots where the

cardamom had been cleared to ground level and uprooted,

respectively, than in plots of the unmanipulated control

treatment, while removing just dead cardamom leaves and

Table 2. Relative abundance of the ten most abundant species of: (a) seedling emergents, expressed as percentage of all seedlings in 2009 (total germi-

nants = 664) and 2011 (total germinants = 1531), and (b) overstorey species (individuals ≥5 cm DBH in 2009; total number = 486) expressed as a percent-

age of all trees on experimental plots in montane forest underplanted with cardamom in Knuckles Forest Reserve, Sri Lanka.

Family Species Life form Percentage of

total germinants

(a) Seedling emergents

2009

Euphorbiaceae Glochidion coriaceum Tree 9.0

Apocynaceae Rauvolfia densiflora Tree 7.2

Rubiaceae Psychotria nigra Shrub 7.2

Chloranthaceae Sarcandra chloranthoides Shrub 6.0

Rutaceae Acronychia pedunculata Tree 4.8

Unknown Unknown sp. Unknown 4.7

Euphorbiaceae Macaranga peltata Tree 3.3

Euphorbiaceae Macaranga indica Tree 3.0

Symplocaceae Symplocos cochinchinensis Tree 2.9

Myrtaceae Syzygium fergusoni Tree 2.9

2011

Rubiaceae Psychotria nigra Shrub 26.0

Apocynaceae Rauvolfia densiflora Tree 12.6

Chloranthaceae Sarcandra chloranthoides Shrub 7.4



Myrtaceae Syzygium fergusoni Tree 3.4

Rutaceae Acronychia pedunculata Tree 3.3

Euphorbiaceae Glochidion coriaceum Tree 2.7

Myrsinaceae Ardisia gardneri Tree 2.6

Myrsinaceae Maesa indica Tree 2.5

Family Species Life form Percentage of

total trees sampled

(b) Overstorey species ≥5 cm DBH

Lauraceae Actinodaphne elegans Tree 23.3


Anacardiaceae Nothopegia bedoomi Tree 12.9

Rutaceae Acronychia peduculata Tree 10.3

Myrtaceae Eugenia twaitessii Tree 7.82

Theaceae Camellia sinensis Tree 4.73

Rubiaceae Psychotria thwaitesii Tree 4.12


Euphorbiaceae Mallotus phillippinensis Tree 3.50

Euphorbiaceae Macaranga indica Tree 2.47



stems did not increase new cardamom seedling density over

the control treatment (Fig. 3, Appendix S5). There was no

effect of returning the cardamom trash to the plots on the

recruitment of new cardamom seedlings (Fig. 3). The

height of new cardamom seedlings was increased more in

unmanipulated cardamom plots and the plots where carda-

mom had been removed to ground level than the plots

where cardamomhad been removed completely, but height

did not differ among other treatments (Appendix S6).

The cardamom plants in March 2009 re-sprouted in the

plots where cardamom had been cleared to ground level

(Fig. 3). Uprooting the entire cardamom plants reduced

resprouting to zero as long as the rhizomes were removed

from the plots; however, when the uprooted cardamom

rhizomes were returned to the plots there is evidence that

they survived and re-sprouted to a similar extent as the

plants that were retained by slashing (significant interac-

tion: t = �2.71, P = 0.01; Appendix S5). The mean height

of sprouts did not differ among treatment plots (Appendix

S6). The density andmean height of new cardamom plants

recorded in June 2011 (seedlings and re-sprouts could not

be distinguished at this stage) did not differ among treat-

ments (Fig. 3, Appendix S5, S6).

The density of cardamom seedlings across all plots in

March 2009 was not correlated with woody plant seedling

density (r [n = 190] = 0.03, P = 0.78), but the density of

cardamom re-sprouts was positively correlated with seed-

ling density across all plots where cardamom stems were

0

10

20

30

40

50

60

70

80


2009 2011

Mea

n co

ver

of h

erbs

(% p

lot–1

)

Treatments in two cesus periods

0

5

10

15

20

25

30


2009 2011

Cov

er o

f Ageratina

(% p

lot–1

)

Treatments in two census periods

cc

b

a

(a)

(b)

Fig. 2. Mean (�SE) percentage cover of (a) all herbaceous plants including Ageratina riparia, and (b) A. riparia alone recorded per 5-m2 quadrat in March

2009 and June 2011 for plots where cardamom stands were abandoned and retained in an unmanipulated state (AB); plots managed by removal of dead

cardamom stems (CL); plots where cardamom stems were slashed at ground level and removed (SL); plots where cardamom stems were slashed at

ground level and cardamom trash placed uniformly across the plots (ST); plots where cardamom stems were uprooted and removed entirely from the

plots (UP); and plots where cardamom stems were uprooted and cardamom trash placed uniformly across the plots (UT), in a montane forest in Knuckles

Forest Reserve, Sri Lanka. In (a) lowercase letters denote significant (P < 0.05) differences among treatments AB, CL, SL and UP in 2009; treatments ST and

UT were not significantly different from SL and UP in 2009, and no plots differed significantly among treatments in 2011 (Appendix S4).



removed by slashing or uprooting (r [n = 66] = 0.37,

P < 0.05). The density of cardamom plants in June 2011

was not correlated with woody plant seedling density

(r [n = 126] = 0.08, P = 0.59).

Discussion

Effects of cardamom removal onwoody plant seedling

emergence

The removal of relict cardamom plants promoted a short-

term increase in the emergence of seedlings of woody

plants in abandoned cardamomplantations in high conser-

vation value tropical lower montane forest in Sri Lanka.

Since the cardamom had been originally planted into the

forest understorey, these new recruits included seedlings

of resident canopy trees, as well as trees and shrubs that

had been retained during the cultivation phase or subse-

quently re-colonized (Dhakal et al. 2012). The increase in

seedling emergence in response to cardamom removal

may have arisen because increased light transmission to

the forest floor triggered the germination of photoblastic

seeds (Swaine &Whitmore 1988; Dupuy & Chazdon 1998;

Pearson et al. 2002), or because release from competition

for soil nutrients and water stimulated germination or

seedling emergence (G�omez-Aparicio 2009).Where carda-

mom was removed by uprooting, soil disturbance may

have triggered the germination of deeply buried and dor-

mant seeds (Pearson et al. 2003). This result is consistent

with studies demonstrating higher recruitment and/or sur-

vival of tree seedlings in forests after clearing non-native

invasive herbaceous or liana species (Sweeney et al. 2002;

Hartman &McCarthy 2004; Minden et al. 2010), although

in some cases the establishment of tree seedlings may

depend on the sustained removal of understorey plants

(Duclos et al. 2013). The species composition of emergent

seedlings did not differ substantially among the cardamom

removal treatments, which suggests that they originated

from a common source (such as the soil seed bank and/or

newly dispersed seeds) that was distributed uniformly with

respect to the distribution of treatments. However further

research is required to determine whether differences in

species composition in response to treatments would

emerge over longer time scales than the duration of this

experiment through differential effects on seedling demog-

raphy.

The effect of cardamom removal on seedling emergence

varied among the methods employed and diminished with

time since the treatments were imposed. Cumulative

emergence of seedlings over the first 15 mo of the experi-

ment was no different for plots on which cardamom had

been slashed or uprooted, but seedling density at the end

of this period was higher in response to the uprooting

treatment. This contrast suggests that survival of the new

emergents was greater in response to the removal of the

entire cardamom plant, possibly because recovery of the

cardamom through resprouting in the slashing treatment

0

2

4

6

8

10

12

AB CL SL ST UP UT SL ST UP UT SL ST UP UT

2009 new seedlings 2009 sprouts 2011 new plantsMea

n ca

rdam

om se

edlin

g de

nsity

per

(5 m

2 ) se

edlin

g em

erge

nce p

lot

Treatments in two cenus periods

c

a

b

a

Fig. 3. Mean (�SE) density of new seedlings and sprouts in March 2009, and all new cardamom plants in June 2011 recorded per 5-m2 quadrat for plots

where cardamom stands were abandoned and retained in an unmanipulated state (AB); plots managed by removal of dead cardamom stems (CL); plots

where cardamom stems were slashed at ground level and removed (SL); plots where cardamom stems were slashed at ground level and cardamom trash

placed uniformly across the plots (ST); plots where cardamom stems were uprooted and removed entirely from the plots (UP); and plots where cardamom

stems were uprooted and cardamom trash placed uniformly across the plots (UT), in a montane forest of Knuckles Forest Reserve, Sri Lanka. Lowercase

letters denote significant (P < 0.05) differences among treatments AB, CL, SL and UP for new seedlings in 2009; treatments ST and UT were not significantly

different from SL and UP in 2009, and no plots differed significantly among treatments in 2011 (Appendix S5).



imposed competition for soil resources that constrained

survival of new seedlings (Denslow et al. 2006; Duclos

et al. 2013). Differences among treatments in the density

of seedlings had disappeared entirely by June 2011, which

was 27 mo since the last imposition of cardamom removal

treatments. This suggests that cardamom removal stimu-

lates a short-term flush of seedling emergence of woody

plants, which is detectable over the first year following

treatment, but without further intervention there would

be negligible impact on longer-term seedling recruitment

of woody plants.

The equalization of seedling density across treatments

between June 2009 and June 2011 resulted from the lower

survival of tagged seedlings on plots from which the carda-

mom had been removed by uprooting than in the unma-

nipulated control plots or plots where the cardamom had

been removed by clearing, thus reversing the pattern of

lower mortality on these more disturbed plots in the first

15 mo of the experiment. This phase of higher mortality

on the cardamom removal plots between 2009 and 2011

coincided with an increase in the cover of herbs and the

non-native shrub Ageratina riparia on the cardamom

removal plots, which was already detectable in 2009 and

for A. riparia became more pronounced by 2011, particu-

larly on the plots disturbed by uprooting cardamom.

Expansion of non-native invasive species in response to

large-scale natural or anthropogenic disturbance has also

been observed in tropical montane forests in Jamaica and

Tanzania, respectively, but the mechanisms that deter-

mine the link between disturbance and colonization of

non-native species have not been determined (Belling-

ham et al. 2005; W. Dawson, D.F.R.P. Burslem, & P.E.

Hulme, submitted). The positive association between

A. riparia cover and canopy openness at our study site is

consistent with results from other tropical forests, showing

that canopy gaps promote the establishment of non-native

invasive plants (Rogers & Hartemink 2000; Peters 2001;

Baret et al. 2008). We conclude that removing cardamom

had complex time-dependent effects on seedling emer-

gence and recruitment that were partly mediated by inter-

actions with other members of the plant community

(Kettenring & Adams 2011).

Although removal of cardamom triggered new emer-

gence of woody plant seedlings in the short term, the spe-

cies that emerged in largest numbers, such as Glochidion

coriaceum, Psychotria nigra and Rauvolfia densiflora, are wide-

spread species of low conservation value. Furthermore, the

beneficial effects on woody plant recruitment were offset

over longer time periods by parallel increases in the cover

of other herbs and the non-native perennial A. riparia. Ele-

vated mortality of new seedling emergents in response to

competition with these herbs resulted in elimination of a

net benefit to clearing the cardamom within 2 yr of the

final treatment, and an expansion of the Ageratina cover

on the treated plots. These responses suggest that eradicat-

ing cardamom would only be effective as a strategy for

restoring tree seedling recruitment if it was sustained over

long periods and combined with control of herbs and non-

native invasive species. Similar conclusions have been

derived from experimental work on the control of invasive

species (Horvitz & Koop 2001; Denslow et al. 2006) and

vegetation invading open areas in logged forests (Duclos

et al. 2013; Schwartz et al. 2013).

A practical intervention for restoring tree seedling

recruitment in abandoned cardamom plantations

Our research suggests that cardamom eradication inter-

ventions would need to be repeated annually over many

years to be successful, and they risk promoting expansion

of the cover of herbaceous plants, including non-native

species unless these are also controlled. As a result, this

approach would be labour-intensive and costly and may

ultimately limit its uptake as a practical method for restor-

ing seedling recruitment over large areas of abandoned

plantation. Based on the experience derived from our

experiment, we estimate that ca. 25 or 40 person-days

would be required to slash or uproot, respectively, the car-

damom plants from 1 ha of forest. There is also a risk that

disturbance associated with repeated cycles of cardamom

eradication would increase soil erosion in the steep terrain

at this site (Sharma et al. 2007). Further research is

required to determine whether gradual reductions in car-

damom density over longer periods of time would be a

more effective strategy for restoring tree seedling recruit-

ment whilst avoiding the negative consequences of instan-

taneous large-scale removal.

As an alternative to this intensive eradication

approach, our study suggests that minimal management

of the crop through removal of dead cardamom stems

and leaves and collection of the fruits (pods) is not detri-

mental to emergence of seedlings of woody plants. Over

time, the propagule pressure from the crop would decline

if the pods are harvested rather than allowed to mature

and spread within the abandoned plantations, and thus

the density of adult cardamom plants would naturally

decline over time as the residual crop plants senesce and

die. As long as the crop is not fertilized or replanted, this

minimal intervention strategy would permit the estab-

lishment of tree seedlings that would eventually supple-

ment and replace the canopy-forming trees of larger size

classes (>15 cm DBH) that currently occur at low density

in the cardamom plantations (Dhakal et al. 2012). Adopt-

ing this strategy would also allow local people in commu-

nities surrounding the abandoned plantations to derive

an income by harvesting cardamom pods. Careful



management, enforcement and monitoring would be

required to ensure that re-establishing the extraction of

cardamom from the plantations does not provide incen-

tives to maintain or even intensify cardamom cultivation

activities in the forest (Hall et al. 2011).

A strategy for restoration based on minimal manage-

ment and harvesting of cardamom pods relies on the

assumption that cardamom plants will gradually disappear

from the forest as they age and senescewithout replacement.

This source of uncertainty requires additional research, but it

may be significant that themean density of cardamomplants

in unmanaged (abandoned) plantations tends to be lower

than in actively managed plantations in the Knuckles

Forest Reserve (Dhakal et al. 2012). The risks of maintain-

ing abandoned cardamom plantations in which the pods

are allowed to mature are also evident at our study sites,

because cardamom is beginning to spread into patches of

primary lower montane forest adjacent to abandoned

cardamom plantations (Dhakal et al. 2012). We propose

that a strategy of promoting gradual population decline of

cardamom from abandoned plantations through senes-

cence and inhibition of cardamom recruitment would be

most effective in restoring tree regeneration and reversion

to the community structure of natural primary forest.

Acknowledgements

We thank the UK Darwin Initiative (Project No. 15-010)

for financial support and the Forest Department of Sri

Lanka for granting permission to carry out research in

the Knuckles Conservation Area. We are also grateful to

Midland State Plantation for allowing us to carry out

research in their cardamom plantations. We are also

grateful to the Postgraduate Institute of Science, Univer-

sity of Peradeniya, for providing office facilities to carry

out this research.

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Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Appendix S1.Maps and photographs showing study site,

experimental plots and cardamom plant.

Appendix S2. List of seedling species that emerged in

seedling emergence quadrats.

Appendix S3. Non-metric multidimensional scaling

(NMS) ordination diagrams of experimental plot scores

and species scores in (a) 2009 and (b) 2011.

Appendix S4. Summary of the output of statistical mod-

els: cover of herbaceous plants and Ageratina riparia across

treatments in 2009 and 2011.

Appendix S5. Summary of statistical models: density of

new cardamomplants among treatments in 2009 and 2011.

Appendix S6. Statistical summary of seedling survival,

heights of woody seedlings and new cardamom seedlings

and re-sprouts.



strategies for restoring tree seedling recruitment in high conservation value tropical montane...

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