Resilience to chronic defoliation in a dioecious understorey tropical rain forest palm

Resilience to chronic defoliation in a dioecious

understorey tropical rain forest palm

Leonel Lopez-Toledo1,2†, Niels P. R. Anten3,4, Bryan A. Endress2, David D. Ackerly5 and

Miguel Martınez-Ramos1*

1Centro de Investigaciones en Ecosistemas, Universidad Nacional Autonoma de Mexico, Antigua Carretera a

Patzcuaro No. 8701. Col. San Jose de La Huerta, C. P. 58190, Morelia, Michoacan, Mexico; 2Division of Applied

Plant Ecology, Institute for Conservation Research, San Diego Zoo Global, 15600 San Pasqual Valley Road

Escondido, CA 92027, USA; 3Ecology & Biodiversity Group, Institute of Environmental Biology, Utrecht University,

P.O. Box 800.84, 3508 TB, Utrecht, The Netherlands; 4Center for Crop System Analysis, Wageningen University,

P.O. Box 430 6700 AK, Wageningen, The Netherlands; and 5Department of Integrative Biology, University of

California, Berkeley, CA 94720, USA

Summary

1. Perennial plants often endure chronic loss of leaf area due to recurrent physical damage, herbiv-

ory and, for species used as non-timber forest products, due to leaf harvesting. However, little is

known about functional and demographic resilience (extent and speed of recovery) of plants

subjected to varying levels of chronic defoliation.

2. We used a dioecious, understorey palm (Chamaedorea elegans) to evaluate temporal trajectories

and rates of recovery of leaf functional traits and vital rates (survival, growth and reproduction)

after being subjected to experimental chronic defoliation regimes.

3. Pristine populations of mature C. elegans, categorized by gender (male and female), were sub-

jected to five defoliation levels (0%, 33%, 50%, 66% or 100% of newly produced leaves) every

6 months over a period of 3 years (1997–2000). To evaluate recovery from defoliation, surviving

palms were monitored for 3 years after the cessation of the defoliation treatment (2000–2003). We

recorded leaf functional traits (leaf persistence, leaf production rate, leaf size and leaf area) and

annual rates of mortality, growth and reproduction.

4. Cumulative effects of chronic defoliation concomitantly reduced leaf traits, survival, growth and

reproduction, and this effect was stronger in female than in male palms, independent of plant size.

Recovery fromdefoliation was faster inmales than in females, but proceeded gradually overall. Sur-

vival increased first, followed by growth, while reproductive traits showed the slowest recovery rate.

Recovery was independent of plant size. Notably, 3 years after defoliation treatment, the standing

leaf area and probability of reproduction had not recovered to pre-defoliation levels. Additionally,

we found that the occurrence of a severe drought in the first year (2000) after defoliation ceased led

to decreased survival, growth and reproduction and the ability of plants to recover fromdefoliation.

5. Synthesis. Chronic defoliation reduces fitness components of C. elegans palms differentially

between genders. Recovery is gradual and is slower and less complete in females compared with

males. The lower level of resilience to chronic defoliation shown by female plants may have pro-

found consequences for the dynamics and genetic variability of populations of tropical understorey

plants undergoing prolonged defoliation. Such effects may be aggravated by severe drought

episodes that are expected to increase in frequency according to global climate change predictions.

Key-words: Chamaedorea palms, drought, leaf harvesting, Mexico, non-timber forest prod-

ucts, plant population and community dynamics

Introduction

During their life, long-lived plants usually undergo several

defoliation events due to recurrent biotic (e.g. due to herbi-

vores and pathogens) or physical damage (e.g. due to wind,

*Correspondence author. E-mail: [email protected]

†Present address: Instituto de Investigaciones sobre los Recursos

Naturales-Universidad Michoacana de San Nicolas de Hidalgo,

Morelia 58337,Michoacan,Mexico.

� 2012 The Authors. Journal of Ecology � 2012 British Ecological Society

Journal of Ecology doi: 10.1111/j.1365-2745.2012.01992.x

fire, lightning and mechanical traumas). Leaves of many wild

plant species, particularly palms, are also repeatedly harvested

(Endress, Gorchov & Noble 2004). Depending on the severity

and frequency of leaf loss, negative effects on fitness compo-

nents may occur (Sampaio & Scariot 2010).While the recovery

of perennial plants from single defoliation events has been

clearly documented, much less is known about the extent and

rate at which functional and demographic attributes can

recover from multiple defoliation events occurring at different

magnitudes (Belsky et al. 1993).

Plants can compensate for leaf area losses by adjusting the

balance between photosynthesis and respiration, reducing

resource allocation to reproduction and ⁄or mobilizing stored

reserves from roots or other storage organs to the production

of new leaves (McNaughton 1983; Belsky et al. 1993;

Cunningham 1997; Anten, Martinez-Ramos & Ackerly 2003).

This compensatory ability enables plants to mitigate the nega-

tive impact of defoliation on survival and growth. However,

under repeated defoliation, the capacity for compensation can

be reduced or lost as stored reserves are depleted, which may

result in reductions in both growth and survival (Canham et al.

1999; Martınez-Ramos, Anten & Ackerly 2009). The degree

and pattern of recovery in functional and demographic rates

once defoliation has ended is still poorly understood. Assum-

ing that carbon limitation would be themain limiting factor on

recovery, the following general pattern could be expected: (i)

allocation of remaining resources and new photosynthetic

products (carbon, energy and nutrients) to increase leaf area

growth, (ii) allocational shifts should lead to enhanced plant

growth and (iii) reproductive activity resumes once the plant

attains enough photosynthetic reserves.

The time involved in this recovery process has not been

studied, but we can expect that the recovery rate will depend

on the plant function under consideration and the magni-

tude of defoliation to which plants were exposed. Some

studies have shown that recovery rates from single defolia-

tion events decrease with the magnitude of leaf area loss

and that larger plants may recover faster than smaller ones,

possibly due to greater pools of stored reserves (Marquis

1984; Boege 2005). Also, recovery rates may depend on

resource availability at the growing site (Hawkes & Sullivan

2001), species habit, plant phenology, ontogenetic stage or

the presence of specialized storage organs (Belsky et al.

1993; Hawkes & Sullivan 2001; Boege 2005; Lapointe et al.

2010). In the case of dioecious species, chronic defoliation

might have gender-specific effects on fitness, due to gender

differences in resource allocation to reproduction, growth

patterns and defence against herbivores (Cepeda-Cornejo &

Dirzo 2010). For example, in understorey palms, it has been

found that females have larger carbon investment to repro-

duction (Oyama & Dirzo 1988), grow more slowly and are

often better defended than males (Cepeda-Cornejo & Dirzo

2010). Due to these differences, it can be expected that

recovery rates would differ between female and male plants,

with females taking more time to recover their reproductive

activity than males due to the higher energetic costs involved

in the female reproductive function (Obeso 2002).

The occurrence of stochastic events, such as those imposed

by climatic factors (e.g. severe drought events as those caused

by El Nino Southern Oscillation (ENSO), in Mesoamerica),

may aggravate the effects of defoliation (Martınez-Ramos,

Anten & Ackerly 2009) and likely the ability to recover from

chronic leaf area losses. Overall, while there are several poten-

tial intrinsic and extrinsic factors that may affect the rate of

recovery from chronic defoliation, there is still little knowledge

on how these factors operate and on the long-term functional

and demographic consequences of such disturbances. For

example, it remains unclear whether recovery of vital rates

(survival, growth and reproduction) occurs along different

temporal trajectories and whether there are defoliation thresh-

olds beyond which the plants can no longer recover (i.e. loss of

resilience). Understanding these issues is important from an

evolutionary and ecological perspective, as well as to design

sustainable management programmes for species whose leaves

are harvested as non-timber forest products.

Many palm species are important as non-timber forest

products in tropical regions. Specifically, several are com-

mercially valued for their leaves and are subjected to

intensive repeated leaf harvesting (Bridgewater et al. 2006;

Zuidema, De Kroon & Werger 2007; Lopez-Toledo,

Horn & Endress 2011). The simple growth form of palms

(one or few monopodic stems with a single cluster of

leaves) makes them excellent model species to assess

demographic consequences and resilience to chronic defoli-

ation in plant populations (Endress, Gorchov & Noble

2004). In this study, we used the understorey, dioecious,

neotropical palm Chamaedorea elegans to evaluate tempo-

ral trajectories and rates of recovery of functional (leaf

persistence, leaf production rate, leaf size and plant leaf

area) and demographic traits (survival, growth and repro-

duction) after being subjected to different levels of experi-

mental chronic defoliation regimes. To our knowledge,

this is the first study describing the cumulative effects of

chronic defoliation on the recovery process following such

defoliation. In the previous studies, we have evaluated

mechanisms of compensation in response to defoliation

(Anten & Ackerly 2001; Anten, Martinez-Ramos &

Ackerly 2003) and examined the demographic behaviour

of C. elegans under contrasting chronic defoliation regimes

(Martınez-Ramos, Anten & Ackerly 2009). Here, we assess

the recovery capacity of the palms, as a function of the

intensity of defoliation (percentage of leaf area loss), gen-

der and stem size over 3 years following the end of defoli-

ation. Specifically, we tested the following hypotheses: (i)

the rate of recovery declines with the magnitude (percent-

age of leaf area loss) of chronic defoliation, (ii) males

recover faster than females, (iii) plant size determines

responses to chronic defoliation and recovery, (iv) recovery

is a gradual, stepwise process with leaf traits being the

first to recover to pre-defoliation levels, followed by

growth, and finally reproductive performance, with females

showing a more pronounced delay in reproductive recov-

ery. Finally, we explored the effect of a severe drought on

the recovery process.

2 L. Lopez-Toledo et al.

� 2012 The Authors. Journal of Ecology � 2012 British Ecological Society, Journal of Ecology

Material and methods

STUDY SITE

This study was conducted at the Chajul Biological Field Station,

within the Montes Azules Biosphere Reserve in Chiapas, Mexico

(l6�06¢ N, 90�56¢ W). Dominant vegetation in this region is lowland

evergreen tropical forest. Precipitation and temperature were quite

variable during the study period (1999–2003; Fig. S1); a dry season,

with considerably less rainfall than the long-term average, occurred

in 2000 (January–May). This rainfall shortage was similar to that

in 1998, when a severe ENSO event occurred (Martınez-Ramos,

Anten&Ackerly 2009).

STUDY SPECIES

Chamaedorea elegans Willd (Arecaceae) is a solitary and dioecious

understorey palm species native to south-east Mexico, Guatemala

and Belize (Anderson, Galeano & Bernal 1997). In Chajul,

C. elegans grows up to 1.5 m in height and is restricted to the

karst-range areas (300–700 m asl). Chamaedorea elegans represents

one of the most commercially important NTFP’s in SE Mexico,

Guatemala and Belize, as their leaves and fruits are collected and

exported for the European and US floral industry (Hodel 1992).

However, due to overexploitation, this species has become scarce

in some areas (Sanchez-Carrillo & Valtierra-Pacheco 2003). For a

detailed description of the species, see Martınez-Ramos, Anten &

Ackerly (2009).

EXPERIMENTAL SYSTEM

Pristine natural populations of C. elegans within Montes Azules

reserve were selected. These populations were subjected to experi-

mental harvesting every 6 months over 3 years (1997–2000). Plants

were selected and stratified by initial height and gender categories

(male and female) and then randomly assigned to one of the five

following defoliation treatments: 0%, 33% (one from every three

leaves), 50% (two of every four leaves), 66% (two of every three

leaves) and 100% (all leaves). There were 190–196 replicates per

treatment for the 0%, 33%, 50 and 66% defoliation levels. The

first defoliation was conducted in March 1997, and the final event

was in March 2000 after which the palms were left untouched

(details in Anten, Martinez-Ramos & Ackerly 2003 and Martınez-

Ramos, Anten & Ackerly 2009).

Previously published work described the immediate effects of

defoliation from 1997 to 1999, while in this study, we evaluate

recovery of the surviving palms, over six subsequent censuses,

from October 2000 to March 2003. Data for 2000 represent the

final year under defoliation and are presented as ‘Cumulative

effects of chronic defoliation’, while data from 2001 (Recovery-

Yr1) to 2003 (Recovery-Yr3) are presented as ‘Recovery from

defoliation’.

At each census date, we recorded mortality and, for surviving

individuals, gender, stem length, number of standing leaves, num-

ber of persistent leaves (live leaves produced in previous years),

leaf production rate, length of the most recent fully expanded leaf

and reproductive activity (inflorescence, infructescence and fruit

production). As another measure of reproductive performance for

females, we quantified the proportion of inflorescences that

matured into infructescences. For data analysis, a palm’s repro-

ductive status (female and male) was based on cumulative obser-

vations made throughout the 6 years of study.

DATA ANALYSIS

We carried out analyses focusing on two issues: (i) to evaluate the

cumulative effects of chronic defoliation regimes (i.e. 3 years after the

first defoliation event) and (ii) to assess the ability of palms to recover

from the negative effects of such regimes (over the course of 3 years

since the last defoliation event).

We included 11 different functional and demographic traits as

response variables for analyses. Functional traits included five leaf

attributes: (i) leaf persistence (number of persistent leaves produced

in previous year), (ii) leaf production rate (newly produced leaves per

palm year)1), (iii) total standing number of leaves, (iv) leaf size

(length) and (v) total leaf area per palm. Leaf length refers to the dis-

tance from the base to the tip of the lamina of the newest leaf of each

palm, and total leaf area was estimated from an allometric equation

previously obtained, based on the number of leaves and the lamina

length of each leaf (Anten & Ackerly 2001). Demographic traits

includedmortality, growth and reproduction.Mortality was analysed

as a binary response variable and expressed as an annual mortality

rate (ind ind)1 year)1). Growth was quantified as the annual exten-

sion rate of the stem (cm ind)1 year)1). Reproduction was analysed

through four traits: (i) the probability of reproduction, that is, the

proportion of total female or male palms reproducing (flowers pro-

duction) each year (ind ind)1 year)1), (ii) annual inflorescence pro-

duction per female ormale palm (inflorescences ind)1 year)1), (iii) the

proportion of inflorescences that mature into infructescence per

female palm and (iv) fruit production per reproductive female (fruits

reproductive ind)1 year)1).

The extent towhich defoliated plants were able to recover was anal-

ysed by comparing the mean trait response for a given defoliation

treatment to that of the control palms of the same gender.We consid-

ered a trait fully recovered from defoliation, when the mean value for

the defoliated treatment was not significantly different from that of

the controls (based on analysis below). The speed of recovery was

quantified by determining the number of years it took for full recov-

ery, and the possible outcomes were 1, 2 and 3 years after defoliation

stopped.

We conducted two separate statistical analyses to assess the cumu-

lative effects of the defoliation treatments on the response variables

and to assess the recovery from the treatments. For the first analysis,

we tested effects due to gender (‘G’ with two levels: females and

males), defoliation treatment (‘DT’ with four levels: 0%, 33%, 50%

and 66%), initial stem length (‘SL97’), which represent plant size at

the beginning of the defoliation experiment (in the year 1997), and

all the interactions among these variables, considered as fixed factors.

The analyses were conducted using linear models (LM) for continu-

ous response variables (e.g. stem growth, leaf length and total

leaf area) and generalized linear models (GLM) for count (e.g. leaf

persistence, inflorescence and fruit production) and binomial (e.g.

probability of mortality, proportion of infrutescences ⁄ inflorescences,probability of reproduction) response variables (Crawley 2007).

For the second analysis, we also tested the effects of gender and

defoliation treatment, but we used stem length at the year 2000

(SL00), which represents plant size at the beginning of the recovery

period. We also included the factor year (Yr) as another variable

to assess differences among years (2001, Recovery-Yr1 to 2003,

Recovery-Yr3), and all interactions among these four independent

variables were considered as fixed factors. In this case, due to the

repeatedmeasures design, we conducted linear mixed models (LMM)

for the continuous variables and generalized LMM for the count and

binomial variables. The repeated measures of every year on individu-

als were included as a random factor (Pinheiro &Bates 2001).

Resilience to chronic defoliation in palms 3


For LM and LMM analyses, when required, response variables

were log(x) or log(x + 1) transformed tomeet normality criteria. For

count variables, a Poisson error and a logarithmic link function were

used, while for binomial variables, a binomial error and a logistic link

function were applied. For GLMs, when overdispersion problems

occurred, a proper rescaled model was used (Crawley 2007; Everitt &

Hothorn 2010). All analyses were completed in R 2.11.1 (R Develop-

ment Core Team 2010).

Results

Results for leaf traits are presented first, followed bymortality,

growth and reproduction. For each set of characteristics, we

first show the cumulative effects of defoliation as reflected in

the 2000 final harvest data (Table 1) and subsequently present

the results for recovery (Table 2). The charts presented in the

results section highlight the main effects of defoliation treat-

ment, gender and years. Additional charts showing the rela-

tionship between the attributes analysed and stem length are

presented in the Supporting information.

LEAF FUNCTIONAL TRAITS

Cumulative effects of chronic defoliation

After 3 years of sustained defoliation, values of all leaf traits

analysed had declined with respect to that of control palms.

Overall, across all defoliation treatments, male palms had sig-

nificantly higher leaf trait values than females (Table 1;

Fig. 1). The negative effect of defoliation on leaf persistence

and leaf length was stronger among females than amongmales

(Fig. 1a–d; Table 1). For the other leaf traits, defoliation

effects did not differ significantly between genders. Stem length

did not affect any of the leaf traits analysed (Table 1).

Recovery from defoliation

Recovery of leaf traits in defoliated palms compared with

the control group varied depending on gender and the level

of defoliation. The magnitude of such effects varied among

years with higher values in 2001 for most of the leaf traits.

However, differences among years were only significant for

leaf production rate, leaf length and total leaf area

(Table 2, Fig. 1). Overall, male palms from all defoliation

treatments recovered more quickly than female palms, and

after 2 or 3 years, all leaf trait values of defoliated palms

had values that were not significantly different from those

observed in the control male palms (Fig. 1). By contrast,

over the same time span, female palms in the 50% and

66% defoliation treatments only recovered leaf production

rate (Fig. 1c) and the standing number of leaves (Fig. 1e),

whereas values of leaf persistence (Fig. 1a), leaf length

(Fig. 1b) and total leaf area (Fig. 1i) were still lower than

those of non-defoliated female palms. For each of the three

recovery years, on average, male palms exhibited signifi-

cantly higher leaf trait values than female palms, except

leaf length in the third year of recovery (Table 2, Fig. 1).

It is interesting to note that in Recovery Yr-1 (2001), female

palms, and to a lesser extent male palms, frommost treatments

(included control palms) increased their mean total leaf area

(Fig. 1i) due to an increase in leaf production rate (Fig. 1c)

and the production of larger leaves (Fig. 1g). We only found

significant interactive effects of defoliation treatment with stem

Table 1. Results of linear models (LM) and generalized linear models (GLM) used to assess the cumulative effects of chronic defoliation on

Chamaedorea elegans in south-eastern Mexico. The terms tested in the models were gender (G), defoliation treatment (DT), initial stem length

(SL97) and the interaction among these terms

G DT G*DT

Functional traits

Leaf persistency 3.6* (1) 50.4*** (3) ns

Leaf product rate 5.3* (1) 7.8* (3) ns

Total leaves 3.6 (3) 28.3*** (3) ns

Leaf length 6.5* (1,609) 24.4*** (1,609) 3.1* (1,609)

Total leaf area 6.5* (1,609) 24.1*** (1,609) 3.1* (3,609)

Demographic traits

Mortality 6.4** (1) 8.1* (3) ns

Growth rate 4.1* (1,595) 3.9* (3,595) ns

Functional traits

Probability of reproduction ns 39.2*** (3) ns

Inflorescences production 4.5* (1) 7.9* (3) ns

Infrutescences ⁄ inflorescences ratio 8.9* (3)

Fruit production 23.6** (3)

GLM (leaf persistency, leaf production rate, total leaves and mortality) and LM (leaf length, total leaf area and growth rate) statistics

are provided (F values for LM and v2 for GLM, degrees of freedom in brackets); significance level: *P £ 0.05; **P < 0.01;

***P < 0.001; ns, non-significant. Only significant terms were included in the minimal adequate model, – indicates that this term was

removed from the model. For analysis of female-exclusive variables (infructescences ⁄ inflorescences ratio and fruit production), the term

gender was not tested.



Table

2.Resultsoflinearmixed

models(LMM)andgeneralizedlinearmixed

models(G

LMM)usedto

assesstherecoveryfrom

chronicdefoliationoffunctionalanddem

ographictraitsofChamaedorea

elegansin

south-eastern

Mexico.T

heterm

stested

inthemodelsweregender

(G),defoliationtreatm

ent(D

T),year(Y

r),stem

lengthafter

defoliation(SL00)

andtheinteractionsamongtheseterm

s.Individual

withinyearwasincluded

inthemodelasrandom

factorto

accountfortherepeatedmeasurements

Factors

GDT

SL

Yr

G:D

TDT:Y

rG:Y

rDT:SL

Yr:SL

Functionaltraits

Leafpersistency

3.6*(1)

37.9***(3)

4.1*(1)

ns

ns

ns

ns

14.5**(3)

ns

Leafproduct

rate

10.2***(1)

7.8*(3)

ns

19.4***(2)

ns

ns

ns

ns

ns

Totalleaves

19.6***(1)

47.2***(3)

4.3*(1)

ns

ns

ns

ns

ns

ns

Leaflength

ns

13.9***(3,1604)

ns

11.8***(2,1604)

12.1***(3,1604)

2.5*(6,1604)

4.7*(2,1604)

6.9*(3)

ns

Totalleafarea

7.5**(1,1604)

19.1**(3,1604)

ns

4.1*(2,1604)

2.7*(3,1604)

4.6***(6,1604)

ns

ns

ns

Dem

ographic

traits

Mortality

ns

11.2***(3)

5.2*(3)

ns

ns

11.4***(6)

ns

11.9***(3)

35.1***(2)

Growth

rate

7.8*(3,1600)

3.6*(3,1600)

–39.1***(2,1600)

3.6*(3,1600)

ns

ns

ns

ns

Reproductivetraits

Probabilityof

reproduction

ns

23.8***(3)

ns

11.5**(3)

ns

ns

7.6**(2)

ns

ns

Inflorescence

production

14.7***(1)

45.3***(3)

7.1**(2)

27.7***(2)

ns

ns

11.4**(2)

ns

ns

Infrutescences

⁄inflorescencesratio

7.5**(3)

ns

5.8*(2)

16.1**(6)

ns

ns

Fruitproduction

19.2**(3)

ns

21.7**(2)

ns

12.6**(3)

ns

GLMMs(leafpersistency,leafproductionrate,totalleaves

andmortality)andLMMs(leaflength,totalleafareaandgrowth

rate)statisticsare

provided

(Fvalues

forLM

and

v2values

for

GLMM;degrees

offreedom

inbrackets);significance

level:*P

£0.05;**P<

0.01;***P<

0.001;ns,

non-significant).Thetable

presents

only

significantterm

s.Theinfrutescences

⁄inflorescences

ratioandfruitproductionwereonly

tested

infemales.



length (SL00) on leaf persistence and leaf length, independent

of gender (Table 2). Overall, bigger palms from the 50% and

66% defoliation treatment had less persistent leaves compared

with control palms (Fig. S2). While leaf length increased with

stem length in defoliated palms, this was not the case for the

control plants. As a result of these trends, smaller defoliated

palms had smaller leaves than control plants, while the con-

trary was true for bigger palms (Fig. S3). Finally, we detected

a positive single effect of stem length on the number of leaves,

which was independent of the defoliation treatment, gender

and year; however, stem length explained only 9% of the inter-

individual variation.

MORTALITY


Overall, in the final year of defoliation treatments, the effect of

defoliation on mortality rates differed between genders, with

higher mortality rates in females (Table 1, Fig. 2). Among

female palms, mortality increased with defoliation level, with

66% defoliated females having a threefold higher mean (±SE)

mortality rate (9.1%±0.1) than control palms (Fig. 2a). By

contrast, mortality rates did not differ significantly between

defoliated and controlmale palms (Fig. 2a,b).

0% 33% 50% 66%

Defoliation treatment

0.00

0.04

0.08

0.12

2000 2001 2002 2003

(i)

2000 2001 2002 2003

(j)

20

30

40

50 (g) (h)

1.0

3.0

5.0

7.0 (e) (f)

(d)

Tota

l le

af a

rea

(m2)

Leaf

len

ght

(cm

) Tota

l le

aves

Le

af p

roduct

ion r

ate

(lea

ves

ind

–1 y

r–1)

0.0

1.0

2.0

3.0

4.0 (a)

0.0

1.0

2.0

3.0 (c)

(b)

Pers

iste

nt

leav

es(n

um

ber

of

leav

es)

Year

Fig. 1. Recovery patterns of leaf functional

traits of Chamaedorea elegans palms, as a

function of gender and chronic defoliation

levels in south-eastern Mexico. Leaf persis-

tence, leaf production rate, total leaves, leaf

length and total leaf area for females (a, c, e,

g and i) and males (b, d, f, h and j). The indi-

cated defoliation treatments correspond to

the percentage of standing leaves removed

every 6 months over 3 years. Last defolia-

tion event was applied in 2000. Bars indicate

mean value, and vertical lines represent±1

standard error.




The ability to survive after chronic defoliation depended on

defoliation treatment, and there were no significant differences

among genders (Table 2, Fig. 2). In the first year after defolia-

tion (2001), mortality rate increased for both genders and for

all defoliation treatments including the control (0% defolia-

tion). This amplified differences among defoliation treatments,

where mortality rate rose over 15% in the 66% defoliation

treatment (Fig. 2). Two years after last defoliation event

(2002), mortality rates of male and female defoliated palms

were not significantly different from those of control palms.

Mortality rate varied depending on the interaction between

defoliation treatment and stem length (SL00) and between

defoliation treatment and year (Table 2). Effects of plant size

were mainly observed in the Recovery-Yr1, where bigger

palms (independent of gender) subjected to 66% defoliation

exhibited higher mortality rates than palms from the other

defoliation treatments, and this difference disappeared in later

years (Fig. S4).

GROWTH


Three years of repeated defoliation lead to a reduction in stem

growth rate (Table 1), principally in palms from the 66%defo-

liation treatment (Fig. 3). Defoliation impacted growth of

males and females in a similar way (Table 1). Across all treat-

ments, females grew significantly slower than males with a

mean (±SE) of 4.01 (±0.19) vs. 4.56 (±0.22) cm year)1, respec-

tively. Initial stem size did not affect the response on stem

growth.


One year after the last defoliation event (2001), growth rates of

palms from all defoliation treatments, including the control,

decreased and were slower than in subsequent years. In this

year, greater impacts of defoliation were observed on female

compared with male palms (Table 2); female palms from the

50% and 66% defoliation treatments had growth rates that

were 28%and 49% slower than those of control palms, respec-

tively. Defoliated females took more time to recover; it took

2 years until growth rates were similar to growth rates of the

control female palms compared with only 1 year for the males

(Table 2, Fig. 3a,b). However, 3 years after the last defoliation

event, differences in growth between males and females were

no longer significant (Table 2, Fig. 3). Stem size did not affect

the recovery process of stem growth (Table 2).

REPRODUCTIVE TRAITS


All defoliation treatments reduced the probability of reproduc-

tion, and to a lesser extent inflorescence production, in female

palms, while in male ones, only the 66% treatment produced a

Mort

ality

rate

(in

d ind

–1 y

ear–

1)

Year

0% 33% 50% 66%Defoliation treatment

0

0.1

0.2

0.3

2000 2001 2002 2003

(a)

2000 2001 2002 2003

(b)

Fig. 2. Temporal changes in mortality (ind

ind)1 ha)1) in Chamaedorea elegans palms

after being subjected to different chronic

leaf defoliation treatments in Chajul, south-

eastern Mexico. 2000 represents the last year

of defoliation treatment. Differences among

genders are illustrated in the different charts:

(a) females and (b) males. Bars indicatemean

value, and vertical lines represent±1 stan-

dard error.Ste

m g

row

th (

cm y

ear–

1)

Year

0% 33% 50% 66%


2000 2001 2002 2003

(b)

1

2

3

4

5

2000 2001 2002 2003

(a)

Fig. 3. Temporal changes in stem growth

(cm year)1) in Chamaedorea elegans palms

after being subjected to different chronic leaf

defoliation treatments in Chajul, south-east-

ern Mexico. 2000 represents the last year of

defoliation treatment. Differences among

genders are illustrated in the different charts:

(a) females and (b) males. Bars indicatemean


dard error.



significant reduction (Table 2; Fig. 4). In female palms, infr-

uctescence ⁄ inflorescence ratio (Fig. 5a) and fruit production

per reproductive palm (Fig. 5b) strongly decreased as defolia-

tion level increased. Stem length did not affect the response of

any of the reproductive traits analysed (Table 1).


Recovery depended on the reproductive trait considered and

on the defoliation treatment and gender (Table 2). In the first

year after defoliation (2001), most reproductive trait values of

palms from all defoliation treatments (including control

palms) decreased with respect to those of previous and subse-

quent years, especially in female palms (Figs 4 and 5). In this

and the following 2 years, female palms from all defoliation

treatments had a much lower probability of reproduction than

control female palms (Fig. 4a, Table 2). By contrast, male

palms from all defoliation treatments exhibited probabilities of

reproduction similar to controlmale palms 2 years after defoli-

ationwas suspended (Table 2, Fig. 4b).

In contrast to the probability of reproduction, inflorescence

production of female palms from all defoliation treatments

had risen to values similar to control palms 2 years after the

last defoliation event (Fig. 4c). Inflorescence production in

male palms was not affected by defoliation, and individuals

from all defoliation treatments recovered inflorescence produc-

tion in just 1 year (Fig. 4d).

Recovery of other reproductive components of female

palms varied depending on the trait considered. While the

infructescence ⁄ inflorescence ratio of female palms from all

defoliation treatments reached values similar to that of con-

trol palms 2 years after defoliation (Fig. 5a), rates of fruit

production per reproductive palm recovered only after

3 years (Fig. 5c) did not recover at all (Fig. S2). The only

significant interactive effect between stem length and defolia-

tion was observed on fruit production (Table 2). Overall,

while in the control palms, fruit production increased with

stem length, in the defoliated palms, such relationship was

negative, especially for palms subjected to the 50% and 66%

defoliation treatments (Fig. S5). Finally, inflorescence pro-

duction increased with stem length, independent of defolia-

tion treatment and gender, but the explained variance was

only 10% (Table 2).

Discussion

Leaf area losses, which are caused by physical or biotic agents,

can strongly influence functional and demographic behaviour

of plants (Marquis 1984; Anten & Ackerly 2001; Endress,

Gorchov &Noble 2004). Our results show that the cumulative

effects of repeated defoliation on leaf functional traits and

demographic attributes of C. elegans palms depend on both

the defoliation level and gender, but not on plant size. Specifi-

cally, our findings support the hypotheses that: (i) female

palms suffer stronger negative demographic effects due to

defoliation than males, (ii) the magnitude of the negative

effects increased with the level of defoliation, (iii) the effects on

reproduction were stronger than effects on leaf traits, growth

and survival. Regarding the ability of palms to recover from

defoliation (resilience), we found that: (i) leaf length and leaf

production rate recover faster than total leaf area, (ii) survival

rates recover more quickly than growth and reproduction, (iii)

male palms recover faster than females and (iv) the recovery

time increases with higher levels of defoliation (Table 3). Plant

size did not have a consistent effect on the recovery of defoli-

ated palms.

ForC. elegans, leaf harvesting is probably themain cause of

leaf area loss, and our defoliation treatments bracketed the

0% 33% 50% 66%


Year Year

0.0

0.2

0.4

0.6

0.8

1.0 (a)

2000 2001 2002 2003

(d)

(b)

Probab

ility

of

repro

duct

ion

0.0

0.5

1.0

1.5

2.0

2.5

2000 2001 2002 2003

(c)

Inflore

scen

ce p

roduct

ion

Fig. 4. Temporal changes in reproductive

traits of Chamaedorea elegans palms after

being subjected to different chronic leaf defo-

liation treatments in Chajul, south-eastern

Mexico. 2000 represents the last year under

defoliation. The top charts show the proba-

bility of reproduction, and the bottom charts

show inflorescence production for: females

(a, c) andmales (b, d).



levels at which this harvesting occurs. Although such defolia-

tion levels in Chamaedorea species may also happen due to

natural causes (N. P. R. Anten, personal observations), they

typically tend to be lower (1–23% of leaf area; Martınez-

Ramos, Anten & Ackerly 2009; Cepeda-Cornejo & Dirzo

2010). However, for many other species, stochastic events such

as insect outbreaks, branch fall, strong storms, browsing and

fire may damage higher proportion of leaf area and cause

higher functional damages and affect population patterns

(Coley, Bryant & Chapin 1985; McPherson & Williams 1998;

Lopez-Toledo, Horn&Endress 2011).

EFFECTS OF CHRONIC DEFOLIAT ION

Earlier defoliation studies conducted on palm species found

that single defoliation events generally had no negative func-

tional or demographic effects. In some cases, overcompensa-

tion, that is, faster growth and reproduction in defoliated

plants, was even observed (Mendoza, Pinero & Sarukhan

1987; Oyama & Mendoza 1990; Chazdon 1991). In contrast,

our results strongly suggest that cumulative effects of chronic

defoliation may lead to strong reductions in demographic

rates. Palms tend to maintain large carbohydrate stores, and

these stores play a crucial role in survival and regrowth after

defoliation (Kobe 1997). ForC. elegans, the cumulative effects

of chronic defoliation were independent of stem size, which

may be indicative of the importance of storage organs other

than stems, such as roots. In chronically defoliated palms,

these stores may be depleted by the continuous resource

demand to support regrowth of photosynthetic tissues

and maintenance of vegetative organs (Belsky et al. 1993;

McPherson & Williams 1998). For example, non-structural

carbohydrates in below-ground organs of Sabal palmetto seed-

lings were depleted after repeated events of defoliation, which

then resulted in reduced growth rates and increased mortality

rates (McPherson&Williams 1998).

The effects of leaf area losses also depend on the level of

defoliation. Even a single, but severe (75–100% of leaves

removed), defoliation eventmay result in significant reductions

in functional or demographic traits (Mendoza, Pinero &

Sarukhan 1987; Oyama & Mendoza 1990; Boege 2005). Our

results agree with these studies, as our lower defoliation

treatment (33%) had only minor negative effects in some

reproductive traits (probability of reproduction and fruit pro-

duction), while the more intensive defoliation treatments (50–

66%) had strong negative effects on all analysed demographic

rates. This indicates that chronic defoliation at high intensities

may cause strong negative effects on plant fitness (Endress,

Gorchov & Berry 2006; Martınez-Ramos, Anten & Ackerly

2009).

GENDER EFFECTS AND RECOVERY FROM CHRONIC

DEFOLIAT ION

In dioecious species, resource allocation to reproduction tends

to be asymmetrical between genders (Case &Ashman 2007). It

has been documented that female plants invest more resources

in reproductive functions than males and that their growth

rates are consequently slower than those of males (Ataroff &

Schwarzkopf 1992). This has also been documented in four

species ofChamaedorea palms (Oyama&Dirzo 1988; Cepeda-

Cornejo & Dirzo 2010). Our study on C. elegans is the first

showing differences between genders both in the cumulative

effects of chronic defoliation and in the resilience to such dis-

turbance in perennial plants. Differential gender-specific

resource allocation could explain why, after chronic defolia-

tion, female palms produced lower photosynthetic total area

and, concomitantly, lower survival and growth than males.

Also, the recovery of most functions, and particularly repro-

duction, following the cessation of chronic defoliation was

both slower and less complete in females. In the case of fruit

production, there seemed to be no recovery at all even 3 years

after defoliation had stopped, that is, the relative difference

between defoliated and non-defoliated females did not

decrease. The latter effect was probably caused by the slower

recovery in leaf area and associated carbon reserves in females.

The detected interactive effect between plant size and defoli-

ation on leaf length and leaf persistence could be indicative of

different strategies associated with leaf area production. Smal-

ler defoliated palms maintained more but smaller leaves, while

larger defoliated palms maintained fewer bigger leaves. Such

different strategies could be associated with the fact that more

but smaller leaves entail lower support costs at the leaf level,

but larger costs of stem growth and self shading (Anten &

Ackerly 2001). On the other hand, the higher mortality and

lower fruit production exhibited by bigger recovering palms

Year Year

0% 33% 50%


0

20

40

60

2000 2001 2002 2003

(b)

0

0.1

0.2

0.3

0.4

0.5

2000 2001 2002 2003

(a)

Proport

ion I

nfr

/Infl

Fruit p

roduct

ion

66%

Fig. 5. Temporal changes in reproductive

traits of female palms of Chamaedorea

elegans after being subjected to different

chronic leaf defoliation treatments in Chajul,

south-eastern Mexico. 2000 represents the

last year of defoliation treatment. (a)

Infrutescences ⁄ inflorescences ratio and (b)

fruit production per reproductive female

(ind.ind repr)1 year)1). Bars indicate mean


dard error.



may have two possible complementary explanations. In gen-

eral, as plant size increases, the leaf area ratio (leaf area per bio-

mass unit) and thus the balance between photosynthetically

active and non-active tissue decreases (Poorter 1999). A reduc-

tion in leaf area by defoliation could therefore be more likely

to result in a negative carbon balance in large plants, relative to

smaller ones. It is also possible that reproductive costs,

expressed as future reductions in survival and or reproduction,

are higher for larger plants (e.g. Pinero, Sarukhan & Alberdi

1982) and that such costs aremore strongly expressed in defoli-

ated plants.

Overall, our results suggest that the recovery process from

chronic defoliation inC. elegans proceeds in a series of gradual

steps. As discussed previously, single or few defoliation events

have limited or no perceptible negative consequences on func-

tional or demographic traits, and plants easily recover their

pre-defoliation status (Oyama & Mendoza 1990; Chazdon

1991; Endress, Gorchov &Noble 2004). If defoliation is recur-

rent, functions of relatively low energetic and demographic

costs, such as reproduction, are the first traits negatively

affected. In long-lived understorey palms, it has been docu-

mented that individuals allocate more resources to somatic

structures (roots, stems and leaves) important for survival and

growth than to reproductive organs (Pinero, Sarukhan &

Alberdi 1982; Oyama & Dirzo 1988). In long-lived plants,

reproductive rates tend to be much less important for popula-

tion growth and fitness (i.e. they have much lower elasticity)

than growth and survival parameters (Franco & Silvertown

2004). As defoliation persists through time, a decrease in func-

tional components of higher energetic and demographic costs,

such as stem growth and leaf area production, occurs. Finally,

if defoliation continues, plants are not able to maintain a posi-

tive carbon balance and die.

The recovery process from chronic defoliation also follows a

gradual pattern. Leaf area recovered first, mediated by recov-

ery of other leaf traits such as leaf persistence, leaf production

and leaf size. This fast recovery of leaf area and associated light

capture is probably vital for survival in the forest understorey.

In males, all leaf traits had recovered to the levels of non-

defoliated plants within 3 years following the cessation of

defoliation. By contrast, leaf persistence and leaf length, and

by consequence total standing leaf area, did not fully recover

in females during this period.Once leaf area has recovered, sur-

vival recovers faster than growth and growth recovers faster

than reproduction.

Our results indicate that chronic and high levels of defolia-

tion strongly reduce seed production, increase mortality and

reduce growth. All this together may shrink populations and

skew sex ratios to a higher proportion of males, which may

consequently influence long-term population growth as found

in other dioecious palm species (Holm, Miller & Cropper

2008). This may also affect genetic variation (Eguiarte et al.

1993) well beyond the period over which defoliation takes

place. It is likely that chronic defoliation may be responsible

for the reduction or local extinction of Chamaedorea popula-

tions in some tropical regions in Mexico and Central America

with high leaf extraction rates (Sanchez-Carrillo & Valtierra-

Pacheco 2003; Bridgewater et al. 2006; Endress, Gorchov &

Berry 2006). Our results thus strongly indicate that the impact

of stress events on plant performance and population dynam-

ics should include estimates of recovery time, and in long-lived

species, this should be extended several years beyond the per-

iod over which the stress events occurred. Another important

implication of our results is that studies on gender differences

in demographic rates should have long-term approaches and

recognize historical or severe stress events to identify possible

effects of stress events that occurred in the past. These issues

have not been addressed in natural populations and will be

very important in future research.

STOCHASTIC EFFECTS

Defoliation effects may interact with other factors such as cli-

matic stochasticity. Previous studies have shown that the

impact of such external factors may even be stronger than

those of defoliation. For example, our previous study with

C. elegans included a severe drought related to an ENSO event

in 1998, which caused strong effects inmortality and reproduc-

tion independently of defoliation level (Martınez-Ramos,

Anten & Ackerly 2009). Surprisingly, during the year period

2000–2001, a similar anomaly in precipitation and temperature

to that of El Nino-1998 was recorded in our study locality

(Lacantum, Chiapas, CNA-Mexico). During the 2000 dry sea-

son, rainfall from February to April was 66% lower than the

long-term average (Fig. S1). As our results show, this drought

Table 3. Rates of functional and demographic recovery of

Chamaedorea elegans palms with different levels of chronic defoliation.

Speed of recovery is measured as the number of years (1–3 years)

required for a palm to reach statistically same trait values than those of

non-defoliated (control) palms. ‘>3’ means that this specific trait did

not recover 3 years after the last defoliation event. The – symbol

indicates those factors are restricted to females. Percentages correspond

to three chronic defoliation levels (per cent of standing leaves removed)

applied every 6 months over 3 years (1997–2000)

Trait

Females Males

33% 50% 66% 33% 50% 66%

Functional leaf traits

Leaf persistence 1 >3 >3 2 3 3

Leaf production rate 2 2 2 1 2 2

Total leaves 2 3 3 2 3 3

Leaf length 1 3 >3 1 1 2

Total leaf area 2 >3 >3 2 3 3

Demographic traits

Mortality 1 1 2 1 1 2

Growth rate 2 2 3 1 1 1

Reproductive traits

Probability of reproduction >3 >3 >3 1 2 2

Inflorescence production 2 2 2 1 1 1

Infrutescences ⁄inflorescences ratio

2 2 3 – – –

Fruit production per

reproductive female

3 >3 >3 – – –



event had clear impacts on the ability of palms to recover, as it

intensified the effects of defoliation and slowed recovery rates.

As droughts have been predicted to become more frequent in

tropical forest areas in the future (Easterling et al. 2000), their

effects on plant recovery fromdefoliation should be considered

when quantifying the impact of chronic defoliation in under-

storey palms.

Conclusion

In this study, we have shown that chronic defoliation reduces

fitness components (survival, growth and reproduction), and

this reduction is higher as defoliation levels increase, particu-

larly for female plants. Plants appear to survive chronic defoli-

ation by strongly reducing reproduction and subsequently

growth. Once defoliation stops, males recover faster than

females, and the recovery appears to be stepwise, with survival

and growth increasing first and reproductive functions recov-

ering more slowly. The slow recovery of females, in particular,

may have significant consequences for population dynamics

and genetic variation and should be considered in demo-

graphic studies as well as in studies that determine the impact

of leaf harvesting. Climatic factors, such as severe drought,

affect the ability of plants to recover from chronic defoliation.

Thus, the incidence of severe episodic disturbances, such as

drought, may play a dominant role in the population dynamics

of tropical rain forest understorey plants when combined with

chronic defoliation.

Acknowledgements

This study was supported by theU.S. National Science Foundation (grant IBN

9604030) and the Packard Foundation (No. 1999-4903). CIECO-UNAM

provided additional financial support. LLT was supported by a Master

Scholarships (CONACYT: 163218) and the Postdoctoral Program of the San

Diego Zoo Global. We acknowledge logistic support from CIECO-UNAM

and Chajul Field Station.We thank Jorge Rodrıguez, Gilberto Jamangape and

Praxedis Sinaca for help with fieldwork. MMR thanks DGAPA-UNAM and

CONACYT for sabbatical fellowships at the University of California at

Berkeley. Finally, we thank the Editors and anonymous reviewers for their

valuable suggestions.

References

Anderson, H., Galeano, G. & Bernal, R. (1997) Field Guide to the Palms of the

Americas. PrincetonUniversity Press, New Jersey, USA.

Anten, N.P.R. & Ackerly, D.D. (2001) Canopy-level photosynthetic compen-

sation after defoliation in a tropical understorey palm. Functional Ecology,

15, 252–262.

Anten, N.P.R., Martinez-Ramos, M. & Ackerly, D.D. (2003) Defoliation and

growth in an understory palm: quantifying the contributions of compensa-

tory responses.Ecology, 84, 2905–2918.

Ataroff, M. & Schwarzkopf, T. (1992) Leaf production, reproductive patterns,

field germination and seedling survival in Chamaedorea bartlingiana, a

dioecious understorey palm.Oecologia, 92, 250–256.

Belsky, A., Carson,W., Jensen, C. & Fox, G. (1993) Overcompensation by plants

– herbivore optimization or red herring.Evolutionary Ecology, 7, 109–121.

Boege, K. (2005) Influence of plant ontogeny on compensation to leaf damage.

American Journal of Botany, 92, 1632–1640.

Bridgewater, S.G.M., Pickles, P., Garwood, N.C., Penn, M., Bateman, R.M.,

Morgan, H.P., Wicks, N. & Bol, N. (2006) Chamaedorea (Xate) in the

Greater Maya Mountains and the Chiquibul Forest Reserve, Belize: an

economic assessment of a non-timber forest product. Economic Botany, 60,

265–283.

Canham, C.D., Kobe, R.K., Latty, E.F. & Chazdon, R.L. (1999) Interspecific

and intraspecific variation in tree seedling survival: effects of allocation to

roots versus carbohydrate reserves.Oecologia, 121, 1–11.

Case, A.L. & Ashman, T.L. (2007) An experimental test of the effects of

resources and sex ratio onmaternal fitness and phenotypic selection in gyno-

dioeciousFragaria virginiana.Evolution, 61, 1900–1911.

Cepeda-Cornejo, V. & Dirzo, R. (2010) Sex-related differences in reproductive

allocation, growth, defense and herbivory in three dioecious neotropical

palms.PLoSONE, 5, 3.

Chazdon, R. (1991) Effects of leaf and ramet removal on growth and reproduc-

tion ofGeonoma congesta, a clonal understorey palm. Journal of Ecology, 79,

1137–1146.

Coley, P.D., Bryant, J.P. & Chapin III, S. (1985) Resource availability and

plant antiherbivore defense. Science, 230, 895–899.

Crawley,M. (2007)TheR Book. JohnWiley & Sons Ltd, Chichester, UK.

Cunningham, S.A. (1997) The effect of light environment, leaf area, and stored

carbohydrates on inflorescence production by a rain forest understory palm.

Oecologia, 111, 36–44.

Easterling, D.R., Meehl, G.A., Parmesan, C., Changnon, S.A., Karl, T.R. &

Mearns, L.O. (2000) Climate extremes: observations, modeling, and

impacts. Science, 289, 2068–2074.

Eguiarte, L., Burquez,A., Rodrıguez, J.,Martınez-Ramos,M., Sarukhan, J. &Pin-

ero, D. (1993) Direct and indirect estimates of neighborhood and effective popu-

lation size in a tropical palm,Astrocaryummexicanum.Evolution, 47, 75–87.

Endress, B.A., Gorchov, D.L. & Berry, E.J. (2006) Sustainability of a non-tim-

ber forest product: effects of alternative leaf harvest practices over six years

on yield and demography of the palmChamaedorea radicalis. Forest Ecology

andManagement, 234, 181–191.

Endress, B.A., Gorchov, D.L. &Noble, R.B. (2004) Non-timber forest product

extraction: effects of harvest and browsing on an understory palm. Ecologi-

cal Applications, 14, 1139–1153.

Everitt, B.S. &Hothorn, T. (2010)AHandbook of Statistical Analyses Using R.

Chapman andHall ⁄ CRC, London, UK.

Franco, M. & Silvertown, J.J. (2004) A comparative demography of plants

based upon elasticities of vital rates.Ecology, 85, 531–538.

Hawkes, C.V. & Sullivan, J.J. (2001) The impact of herbivory on plants in

different resource conditions: a meta-analysis.Ecology, 82, 2045–2058.

Hodel, D.R. (1992) Chamaedorea Palms. The Species and Their Cultivation.

Allen Press,Kansas.

Holm, J.A., Miller, C.J. & Cropper, W.P. (2008) Population dynamics of the

dioecious Amazonian palm Mauritia flexuosa : simulation analysis of sus-

tainable harvesting.Biotropica, 40, 550–558.

Kobe, R.K. (1997) Carbohydrate allocation to storage as a basis of interspecific

variation in sapling survivorship and growth.Oikos, 80, 226–233.

Lapointe, L., Bussieres, J., Crete, M. & Ouellet, J.P. (2010) Impact of growth

form and carbohydrate reserve on tolerance to simulated deer herbivory and

subsequent recovery in Liliaceae.American Journal of Botany, 97, 913–924.

Lopez-Toledo, L., Horn, C. & Endress, B.A. (2011) Distribution and popula-

tion patterns of the threatened palm Brahea aculeata in a tropical dry forest

in Sonora,Mexico.Forest Ecology andManagement, 261, 901–1910.

Marquis, R. (1984) Leaf herbivores decrease fitness of a tropical plant. Science,

226, 537–539.

Martınez-Ramos, M., Anten, N.P.R. & Ackerly, D.D. (2009) Defoliation and

ENSO effects on vital rates of an understorey tropical rain forest palm.

Journal of Ecology, 97, 1050–1061.

McNaughton, S. (1983) Compensatory plant-growth as a response to herbiv-

ory.Oikos, 40, 329–336.

McPherson, K. &Williams, K. (1998) The role of carbohydrate reserves in the

growth, resilience, and persistence of cabbage palm seedlings (Sabal

palmetto).Oecologia, 117, 460–468.

Mendoza, A., Pinero, D. & Sarukhan, J. (1987) Effects of experimental defolia-

tion on growt, reproduction and survival of Astrocaryum mexicanum.

Journal of Ecology, 75, 545–554.

Obeso, J.R. (2002) The costs of reproduction in plants. New Phytologist, 155,

321–348.

Oyama, K. & Dirzo, R. (1988) Biomass allocation in the dioecious tropical

palm Chamaedorea tepejilote and its life history consequences. Plant Species

Biology, 3, 23–33.

Oyama, K. & Mendoza, A. (1990) Effects of defoliation on growth, reproduc-

tion and survival of a netropical dioecious palm, Chamaedorea tepejilote.

Biotropica, 22, 119–123.

Pinero, D., Sarukhan, J. & Alberdi, P. (1982) The costs of reproduction in a

tropical palmAstrocaryummexicanum. Journal of Ecology, 70, 473–481.

Pinheiro, J. & Bates, D.M. (2000) Mixed-effects Models in S and S-Plus.

Springer-Verlag, NewYork, USA.



Poorter, L. (1999) Growth responses of 15 rain-forest tree species to a light

gradient: the relative importance of morphological and physiological traits.

Functional Ecology, 13, 396–410.

RDevelopment Core Team (2010)R:ALanguage and Environment for Statisti-

cal Computing. R Foundation for Statistical Computing, Vienna, Austria,

http://www.R-project.org.

Sampaio, M.B. & Scariot, A. (2010) Effects of stochastic herbivory events on

population maintenance of an understorey palm species (Geonoma schotti-

ana) in riparian tropical forest. Journal of Tropical Ecology, 26, 151–161.

Sanchez-Carrillo, D. &Valtierra-Pacheco, E. (2003) Social organization for the

exploitation of camedor palms (Chamaedorea spp.) in the Lacandona rain-

forest, Chiapas.Agrociencia, 37, 545–552.

Zuidema, P.A., De Kroon, H. & Werger, M.J.A. (2007) Testing sustainability

by prospective and retrospective demographic analyses: evaluation for palm

leaf harvest.Ecological Applications, 17, 118–128.

Received 4 September 2011; accepted 4May 2012

Handling Editor: Luis Santamaria

Supporting Information

Additional Supporting Information may be found in the online

version of this article.

Figure S1. Climate inter-annual (1994–2003) variation at the Chajul

Biological Station, southeasternMexico.

Figure S2.Relationships between leaf persistency and stem length for

recoveringChamaedorea elegans palms subjected to different defolia-

tion levels.

Figure S3.Relationships between leaf length and stem length for reco-

vering Chamaedorea elegans palms subjected to different defoliation

levels.

Figure S4. Temporal changes in mortality rate of recoveringChamae-

dorea elegans palms as a function of defoliation treatments and stem

length.

Figure S5. Relationships between mean annual fruit production and

stem length for recovering Chamaedorea elegans female palms

subjected to different defoliation treatments in south-eastMexico.

As a service to our authors and readers, this journal provides support-

ing information supplied by the authors. Such materials may be

re-organized for online delivery, but are not copy-edited or typeset.

Technical support issues arising from supporting information (other

thanmissing files) should be addressed to the authors.



Date post:	19-Nov-2023
Category:	Documents
Upload:	independent
View:	0 times
Download:	0 times

Resilience to chronic defoliation in a dioecious understorey tropical rain forest palm

Documents