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Section of Ecology and Biodiversity, Institute of. Environmental Biology ... ferent fitness components are an important part of a species' life-history strategy, and ...
Journal of Ecology 2012, 100, 1544–1556

doi: 10.1111/j.1365-2745.2012.02011.x

Defoliation and gender effects on fitness components in three congeneric and sympatric understorey palms Juan C. Hernández-Barrios1, Niels P. R. Anten2,3, David D. Ackerly4 and Miguel Martínez-Ramos1,4* 1

Centro de Investigaciones en Ecosistemas, Universidad Nacional Autonóma de México, Campus Morelia, Antigua Carretera a Pátzcuaro 8701, 58190, Morelia, Michoacán, México; 2Section of Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, PO Box 80084, 3508 TB, Utrecht, The Netherlands; 3Centre for Crop System Analysis, Wageningen University, PO Box 430, 6700 AK, Wageningen, The Netherlands; and 4Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, 94720, USA

Summary 1. Rain forest understorey perennial plants can be frequently exposed to leaf area losses induced by herbivory or physical damage from falling canopy debris. In dioecious species, tolerance to defoliation may differ between genders (e.g. females may suffer more than males), but this topic has so far received little attention. 2. Here, we quantified gender-dependent effects of increased levels (0–100%) of sustained defoliation (applied bi-annually for 2 years) on vital rates in three economically important dioecious understorey palm species in the genus Chamaedorea (C. elegans, C. ernesti-augustii and C. oblongata). We also quantified gender differences in functional and life-history traits and assessed the direct reproductive costs in terms of biomass allocation to reproduction. 3. In the three species, non-defoliated (control) females were smaller and had three to seven times higher reproductive allocation than males. 4. Defoliation did not affect survivorship in any of the three species, except in the 100% defoliation treatment. Stem growth (RGR) and especially reproduction (probability of reproduction and reproductive output) were negatively affected by defoliation. Females of C. ernesti-augustii suffered higher mortality than males at 100% defoliation, but this was not the case for the other two species. Also, only in C. ernesti-augustii females exhibited lower RGR than males. In all species, the probability of reproduction did not differ between genders. The reproductive output (production rate of inflorescences) differed among genders only in C. ernesti-augustii, where males were more productive than females. 5. Interestingly, in most cases, defoliation effects on vital rates did not differ significantly between males and females, indicating that tolerance to defoliation was similar between genders. Such results were independent of plant size (stem length). 6. Synthesis. Our results do not support the prevailing theory that the greater reproductive costs of females will lead to reduced tolerance to stresses such as defoliation. The implications of these results and their importance for designing sustainable leaf harvesting regimes are discussed. Key-words: biomass allocation, Chamaedorea, compensatory growth, dioecious species, mexico, plant development and life-history traits, reproductive ecology, Selva Lacandona

Introduction The understanding of species responses to changes in resource availability and environmental stress represents a central topic in ecology and conservation biology (Hawkes & Sullivan 2001; Wise & Abrahamson 2007). As resources for plants are *Correspondence author. E-mail: [email protected]

often in short supply in natural conditions, fitness of individuals depends on the allocation of limited resources to mantainance, growth and reproductive functions (Bazzaz, Ackerly & Reekie 2000). Patterns of resource use and allocation to different fitness components are an important part of a species’ life-history strategy, and such patterns may mediate responses to environmental heterogeneity and physical damage (Stearns 1992). Also, in dioecious species, allocation patterns may

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

Defoliation and gender effects on fitness 1545 differ between sex morphs depending on resource availability and gender-specific costs of reproduction. Females tend to expend a large amount of resources in fruiting, and this investment may incur trade-offs with allocation to growth and survival (Thomas & LaFrankie 1993; Obeso 2002; Queenborough et al. 2007). Understorey rain forest plants are frequently exposed to leaf losses through herbivory (Coley & Barone 1996; CepedaCornejo & Dirzo 2010) and falling canopy debris (MartínezRamos et al. 1988; Clark & Clark 1991). However, negative effects produced by such damages on vital rates are often small or negligible, indicating that understorey plants exhibit some degree of tolerance to defoliation (e.g. Chazdon 1991; Marquis, Newell & Villegas 1997; Endress, Gorchov & Peterson 2004; Martínez-Ramos, Anten & Ackerly 2009). Overall, compensatory reponses to defoliation in such plants tend to favour survivorship and growth at the expense of reproduction (Marquis, Newell & Villegas 1997; Anten, Martínez-Ramos & Ackerly 2003; Bloor & Grubb 2003). On the basis of life history and resource allocation theories (Stearns 1992), one would expect tolerance threshold levels of defoliation beyond which individuals are no longer capable of compensating to sustain their vital rates (Anten, Martínez-Ramos & Ackerly 2003). Because a higher allocation to reproduction may reduce resources available for compensatory responses, at higher defoliation intensities females may suffer higher mortality, slower growth and/or lower rates of reproduction than males (Obeso 2002). It has been argued that both intra- and interspecific trade-offs exist between the two herbivory-related strategies: resistence (chemical and mechanical traits that reduce the chance of herbivory; Agrawal 1998) and tolerance (maintenance of fitness under leaf or other biomass losses; Strauss & Agrawal 1999). The Neotropical palm genus Chamaedorea is a useful study system to address these questions. Species are dioecious, and leaves are harvested commercially so plants experience a wide range of defoliation levels. Studies on C. alternans (Oyama & Dirzo 1988), C. ernesti-augustii (Bullock 1984) and C. pinnatifrons (Cepeda-Cornejo & Dirzo 2010) have found that females allocate more biomass to reproduction and exhibit lower growth rates compared with males. These differences were associated with greater leaf toughness, higher phenolics concentration and a lower incidence of herbivory in females than males (Cepeda-Cornejo & Dirzo 2010). Our group has conducted experimental defoliation studies of several other Chamaedorea species, and in previous papers, we have reported that C. elegans plants can maintain survival rates in response to repeated defoliation but exhibit strong reductions in reproduction (Anten & Ackerly 2001a,b; Anten, MartínezRamos & Ackerly 2003). In addition, effects of defoliation on this species can be aggravated by drought (Martínez-Ramos, Anten & Ackerly 2009) and may persist for several years after defoliation has ended (López-Toledo et al. 2012). Yet, the extent to which defoliation tolerance differs between genders has not been investigated. As noted earlier, people harvest leaves of understorey palms for various uses, and harvesting can be intense (a large

percentage of leaves removed) and persistent (harvesting over many years; Hodel 1992; Neumann & Hirsch 2000). In Mesoamerica, local residents harvest Chamaedorea leaves for the floral industry; the leaves are one of the most important non-timber forest products (NTFP) in the region (Bridgewater et al. 2006). Non-sustainable harvesting regimes threaten the viability of the natural populations of these species (CEC 2003). In this article, we studied three sympatric Chamaedorea (C. elegans, C. ernesti-augustii and C. oblongata) species from the tropical rain forest region of south-eastern Mexico, to assess gender-specific demographic responses to increased levels of repeated defoliation (from 0 to 100% leaf removal), bracketing the levels at which natural herbivory and leaf harvesting occur. As we will document here, in natural populations, females of these three species are smaller and have much higher reproductive allocation than males. Therefore, we hypothesized that females have higher costs of reproduction, expressed as lower tolerance to defoliation, than males. The central questions that we addressed were as follows: what are the effects of different levels of repeated defoliation on survivorship, growth and reproduction of female and male individuals? Does the reproductive function of female individuals imply higher costs in terms of growth, survival and reproduction than that of males? Therefore, are female individuals less tolerant to repeated defoliation than males? And, to what extent are there differences in these responses to defoliation among closely related species? We also discuss the implications of our results for developing criteria for sustainable leaf harvesting regimes.

Materials and methods SPECIES AND SITE DESCRIPTION

The genus Chamaedorea is the largest palm genus in the Neotropics (Hodel 1992). Chamaedorea elegans Mart., C. oblongata Mart., and C. ernesti-augustii Wendl., are dioecious and occur in the understorey of the tropical rain forests in south-eastern Mexico and parts of Central America (Henderson, Galeano & Bernal 1995). The three species have a single stem with monopodial growth. Chamaedorea elegans, C. ernesti-augustii and C. oblongata reach a maximum height of 1.5, 2.5 and 4 m, respectively. Chamaedorea elegans and C. oblongata have compound pinnate leaves, whereas C. ernesti-augustii has simple and profoundly bifid leaves. Average fruit production varies considerably between the three species, from about 50 fruits per infructesence in C. ernesti-augustii and C. elegans, to up to 400 fruits per infructescence in C. oblongata. Natural herbivory damage typically ranges from 1% to 23% in Chamaedorea species (MartínezRamos, Anten & Ackerly 2009; Cepeda-Cornejo & Dirzo 2010), but local people (xateros) usually return to the same palm once or twice a year to collect 30–100% of all standing leaves (Reining et al. 1992). Field experiments were conducted in three old-growth tropical rain forest sites, located in Chiapas, Mexico, at the Chajul Biological Station (CBS) in the Montes Azules Biosphere Reserve (16°06′ N, 90°56′ W) and the Lacantún Biosphere Reserve (LBR; 16°37′N, 90° 58′W). During 1980–2009, mean annual temperature was 24.1 °C, and the annual precipitation was 2850 mm with a dry season

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

1546 J. C. Hernández-Barrios et al. (monthly precipitation < 100 mm) from February to April at both locations (climate data from the Lacantún meteorological station; 16° 08′N, 90°54′W, 160 m a.s.l.). The dominant vegetation in these sites is tropical lowland rain forest. We selected three forest sites (two in CBS and one in LBR), where permanent plots were established to include natural undisturbed populations of the Chamaedorea species under study. Because the species are distributed differentially across geomorphological landscape units (M. Martínez-Ramos, unpubl. data), each species was studied in a different location. For C. elegans and C. oblongata, plots were established near the CBS in March 1997 and October 1997, respectively. Plots for C. elegans (ten of 20 9 50 m each, covering an area of c. 1 ha) were located on well-drained, karstic soils at about 300 m a. s.l. (see Martínez-Ramos, Anten & Ackerly 2009), whereas plots for C. oblongata (nine 20 9 50 m plots for a total of 0.9 ha) were located on a sandy, slightly hilly, lowland forest site, at about 100 m a.s.l. The C. ernesti-augustii plots (two of 50 9 50 m for a total of 0.5 ha) were established in the LBR in January 2006, on a location with a well-drained, karstic soil in a slightly hilly area, at about 525 m a.s.l. Sites were chosen so that they represented the typical habitat in which each species grows (Hodel 1992), and consequently they differed in forest structure and species composition (IbarraManríquez & Martínez-Ramos 2002). Within their specific habitat, C. elegans and C. oblongata can reach population densities of up to 1000, and C. ernesti-augustii up to 1600 mature individuals per hectare (M. Martínez-Ramos & J. C. Hernández-Barrios, unpubl. data).

EXPERIMENTAL METHODS

Study system Within permanent plots, we selected a total of 1269 palms divided in 627, 411 and 231 reproductive individuals of C. elegans, C. oblongata and C. ernesti-augustii, respectively. Table S1 in Supporting Information shows details of sample sizes used per species, gender and defoliation treatment. Stem length (measured from the apex to the ground), number of leaves, reproductive status, length of the most recent fully expanded leaf and unopened inflorescence spike were measured at the initial census. The newest leaf was tagged at this and all subsequent censuses to record leaf production. Each plant was then subjected to one of five defoliation treatments: 0 (control, no leaves removed), 33%, 50%, 66% and 100% of the leaves removed. As an exception, in C. ernesti-augustii, the 33% and 66% treatments were replaced by 25% and 75% treatments, respectively. In C. elegans and C. ernesti-augustii, plants were equally divided over the treatments, except for the 100% level where there were half as many individuals as in the other treatments (Table S1). This was because we expected most of the 100% defoliated plants to die. For C. oblongata, due to the considerable heterogeneity in plant size (N. P. R. Anten unpubl. data), we assigned more plants to the control and 50% defoliation level than to the other treatments to ensure adequate sample sizes for statistical analysis at least at these treatment levels (Table S1). In our samples, female-to-male ratio was not different from a 1 : 1 ratio, both at whole sample level and at each defoliation treatment within each species (Table S1). The treatments were imposed by removing the youngest fully expanded leaf and then moving down the stem, removing every fourth (25%), every third (33%), every other (50%), two of every three leaves (66%), three of every four (75%) or all leaves (100%), depending on the species and treatment. Subsequently, every 6 months over 2 years, we repeated the assigned treatment on each individual, but only on the newly produced leaves. Treatments continued for a third year in C. oblongata and

C. elegans, but only 2 years are reported here for consistency with C. ernesti-augustii. In the second treatment year for the former species (1998), the region experienced a significant El Niño Southern Oscillation (ENSO) drought; in a previous paper, we showed that mortality, growth and infloresence production increased during the drought, independent of gender, but fruit production declined for C. elegans during the ENSO year (Martínez-Ramos, Anten & Ackerly 2009). At each census date, we recorded survivorship, stem length, number of leaves produced, rachis length of newly produced leaves, and inflorescence and infructescence production. Leaf area was estimated non-destructively using allometric relationships. For C. elegans and C. oblongata with pinnate leaves, the potential allometric relationship used was of the form y = axb, where x is the length of the leaf lamina and a and b are coefficients (for C. elegans a = 2.12 9 10 5 and b = 1.995; for C. oblongata a = 3.88 9 10 5 and b = 1.897). In the case of C. ernesti-augustii with simple leaves, an exponential allometric relationship of the form y = aebx was used, where x is the length of rachis, and a and b are coefficients (a = 128.57; b = 0.073). In all cases, r2 was greater than 0.86 (see also Anten & Ackerly 2001a).

Dry weight and reproductive allocation We collected a sample of five reproductive individuals (i.e. bearing inflorescences or infructescences) per gender for each species. All plants were selected from the area surrounding the study sites; their heights were close to the mean heights of adult plants of each species found in our experimental plots. Roots were carefully dug out and washed. Each individual was separated into leaves (rachis and lamina), stems and roots. Since the whole reproductive tissue (i.e. inflorescence rachis and fruits for females, and inflorescence rachis and flowers for males) could not be collected at once in these individuals, a sample of 10 inflorescences or infrutescenses per gender per species was obtained from different individuals during their respective reproductive season. Total fruit dry weight per female was estimated by quantifying the mean dry weight of a fruit per species times the mean annual number of fruits produced per female per species. Mean fruit dry weight was obtained from a sample of 100 fruits collected from 10 females of each species; all fruits were dried at 70 °C during 72 h. The mean number of fruits per infructescence was obtained by counting the fruits and fruit scars in the 10 infructescences collected per species. Mean annual fruit production per female was then calculated by multiplying the mean number of fruits per infructescence by the mean number of infructescences produced over a reproductive season. The dry weight of infructescences (rachis plus fruits) in females and that of inflorescences (rachis plus flowers) for males was considered as the biomass allocated to reprodution. Finally, the estimated reproductive biomass was added to the vegetative biomass to obtain the total dry weight per plant, as well as the reproductive shoot (stem plus leaves) and root proportions per gender of each species.

STATISTICAL ANALYSIS

Defoliation and gender effects on response variables were assessed over the 2-year experimental period for each species. We used generalized linear models (GLM) to test the islolated and interactive effects of gender and defoliation. We also used stem length as a covariate to assess the effect of plant size on the responses of genders to defoliation treatments. In these models, defoliation (D, 0–100%) and stem length were considered a continuous regressor and gender (G) a fixed factor with two levels (females and males). Response variables were

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

Defoliation and gender effects on fitness 1547 survivorship probability, growth (stem growth, number of leaves produced, leaf rachis length and leaf area production per individual), the probability of reproduction and reproductive output (inflorescence or infructescence production per male or female, respectively, during the second year of experimental defoliation). In all the analyses, each individual plant was considered as an experimental unit. Probability of survival was considered a binomial variable, assigning 1 when the individual was alive or 0 when it was dead after 2 years since the first defoliation event. Probability of reproduction was also considered a binomial response variable, using 1 if the individual produced inflorescences (males) or infructescences (females) or 0 when it failed to produce any reproductive structure during the second year after starting defoliation. For these two binomial variables, we used a logit link function (Crawley 1993) of the form Y = exp(X)/[1 + exp(X)] where X = (a + bD + cD2 + dG + eSL + fD*G + gD2*G + hD*SL + iD2*SL + jG*SL + kD2*G*SL), and a is the origin ordinate, related to vital rates in absence (0%) of defoliation, b and c assess the effects of defoliation (D and D2), d the effects of gender (G), e the effect of plant size (stem length), f and g the interactive effects of defoliation and gender, h and i the interactive effects of defoliation and plant size, j the interactive effect of gender and plant size, and k the interactive effect of defoliation, gender and plant size. We introduced the quadratic term D2 to test for nonlinear effects of defoliation, in the context of the logit model (which is itself nonlinear). When coefficients cg, i and/or k are not different from zero, the magnitude of the defoliation effects remains similar across the defoliation levels. When these coefficients are significantly positive or negative, the magnitude of the effects decreases or increases with defoliation level, respectively. Differences in the response of female and male palms to defoliation are indicated by significant interaction gender 9 defoliation terms (i.e. significant nonzero f, g and or k values). Growth was calculated as the relative increase in length of stems (RGR), the number of leaves produced per individual, the average leaf rachis length of newly produced leaves and the cumulative leaf area production per individual over 2 years since the initial defoliation date. RGR was used instead of absolute stem growth to take into account differences in stem length among individuals. RGR was calculated as [ln(SL1) ln(SL2)]/t with SL1 and SL2 the stem length before and after time interval t, respectively. Reproductive output was quantified as the annual production of inflorescences per male, or immature and mature infructescences per female, during the second year after initial defoliation. Growth variables (except for leaf production) were considered to have a normal error, and effects of independent variables were assessed using an identity link function of the form Y = a + bD + cD2 + dG + eSL + fD*G + gD2*G + hD*SL + iD2*SL + jG*SL + kD2*G*SL. Leaf production and reproductive output were considered to have a Poisson error, and effects of independent variables were assessed using a logarithmic link function of the form Y = exp (a + bD + cD2 + dG + eSL + fD*G + gD2*G + hD*SL + iD2*SL + jG*SL + kD2*G*SL). The coefficients of these models have the same meaning as those described earlier. In all GLM analyses, significance of independent variables was evaluated by considering the deviance (c. v2) explained by each model term. We introduced all terms and then removed the non-significant ones. The software JMP.10 (SAS Inc., Cary, NC, USA) was used for all GLM analyses. Finally, to assess whether sex ratios changed after 2 years of sustained defoliation (due to differential mortality), for each species we conducted contingency table (v2) analyses where gender (females and males) were columns and defoliation treatments (five levels) were the rows; we tested the null hypothesis that the frequency of each gender was independent of defoliation treatment.

Results GENDER DIFFERENCES IN FUNCTIONAL AND LIFE-HISTORY TRAITS

Table 1 shows a summary of life-history and functional traits of the three studied species, quantified based on our control (non-defoliated) experimental palms. The species are relatively long-lived with an estimated life span of about 40– 75 years. In the three species, males had higher values than females for most measured traits. In the three species, males allocated more biomass to aerial parts (leaves and stem) than females, although this difference was not significant in C. elegans (Table 1). Reproductive allocation was threefold higher in females than in males in C. elegans and C. ernesti-augustii and sevenfold higher in C. oblongata (Table 1). EFFECTS OF DEFOLIATION ON SURVIVORSHIP AND SEX RATIO

In C. elegans and C. oblongata survivorship probability showed a concave reduction with increasing defoliation (Fig. 1), and both the linear and quadratic defoliation GLM terms were significant; survivorship was affected by defoliation only at 100% leaf removal (Table 2). In both species, survivorship was not significantly affected by gender. By contrast, in C. ernesti-augustii, the effect of defoliation depended on gender (significant gender 9 defoliation interaction; Table 2), with female palms suffering higher mortality than male ones at 100% defoliation. This defoliation level reduced survivorship much less in C. ernesti-augustii (23%) than in the other two species (70–90% reduction; Fig. 1). Stem length had a significant effect on survivorship probability only in C. elegans, but this effect was independent of gender and defoliation (Table 2); overall, survivorship reduced as stem length increased (Fig. S1, Supporting Information). After 2 years of sustained defoliation, the sex ratio of surviving palms was not significantly different from 1 : 1 in any of the defoliation treatments or species (Table S2). EFFECTS OF DEFOLIATION ON RELATIVE GROWTH RATE

In general, growth rates of all species were reduced at higher defoliation levels compared to the values of undefoliated palms. Stem growth (RGR) was affected by defoliation only at the highest intensities of leaf harvesting in all three species as indicated by the significance of the quadratic defoliation term in the GLM (Fig. 2; Table 2). Males exhibited higher RGR than females only in C. ernesti-augustii. Defoliation effects on RGR did not differ between genders in any of the species, but defoliation effects consistently depended on plant size. At high defoliation levels (> 50%), large individuals of C. oblongata and C. elegans suffered higher reductions in growth than small ones, while in C. ernesti-augustii the contrary was observed (Fig. S2).

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

1548 J. C. Hernández-Barrios et al. Table 1. Functional and life-history traits of female and male individuals from natural populations of three Chamaedorea species in southern Mexico. Mean (± SE) values correspond to mature, non-defoliated (control) palms from our experimental study (sample sizes in Table S1). Longevity was estimated using stem length growth and relationships between age and size (Lieberman & Lieberman 1985). Within species, values for genders not sharing same superscript letters differed significantly at P  0.05, according to Student’s t-test (continuous variables), chi-square (count variables) or Mann–Whitney U (biomass allocation components, shown as proportions) tests C. elegans Females (a) Functional traits Stem length (m) Number of leaves Leaf length (cm) Total leaf area (m2) (b) Life-history traits Sex ratio (females/males) Maximum height (m)* Longevity (years)* Reproductive output (inflor. year 1) Stem length growth (cm year 1) Total biomass (g)† Aerial biomass allocation Root biomass allocation Reproductive allocation

0.39 5.4 31.8 0.03

± ± ± ±

0.99 1.4 50 1.0 ± 2.7 ± 31.5 ± 0.67 ± 0.16 ± 0.17 ±

0.01a 0.1a 0.3a 0.001a

0.1a 0.1a 5.3a 0.03a 0.02a 0.03b

C. ernesti-augustii Males

0.44 6.1 32.5 0.04

0.9 3.2 36.4 0.71 0.24 0.05

± ± ± ±

± ± ± ± ± ±

Females

0.01b 0.2b 0.3b 0.001b

0.87 6.2 37.3 0.36

0.1a 0.1b 10.4a 0.04a 0.05a 0.01a

1.08 2.5 70 2.3 ± 2.9 ± 167.6 ± 0.58 ± 0.20 ± 0.21 ±

± ± ± ±

0.03a 0.1a 0.8a 0.01a

0.2b 0.3a 17.1a 0.03a 0.04a 0.03b

C. oblongata Males

0.90 6.7 39.5 0.48

1.5 2.7 175.2 0.72 0.22 0.05

± ± ± ±

± ± ± ± ± ±

Females

Males

0.03a 0.1b 0.6b 0.01b

2.25 4.7 56.0 0.41

± ± ± ±

0.08a 0.1a 0.1b 0.02b

2.25 4.8 48.9 0.32

± ± ± ±

0.32a 0.1a 0.1a 0.01a

0.2a 0.3a 10.6a 0.03b 0.03a 0.00a

1.09 3.6 45 0.4 ± 5.7 ± 145.7 ± 0.56 ± 0.17 ± 0.27 ±

0.1a 0.3a 11.7b 0.02a 0.01a 0.02b

0.8 6.7 96.3 0.77 0.20 0.04

± ± ± ± ± ±

0.2b 0.4b 8.0a 0.01b 0.02a 0.00a

*Values correspond to both genders. † Values correspond to dry matter based on a sample size of five individuals per gender (see Materials and Methods).

Defoliation negatively affected leaf production rates in C. elegans and C. oblongata, but not in C. ernesti-augustii (Table 2). The effects of defoliation and gender on leaf attributes were more evident on leaf size, measured as leaf rachis length, leaf area and the total leaf area produced per palm (Tables 2 & 3); defoliation treatments progressively reduced rachis length of newly produced leaves, and consequently reduced leaf area production as well. Overall, female palms tended to produce smaller leaves in C. elegans and C. ernesti-augustii, but the opposite was true in C. oblongata (Table 3). These gender effects were independent of defoliation in C. oblongata (no significant gender 9 defoliation terms; Table 2). In the other two species, we detected significant defoliation 9 gender effects when plant size was included in the GLM analysis (Table 2). In females of C. elegans, the negative effect of defoliation on leaf size and leaf area production rate declined as the size of the individuals increased, while in males, such reduction was non-existent or less apparent (Fig. S3); such gender and size-dependent effects were similar for leaf area production in C. ernesti-augustii (Fig. S4). In C. oblongata, there was a significant reduction in leaf rachis length (model: LRL = 63.4 0.024*SL, in cm), leaf area (LA = 0.027 0.000017*SL, in m2) and leaf area production (LAP = 0.22 0.00018*SL, in m2 ind 1 year 1) as stem length (SL, cm) increased, independently of gender and defoliation (Table 2). EFFECTS OF DEFOLIATION ON REPRODUCTIVE COMPONENTS

In the three species, both the probability of reproduction and the reproductive output declined progressively with

increasing defoliation (Fig. 3). The quadratic defoliation GLM term was significant in most cases (Table 2). Overall, 100% defoliation reduced reproductive values to zero or close to zero. For all species, the effects of defoliation on the probability of repoduction did not differ between genders (Table 2). In C. ernesti-augustii (but not in the other two species), male individuals exhibited higher reproductive output than females at defoliation levels lower than 66%, but the opposite was observed at 100% defoliation (Fig. 3; significant interaction defoliation 9 gender term Table 2). Chamaedorea oblongata exhibited considerably lower probabilities of reproduction than the other two species (Fig. 3). Finally, plant size effects were detected only in C. elegans (Table 2); both the probability of reproduction (model: PR = exp (1.07 + 0.019*SL)/1 + exp(1.07 + 0.019*SL)) and the reproductive output (RO = exp(0.39 + 0.0052*SL)) increased with stem length (SL, cm). OVERALL RELATIVE EFFECTS OF DEFOLIATION ON VITAL RATES

Figure 4 illustrates the patterns of relative change in vital rates (relative to those of undefoliated palms) in response to increased levels of repetitive defoliation, averaging data from the three studied Chamaedorea species. Defoliation effects on demographic rates followed a clear consistent pattern across all three species with the negative effects on reproduction being strongest, followed by growth (as measured by stem RGR), while the effects on survivorship were the weakest.

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

Survivorship probability (ind ind–1 2-year–1)

Defoliation and gender effects on fitness 1549 Chamaedorea elegans

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Fig. 1. Effects produced by increased levels of sustained defoliation (0%, 25–33%, 50%, 66–75%, 100%; applied every 6 months) on the survivorship probability of female (black dots) and male (open dots) individuals of three Chamaedorea species in southern Mexico. The solid line represents the adjusted generalized linear model for females, and the dashed line represents the model adjusted for males. Solid line only means that the model corresponds to both genders. Error bars correspond to one standard error.

Discussion In our studied Chamaedorea species, leaf harvesting is likely the most important cause for photosynthetic area loss. Our experiment bracketed the levels at which leaves are harvested by local people (Reining et al. 1992). Defoliation levels in

our treatments were somewhat high compared to the mean levels of natural herbivory (1–23% of leaf damage) that have been recorded for Chamaedorea palms (Martínez-Ramos, Anten & Ackerly 2009; Cepeda-Cornejo & Dirzo 2010), but stochastic events such as insect outbreaks, falling branches, strong storms, vertebrate browsing and fire may cause severe leaf area losses in these species (Coley, Bryant & Chapin 1985; McPherson & Williams 1998; López-Toledo, Horn & Endress 2011). In the three studied, Chamaedorea species repeated defoliation below 66–75% leaf removal did not significantly affect survivorship and had only modest effect on growth, indicating that with respect to these vital rates the species exhibited a high degree of tolerance to defoliation, even if defoliation is both intense and persistent. Interestingly the consequences of defoliation were similar between genders in most analysed fitness components, and this pattern was independent of plant size. As such, our results do not support the prevailing theory that the greater reproductive costs of females will lead to reduced tolerance to stresses such as defoliation (Obeso 2002; Cornelissen & Stiling 2005; Cepeda-Cornejo & Dirzo 2010). The literature on inter-sex cost of reproduction among closely related species is limited (Thomas & LaFrankie 1993; Queenborough et al. 2007), especially on issues related to plant compensation to sustained defoliation. In this context, we highlight the contribution of our work that employed similar defoliation treatments imposed under natural conditions on three sympatric and congeneric palm species, with a high number of experimental individuals within each species. It should be noted that the populations of the three species grew at sites with different conditions (e.g. different soil types, see Materials and Methods). This reflects the fact that we intended to study species in their typical habitat. Within each habitat, female and male individuals grew under similar conditions, so that our estimates of reproductive cost were not environmentally biased. Also, the experiment with C. ernestiaugustii was conducted during different years than that for the other two species. The second year for C. elegans and the first one for C.oblongata was an ENSO year (1998), and we have reported previously that the associated drought led to increased growth and mortality rates in C. elegans (MartínezRamos, Anten & Ackerly 2009). Reproductive investment and associated costs may depend on environmental conditions (see Obeso 2002) and differences between the sites; timing of the experiment may have thus affected our results. Several studies (e.g. Reznick 1985; Biere 1995) suggest that reproductive costs would be most apparent under stressful conditions. One could thus expect that the ENSO-related drought would have exacerbated gender difference in defoliation tolerance, but we saw no evidence of this effect. COMPENSATION ABILITY OF UNDERSTOREY TROPICAL RAIN FOREST SPECIES

Our results concur with studies showing that in tropical rain forest understorey species, intense defoliation events (i.e. up to 50% leaf removal) have no significant negative impact on

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

1550 J. C. Hernández-Barrios et al. Table 2. Results of generalized linear models on the effects of defoliation treatments (D), gender (G) and stem length (SL) on survivorship, growth and reproduction of Chamaedorea elegans, Chamaedorea ernesti-augustii and Chamaedorea oblongata at the Lacandona region, southern Mexico. The term D2 indicates that the magnitude of the defoliation effects change across the defoliation levels. Survivorship and growth (stem relative growth rate (RGR), leaf production, leaf rachis length and leaf area production) correspond to plant response after 2 years of repeated defoliation, while reproductive values correspond only to the second year of experimental treatments. Only significant terms are shown with their corresponding chi-square and their statistical significance (P-value); (–) indicates that such factor was not significant and therefore it was removed from the model C. elegans Trait/Source of variation

v2

Survivorship (ind ind 1 2-year 1) D 6.72 D2 23.22 G – SL 12.81 D*G – Stem RGR (cm cm 1 year 1) D – D2 27.53 G – SL – D*SL 3.83 D2*SL 3.86 Leaf production (lvs ind 1 year 1) D 17.31 D2 – Leaf rachis length (cm) D 8.30 D2 30.10 G 7.36 SL 5.99 D*G*SL 5.93 Average leaf area (m2) D 41.01 D2 – G 9.71 SL 13.44 D*G*SL 4.53 Leaf area production (m2 ind 1 year 1) D 5.66 D2 31.63 G 20.53 SL 9.49 D2*G – D*SL – D*G*SL 5.84 Probability of reproduction (ind ind 1 year 1) D – D2 68.19 SL 14.14 Reproductive output (infl/infruct ind 1 year 1) D – D2 58.22 G – SL 15.30 D*G D2*G

C. ernesti-augustii P

v2

C. oblongata v2

P

P

0.010 < 0.001 – < 0.001 –

15.11 – – – 5.43

< 0.001 – – – 0.019

22.55 42.34 – – –

< 0.001 < 0.001 – – –

– < 0.001 – – 0.050 0.050

3.27 6.80 7.11 57.02 3.70 7.38

0.070 0.009 0.008 < 0.001 0.050 0.007

6.94 8.68 – 158.42 – 4.84

0.008 0.003 – < 0.001 – 0.028

< 0.001 –

– –

– –

4.18 7.25

0.041 0.007

0.004 < 0.001 0.007 0.014 0.015

30.71 29.96 – –

< 0.001 < 0.001 – –

5.12 9.62 20.81 6.53 –

0.024 0.002 < 0.001 0.016 –

< 0.001 – 0.002 < 0.001 0.032

27.13 – 28.53 – –

< 0.001 – < 0.001 – –

9.27 – 23.03 6.27 –

0.002 – < 0.001 0.012 –

0.017 < 0.001 < 0.001 0.002 – – 0.016

– 31.72 31.73 – 3.92 4.39 –

– < 0.001 < 0.001 – 0.047 0.036 –

– 16.06 8.47 10.70 – – –

– < 0.001 0.004 0.001 – – –

– < 0.001 < 0.001

40.25 – –

< 0.001 – –

– 9.67 –

– 0.002 –

– < 0.001 – < 0.001

44.57 – 4.28 – 4.63 5.59

< 0.001 – 0.039 – 0.031 0.018

3.98 8.34 – –

0.047 0.004 – –

survival or growth (Marquis 1984; Mendoza, Piñero & Sarukhán 1987; Oyama & Mendoza 1990; Chazdon 1991; Schierenbeck, Mack & Sharitz 1994; Zuidema & Werger 2000; Dyer, Gentry & Tobler 2004; Endress, Gorchov & Peterson 2004; Bruna & Nogueira 2005; Endress, Gorchov & Berry 2006; Valverde, Hernández-Apolinar & Mendoza-Amaro

2006). However, most of these studies were carried out exploring effects of single defoliation events. There is a scarcity of studies assessing the effects of repeated defoliation on vital rates in natural plant populations (Endress, Gorchov & Peterson 2004; Endress, Gorchov & Berry 2006; Valverde, Hernández-Apolinar & Mendoza-Amaro 2006; Martínez-Ramos,

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

Defoliation and gender effects on fitness 1551

RGR stem length (cm cm–1 year –1)

Chamaedorea elegans 0.09 0.08 0.07 0.06 0.05 0.04 0.03

Females Males

0.02 0.01 0

0

20

40

60

80

100

RGR stem length (cm cm–1 year –1)

Chamaedorea ernesti-augustii 0.09 0.08 0.07 0.06 0.05 0.04 0.03 0.02 0.01 0

0

20

40

60

80

100

RGR stem length (cm cm–1 year –1)

Chamaedorea oblongata 0.09 0.08 0.07 0.06 0.05 0.04 0.03 0.02 0.01 0

0

20

40

60

80

100

Defoliation treatment (%) Fig. 2. Effects produced by increased levels of sustained defoliation on stem relative growth rate (RGR) in stem length of female (black dots) and male (open dots) individuals of three Chamaedorea species in southtern Mexico. The solid line represents the adjusted generalized linear model for females, and the dashed line represents the model adjusted for males. Solid line only means that the model corresponds to both genders. Error bars correspond to one standard error.

Anten & Ackerly 2009). Yet, harvesting, herbivory and other types of damage, such as limb and treefalls, storms and fires, tend to occur, repetitively (Martínez-Ramos et al. 1988; Clark & Clark 1991; van der Meer & Bongers 1996; del-Val & Crawley 2005). Our experiment demonstrates that understorey palm species have the ability to survive, but suffer reductions in growth and reproduction, when subjected to intensive and sustained leaf area losses.

In plants, it is very difficult to relate defoliation tolerance directly to a specific functional mechanism (del-Val & Crawley 2005; but see Wise & Abrahamson 2007). Several compensatory mechanisms have been suggested in this respect, including reduced self-shading (Gold & Caldwell 1990; Anten & Ackerly 2001a; Kikuzama 2003; van Staalduinen & Anten 2005), slow growth life-history adaptations (Kobe et al. 1995; Kobe 1997; Svenning 2002), increase in photosynthetic rates (Crawley 1983; Gold & Caldwell 1990; Strauss & Agrawal 1999; Anten & Ackerly 2001b), change in allocation patterns due to alteration of the leaf area-to-total biomass ratios (Hilbert et al. 1981; Crawley 1983; Gold & Caldwell 1990; Strauss & Agrawal 1999; Anten, Martínez-Ramos & Ackerly 2003), and reserve carbohydrate mobilization (Boege 2005; Ichie et al. 2005). In our study system, survival under defoliation was achieved at the expense of reductions in growth and, predominantly, in reproduction. This result strongly indicates that survival in these understorey palms, subjected to severe and repetitive disturbance, is promoted by reallocation of energy and resources from reproductive and growth functions to functions associated with survival. We observed a sequential response to defoliation that was clearly consistent accross the three studied Chamaedorea species, supporting the existence of a trade-off between survival, growth and reproductive functions, as discussed on theoretical and empirical grounds (Reznick 1985; Obeso 2002; Agrawal 2005; Álvarez-Cansino et al. 2010). Along the range of the experimental defoliation levels, reproduction was progressively and strongly reduced, followed by growth, at and above intermediate defoliation levels, and by an increase in mortality at the highest defoliation levels, when no more resources remained to produce photosynthetic leaf tissues; similar results have been shown for other plant species (Klinkhamer et al. 1992). Modelling studies (e.g. Zuidema, de Kroon & Werger 2007) indicate that in long-lived, slowgrowing organisms such as tropical forest understorey plants, population growth rate is most sensitive to variation in survival, followed by variation in growth, and least sensitive to variation in reproduction. This suggests that the response pattern to repeated defoliation events lasting short time periods, as observed in this study, is adaptive in the sense that compensatory mechanisms preferentially act to mitigate negative impacts of leaf area losses on the most important aspects of demography. However, such compensatory capacity can be lost if leaf area losses continue over periods longer than 2 years, exhausting the stored reserves available for compensation (López-Toledo et al. 2012). Even low levels of tissue loss, persisting over time, may eventually exhaust a plant’s capacity to mobilize stored resources of carbon for maintenance and growth, leading to increases in mortality (Eichhorn et al. 2010). NO EVIDENCE OF LOWER TOLERANCE TO DEFOLIATION IN FEMALES THAN IN MALES

Several studies suggest that due to the greater costs associated with the female reproductive function, females should

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

1552 J. C. Hernández-Barrios et al. Table 3. Mean growth parameters (± SE) of female and male individuals of three Chamaedorea palm species after being subjected to five experimental defoliation treatments (0%, 25–33%, 50%, 66–75%, 100%) applied every 6 months over 2 years in southern Mexico Females Species/Traits C. elegans Leaf production (lvs ind

0% 1

year 1)

Leaf rachis length (cm) Average leaf area (m2 leaf 1) Plant leaf area (m2 ind 1) Leaf area production per plant (m2 ind 1 year 1) C. ernesti-augustii Leaf production (lvs ind

2.6 ±0.05 29.8 ±0.5 0.018 ±0.001 0.085 ±0.003 0.039 ±0.002

1

year 1)

Average leaf area (m2 leaf 1) Plant leaf area (m2 ind 1) Leaf area production per plant (m2 ind 1 year 1) C. oblongata

1.7 ±0.1 22.4 ±0.7 0.07 ±0.003 0.204 ±0.015 0.121 ±0.010

2.5 ±0.05 30.5 ±0.5 0.019 ±0.001 0.097 ±0.004 0.049 ±0.002

year 1)

Leaf rachis length (cm) Average leaf area (m2 leaf 1) Plant leaf area (m2 ind 1) Leaf area production per plant (m2 ind 1 year 1)

1.6 ±0.05 65.7 ±1.1 0.029 ±0.001 0.096 ±0.005 0.185 ±0.009

Males

2.1 ±0.05 29.9 ±0.6 0.019 ±0.001 0.077 ±0.004 0.040 ±0.002

1.8 ±0.1 25.0 ±0.8 0.08 ±0.005 0.282 ±0.022 0.173 ±0.012

1.7 ±0.15 20.3 ±0.9 0.06 ±0.004 0.199 ±0.019 0.119 ±0.010

2.3 ±0.05 30.1 ±0.5 0.019 ±0.001 0.086 ±0.004 0.044 ±0.002

1.6 ±0.05 62.2 ±1.6 0.026 ±0.001 0.085 ±0.006 0.165 ±0.012

be less tolerant to stress than males (e.g. Obeso 2002; Cepeda-Cornejo & Dirzo 2010) and, for some dioecious species, it is believed that a greater stress tolerance of males enables them to establish in more resource-limited microhabitats while females may be constrained to higherquality habitats (Lloyd & Webb 1977; Dawson & Ehleringer 1993, 2002; Bierzychudek & Eckhardt 1988; but see Rocheleau & Houle 2001 and Queenborough et al. 2007 for inconclusive evidence). In contrast, our results show that in these three Chamaedorea species, males and females appear to be similarly tolerant to defoliation. The overall effects of defoliation on fitness components did not differ much between genders. We found evidence that female individuals suffered a higher mortality than males at 100% defoliation, but this result occurred in only one of the three studied species. Also, although growth rate differed between genders, the differences were independent of defoliation in the three species, except for leaf size in C. oblongata. Reproductive output

Males

1.9 ±0.1 29.0 ±0.7 0.018 ±0.001 0.067 ±0.004 0.038 ±0.002

2.1 ±0.15 24.5 ±0.8 0.08 ±0.004 0.287 ±0.027 0.173 ±0.017

1.7 ±0.15 20.1 ±0.8 0.06 ±0.003 0.183 ±0.018 0.107 ±0.009

2.2 ±0.05 30.7 ±0.5 0.019 ±0.001 0.084 ±0.004 0.045 ±0.002

1.8 ±0.05 62.6 ±1.1 0.026 ±0.001 0.097 ±0.004 0.190 ±0.008

Males

1.9 ±0.05 27.5 ±0.6 0.016 ±0.001 0.058 ±0.003 0.032 ±0.002

2.0 ±0.15 23.7 ±0.8 0.07 ±0.005 0.281 ±0.027 0.166 ±0.016

1.5 ±0.1 19.0 ±1.1 0.05 ±0.005 0.156 ±0.015 0.088 ±0.009

2.0 ±0.1 28.4 ±0.6 0.017 ±0.001 0.066 ±0.004 0.038 ±0.002

1.5 ±0.05 55.8 ±1.9 0.022 ±0.001 0.066 ±0.005 0.129 ±0.010

Males

1.1 ±0.1 21.7 ±1.6 0.010 ±0.001 0.024 ±0.004 0.011 ±0.02

1.6 ±0.2 23.8 ±1.2 0.012 ±0.001 0.036 ±0.004 0.015 ±0.002

100% 1.9 ±0.1 21.5 ±0.9 0.06 ±0.004 0.211 ±0.016 0.123 ±0.010

66% 1.9 ±0.05 55.9 ±1.1 0.021 ±0.001 0.080 ±0.004 0.156 ±0.009

Females 100%

75%

50% 1.8 ±0.1 57.5 ±1.7 0.022 ±0.001 0.085 ±0.007 0.165 ±0.014

Females 66%

50%

33% 1.8 ±0.05 56.7 ±1.1 0.022 ±0.001 0.081 ±0.004 0.156 ±0.009

Females 50%

25%

0% 1

Females 33%

0%

Leaf rachis length (cm)

Leaf production (lvs ind

Males

1.3 ±0.3 15.9 ±1.8 0.04 ±0.006 0.113 ±0.030 0.071 ±0.016

1.3 ±0.2 18.8 ±1.1 0.05 ±0.004 0.143 ±0.028 0.084 ±0.020

100% 1.7 ±0.1 55.7 ±1. 8 0.021 ±0.001 0.073 ±0.006 0.145 ±0.012

1.3 ±0.2 48.7 ±3.5 0.017 ±0.002 0.047 ±0.010 0.108 ±0.024

1.0 ±0.2 48.2 ±2.7 0.016 ±0.002 0.034 ±0.008 0.078 ±0.015

(inflorescence production) showed a general decline as defoliation increased, but with two species-specific responses between genders: (i) no gender differences in C. elegans and C. oblongata and (ii) male individuals suffering more than females in C. ernesti-augustii. It should be noted, however, that we did not quantify possible changes in inflorescence and infructescence size (flower or fruit number) or seed size and provisioning, and these aspects would be important for a thorough assessment of defoliation effects on reproduction. Cepeda-Cornejo & Dirzo (2010) showed that female individuals in three Chamaedorea species, including one from our study (C. ernesti-augustii, C. alternans and C. pinnatifrons), allocate more biomass to reproduction and have higher anti-herbivore defences than males. Correspondingly, females exhibited lower growth rates but also suffered lower herbivory rates than males, which was taken as evidence of higher costs of reproduction for the female palms. A higher resource allocation to defence in females

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

Defoliation and gender effects on fitness 1553

Reproductive output (infl ind –1 year –1)

Probability of reproduction (ind ind–1 year –1)

Chamaedorea elegans 1

0.8

0.6

0.4

0.2

Females Males

0 0

20

40

60

80

2.2 2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 0

100

20

40

60

80

100

20

40

60

80

100

40

60

80

100

1

Reproductive output (infl ind –1 year –1)

Probability of reproduction (ind ind–1 year –1)

Chamaedorea ernesti-augustii

0.8

0.6

0.4

0.2

0 0

20

40

60

80

2 1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 0

100

Reproductive output (infl ind –1 year –1)

Probability of reproduction (ind ind–1 year –1)

Chamaedorea oblongata 1

0.8

0.6

0.4

0.2

0

0

20

40

60

80

100

Defoliation level (%)

0.5 0.45 0.4 0.35 0.3 0.25 0.2 0.15 0.1 0.05 0

0

20

Defoliation level (%)

Fig. 3. Effects produced by increased levels of sutained defoliation on the probability of reproduction (left panels) and the reproductive output (right panels) of female (black dots) and male (open dots) individuals of three Chamaedorea species in southern Mexico. The solid line represents the adjusted generalized linear model for females, and the dashed line represents the model adjusted for males. Solid line only means that the model corresponds to both genders. Error bars correspond to one standard error.

can be interpreted as an avoidance or resistance strategy, preventing loss of photosynthetic tissue, which is critical for carbon intake for the construction of expensive reproductive structures (e.g. seeds and ancillary parts of fruits), especially in the light-limited understorey environment.

The study of Cepeda-Cornejo & Dirzo (2010) and ours document that in five Chamaedorea species (C. alternans, C. elegans, C. ernesti-augustii, C. oblongata and C. pinnatifrons), females allocate more biomass to reproduction and grow slower compared to males, supporting the existence of a trade-off between growth and reproduction and indirectly

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

Relative change respect to non-defoliated individuals

1554 J. C. Hernández-Barrios et al. na store more non-structural carbohydrates than males when they are exposed to long periods of high light intensity. A final explanation could be that while males and females exhibited similar tolerance in the short-term (i.e. after 2 years of defoliation), long-term effects could still be stronger in females than in males. Evidence for this comes from an analysis by López-Toledo et al. (2012) following the C. elegans individuals in our study for 3 years of defoliation and 3 years of subsequent recovery. Female palms exhibited lower capacity to recover from defoliation than male palms, even 3 years after the last defoliation event.

1

0.8

0.6

0.4 Survivorship Growth Reproduction

0.2

0

DEMOGRAPHIC IMPLICATIONS OF INTENSIVE LEAF

0

20

40

60

80

100

Defoliation level (%) Fig. 4. Averaged response to experimental defoliation on annual rates of survivorship, growth (measured as leaf area production) and reproduction (probability of reproduction) of three Chamaedorea palm species (C. elegans, C. ernesti-augustii and C. oblongata) relative to the control treatment individual palms’performance. The defoliation treatments ranged from 0% to 100% of the leaves removed per individual, biannually over 2 years. Error bars correspond to one standard error (n = 3).

between growth and defence. However, what is surprising is that our experiments show that tolerance to defoliation, as measured through changes in survival, growth and reproduction rates, was rather similar between genders over a wide range (25–100%) of sustained defoliation levels. The existence of a stress tolerance–avoidance trade-off has been documented with respect to various stressors including herbivory (e.g. Agrawal 1998; Cepeda-Cornejo & Dirzo 2010; SánchezVilas & Pannell 2011). Our results together with those of Cepeda-Cornejo & Dirzo (2010), however, indicate that this trade-off may not necessarily exist across genders. The lack of evidence of a trade-off between tolerance and resistance may indicate that these two strategies can evolve independently (Muola et al. 2010). Several explanations can be forwarded to explain the fact that females in our study exhibited similar defoliation tolerance in spite of their larger reproductive costs. One could be that females exhibit a higher potential for compensatory photosynthesis (e.g. Montesinos et al. 2012) enabling them to better mitigate leaf losses, although there is no evidence for this in C. elegans (Anten & Ackerly 2001a). Nicotra, Chazdon & Montgomery (2003) found in a dioecious understorey shrub that even if males achieve higher photosynthetic rates compared to females, the latter can achieve more carbon gain through producing more leaves and a bigger total leaf area. We observed a similar pattern in C. oblongata (Table 3), whose females produced bigger leaves and had a sevenfold larger resource investment in reproduction than males (Table 1). A second possibility is that females store more carbohydrates than males; as has indeed been shown in another study with C. ernesti-augustii (Bullock 1984). Zhao et al. (2009) also found that females of the dioecious tree Populuscathaya-

HARVESTING REGIMES

The intense levels of disturbance derived from human exploitation of natural resources can have effects beyond individual plants and alter population dynamics. This study showed that palm reproduction diminished significantly with intense and repeated defoliation. As such conditions can persist through many years in commercial extractive practices, eventually this could lead to a lack of fecundity at the population level, both in female and in male individuals. Defoliation in this species causes a reduction in the probability of reproduction in both genders and diminishes the number of fruits produced and even affects fruit quality, as observed in C. ernesti-augustii (J. C. Hernández-Barrios, unpubl. data). For instance, the intensive extraction of fruits of Bertholletia excelsa (Peres et al. 2003), the Brazil nut, from natural populations resulted in a distorted demographic structure, with severely diminished numbers of young individuals, a situation that can threaten long-term population viability. Defoliation can also have effects on male reproductive attributes, as has been documented in Cucurbita texana (Quesada, Bollman & Stephenson 1995), where the number of staminate flowers was reduced, as was the quantity and performance of pollen. Regarding the use of the leaves of these Chamaedorea species as a non-timber forest product (NTFP), based on our results, we suggest extractive limits set at low to intermediate levels (  50% leaves harvested every 6 months), where plants are still capable of compensatory growth without suffering high mortality associated with leaf area loss. We also suggest that resting periods (with no harvesting) may be critical to allow individuals and populations to recover, as has been shown in C. elegans (López-Toledo et al. 2012). A valuable next step would be identification of population health indicators (e.g. changes in reproductive frequency) that would provide advance warning of demographic declines and indicate that harvesting should be reduced or stopped for a period of time.

Acknowledgements We thank Gilberto Jamangape, Jorge Rodríguez-Velázquez, Taryn Fransen, Miguel Salinas, Carlos Ramos and José Chankayub for technical assistance in the field. Thanks to Teresa Valverde, Alejandro Casas and two anonymous ref-

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556

Defoliation and gender effects on fitness 1555 erees who improved first versions of the manuscript. This work was supported by the National Science Foundation (grant IBN 9604030) to D.D.A., by the National Autonomous University of Mexico PAPIIT-DGAPA (grant IN-229507) and CONACYT-SEMARNAT (project 2002-C01-0544) to M.M.R. This study constitutes a partial fulfillment of the Graduate Program in Biological Sciences of the National Autonomous University of Mexico (UNAM). J.C.H.B. acknowledges the National Council of Science and Technology (CONACYT) and DGEP-UNAM for PhD Scholarship grants, and Utrecht University for a short-term fellowship. M.M.R. acknowledges sabbatical support from PASPA-DGAP (UNAM) and CONACyT.

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Supporting Information Additional Supporting Information may be found in the online version of this article: Table S1. Original number (sample size) and sex ratio of palms employed in the defoliation experiment conducted on three Chamaedorea species at southern Mexico. Table S2. Number and sex ratio of palms surviving after 2 years of sustained defoliation applied to three Chamaedorea species at southeastern Mexico. Figure S1. Survivorship probability as a function of plant size in Chamaedorea elegans palms at southern Mexico. Figure S2. Defoliation and plant size effects on stem RGR of three Chamaedorea species subjetcted to increased levels of defoliation at south-eastern Mexico. Figure S3. Defoliation and plant size effects on leaf size and leaf area production rates of female and males individuals of Chamaedorea elegans subjected to increased levels of defoliation at south-eastern Mexico. Figure S4. Defoliation and plant size effects on leaf area production rates of female and male individuals of Chamaedorea ernesti-augustii subjected to increased levels of defoliation at south-eastern Mexico. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be reorganized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.

© 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1544–1556