| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Reproductive Biology |
Departamento de Ecología y Comportamiento Animal, Instituto de Ecología, AC, Apartado Postal 63, Xalapa 91070, Veracruz, Mexico
Received for publication August 14, 2003. Accepted for publication February 17, 2004.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: distyly • gender specialization • herbivory • hummingbird pollination • nectar production • Palicourea padifolia • Rubiaceae
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Barrett, 1992
). Two classes of heterostyly can occur depending on whether there are two (distyly) or three (tristyly) floral morphs within plant populations (Barrett, 1992
). In distylous species, about half of the plants in one population have long styles and short stamens (hereafter L-morph), while the remainder have short styles and long stamens (hereafter S-morph) (Barrett, 1992
). Although this balanced polymorphism is designed for reciprocal pollen transfer (i.e., cross-pollination between anthers and stigmas of equivalent height in the floral morphs; Barrett, 1990
), the efficacy of such a mechanism depends often on pollinator effectiveness (Beach and Bawa, 1980
). Despite this, heterostyly can evolve into other reproductive systems when pollen transfer is highly asymmetrical (Ganders, 1979
; Beach and Bawa, 1980
; Lloyd and Webb, 1992
; Barrett, 1992
).
Gender specialization has been documented in distylous species (Wyatt, 1983
; Barrett, 1992
; Webb, 1999
, and references therein). In most cases, L-morph plants have become females and S-morph individuals have become males (Webb, 1999
). Theoretical and empirical studies have stressed the role of an asymmetrical pollen transfer between floral morphs, and consequently of pollinators, as the main evolutionary force in the process of gender specialization in distylous species (Ganders, 1974
; Ornduff, 1975
; Charlesworth and Charlesworth, 1979
; Lloyd, 1979
; Beach, 1981
; Barrett, 1992
, and references therein). Although intrinsic genetic factors may affect gender specialization in plants (Casper, 1992
; Domínguez et al., 1997
; Ávila-Sakar and Domínguez, 2000
), the nature and intensity of other selective pressures favoring gender specialization has rarely been investigated (Olesen, 1979
; Contreras and Ornelas, 1999
; Leege and Wolfe, 2002
). Yet, because cross-pollination is necessary for reproductive success in both morphs, they should not differ in attributes that contribute to attracting or rewarding floral visitors (Leege and Wolfe, 2002
), leading to equal reproductive success.
The purpose of our study was to examine the variation in floral and vegetative traits that function to attract pollinators and, potentially, herbivores in the distylous polymorphism of Palicourea padifolia (Rubiaceae). We first evaluated whether the availability of each morph, population spatial structure, and differences in vegetative and floral traits contribute differently to attracting and rewarding floral visitors and account for the observed differences in reproductive output. We then surveyed the performance of each morph along multiple stages of the reproductive cycle (flower and fruit production, nectar production) to assess whether pollinators and herbivores respond differently to these resources, depending upon the resource that they are seeking. These behaviors represent putative selective pressures that can favor gender specialization.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
.
Plant species
Palicourea padifolia (Roem. and Schult.) C. M. Taylor and Lorence (Rubiaceae) is a long-lived heterostylous, self-incompatible, understory shrub 2–7 m in height (Ree, 1997
; Contreras and Ornelas, 1999
). It occurs in middle-elevation cloud forests from southern Mexico to Panama (Taylor, 1989
). At Clavijero, it grows alone or in groups of 2–4 individuals. We have estimated more than 500 flowering individuals in this population isolated from other populations by a distance of at least 100 m on all sides. Our study population is morphologically distylous. We have previously reported differences in some floral traits commonly associated with the distylous polymorphism between P. padifolia floral morphs (Contreras and Ornelas, 1999
; Ornelas et al., 2004
). Individuals of P. padifolia normally bear 30–40 inflorescences, each opening 2–4 flowers per day during the blooming season, which extends from mid-March to August. Flowers are about 1.5 cm long with narrow tubular corollas and symmetrical placement of floral organs between morphs (Contreras and Ornelas, 1999
). The L-morph corolla tubes are slightly but significantly shorter than those of S-morph plants (Contreras and Ornelas, 1999
). The flowers last a single day, opening just before dawn and wilting at dusk depending on relative humidity. On dry days, anthers dehisce soon after the flower opens and corolla wilting may initiate after noon. The flowers secrete small amounts of nectar and are visited by small bees, bumble bees, butterflies, and hummingbirds (see Results; Ornelas et al., 2004
). Fruit development usually starts in May and asynchronous ripening extends until October. Plants set seeds only when pollinated by the opposite morph (Contreras and Ornelas, 1999
). It has two ovules per flower and either one or two seeds per fruit.
Floral morph frequencies
Because mating success is dependent on the availability of the other morph (Ganders, 1979
; Barrett, 1992
), we first quantified morph frequencies within the Clavijero population. We sampled all flowering plants encountered along transects placed throughout the population and recorded the floral morph.
We recorded the floral morph of the nearest neighbor of 50 plants of each morph chosen haphazardly across the population, as described by Wolfe (2001)
. The spatial structure of floral morphs was then determined by using the Pielou's (1961) coefficient of segregation (S'). We calculated whether near neighbors were more likely to be the same morph or a different one. We also measured the distance between the focal plant and its neighbor (in meters) so as to evaluate spatial distribution.
Flower and fruit standing crop
As a measure of attractiveness to floral visitors and fruit consumers, the number of inflorescences/infructescences were censused monthly from March to October on 20 plants in 1998 (10 of each morph) and 37 plants in 1999 (L-morph = 23, S-morph = 14). Preliminary observations indicated that flower and fruit production among individuals varies depending on previous flowering and fruiting history. Therefore, we used different plants every year and used inflorescence as the unit of replication. Inflorescences/infructescences were counted over the whole observation period because of losses associated with droughts (C. González, J. F. Ornelas, and L. Jiménez, unpublished data) and because asynchronous emergence of inflorescences can occur (Contreras and Ornelas, 1999
). Also, 10 inflorescences per plant were censused monthly from March to October, and the number of buds, number of open flowers, and number of developing and ripe fruits on each one counted. No additional manipulation was performed on plants used in this part of the study.
Nectar production
During 1998 and 1999, we quantified nectar production to determine whether plants of each morph reward pollinators equally and when the pollinators sought out such resources. Inflorescences of 20 additional plants (10 of each morph) were bagged in May with netting before bud opening (20 different plants every year). Nectar was extracted the following day with graduated micropipettes (5 µL) without removing the flowers from the plant. Nectar production was measured repeatedly throughout the life of individual flowers at 3-h intervals (at 0700, 1000, 1300, 1600, and 1900) to minimize the effects of evaporation in the quantification of nectar production. Forty flowers were examined in 1998 (20 of each morph) and 80 in 1999 (L-morph = 38, S-morph = 42).
Flowers subjected to repeated nectar removal might be stimulated to produce additional nectar and these might then confound real secretion patterns (Castellanos et al., 2002
, and references therein). To explore this possibility, we measured the nectar in plants (L-morph = 10, S-morph =11) for which buds of selected inflorescences were excluded from floral visitors to let nectar accumulate for 12, 14, 16, 18, 20, and 22 h. The accumulated nectar was sampled once in each flower the day after the exclusion and groups of flowers measured at 0700, 0900, 1100, 1300, 1500, and 1700. Nectar volume was measured as described and sugar concentration (percentage sucrose) was determined with a pocket refractometer (American Optical 10431, Buffalo, New York, USA; range concentration 0°–50° BRIX scale). The amount of sugar produced was expressed in milligrams after Kearns and Inouye (1993)
.
Because pollinators are probably responding to nectar standing crop, we also extracted the nectar available in flowers that had been exposed to floral visitors and measured its volume and sugar concentration. Data were collected from flowers of both morphs between 1000 and 1200 (N = 50 flowers) and between 1200 and 1400 hours (N = 80 flowers) in July 2002. Nectar was collected at two different times to evaluate eventual variation in sugar through the peak of hummingbird activity (Contreras and Ornelas, 1999
). Nectar volume and sugar concentration were measured as described.
Pollinator behavior
If pollinators of P. padifolia respond to standing crops differences, scheduling of nectar production, or plant conspicuousness (number of open flowers per plant), the timing of nectar seeking or visitation frequency would vary accordingly between floral morphs. We observed 32 focal, nonmanipulated plants (L-morph = 18, S-morph = 14) for 90 min each. Data on hummingbird foraging behavior were collected for 16 d during 1997 (12 plants), 1998 (12 plants), and 1999 (seven plants). Differences in plant sample sizes among years were due to availability of flowering, nonmanipulated plants. Observations were conducted only in May to minimize temporal changes in the composition of the pollinator assemblage and changes in other plant resources for the pollinators. Waiting times until hummingbirds arrived to a focal, nonmanipulated plant were recorded between 0700 and 1100 along the main trail. The observer was situated near the focal plant, close enough to allow careful observation. We recorded the beginning of our observations as time zero and subsequent foraging events as minutes from start time. An event was defined as the arrival of any hummingbird at one of the flowers of the target plant. In each plant, we noted the initial time of observation, time until a hummingbird visited the focal plant, and the number of flowers it visited.
Foliar herbivory and fruit production
In February 1999, we marked 50 plants (L-morph = 28, S-morph = 22) before blooming along the main trail. We then randomly selected five branches with inflorescences and five without them from each plant, and individually marked the two most-apical, mature leaves of each branch. The proportion of damaged leaves (number of damaged leaves/total number of leaves in the corresponding branch) was estimated monthly from March through August 1999. Leaves were categorized as damaged if we observed any indication of leaf consumption. Also, leaf area loss was estimated in the two apical leaves from both types of branch by subtracting the leaf area measured at the beginning of the flowering season (March) from that at the end (August). Leaf area was estimated by drawing the silhouette of each leaf over a transparency sheet and filling up the missing area with black ink. The drawings were cut and then used to estimate leaf area (in square centimeters) consumed with an area meter (LI-COR 3100, Lincoln, Nebraska, USA). Although repeated visitation of focal plants to estimate herbivory levels may have altered natural levels of herbivory (Cahill et al., 2001
), we assumed this uncertainty to be the same in both floral morphs by design.
From branches where herbivory was estimated, fruits were subsequently harvested at the end of the fruiting season (November 1999). We predicted a negative relationship between herbivory and reproductive performance, measured as both the numbers of fruits produced and fruit mass. Fruits were weighed (wet mass, to the nearest 0.01 g) with an electronic balance (Sartorius BP 211D, Goettingen, Germany).
Statistical analyses
We used repeated-measures ANOVAs to analyze differences between morphs regarding flowering and fruiting standing crop, herbivory (proportion of damaged leaves), and nectar production (volume). The model includes the effects of month or time of day as repeated factors (i.e., within-subject factors) and the effects of morph and year (except herbivory) as between-subjects factors. To improve normality, phenological and nectar data were log(x + 1) transformed, and the proportion of damaged leaves was arcsine transformed before analysis, but untransformed data are reported.
Variation in accumulated nectar (volume, sugar concentration, and mass of sugar in milligrams) and nectar standing crop (volume) between morphs as a function of time for the nectar to accumulate and area loss differences between leaves from branches with and without inflorescences of both floral morphs were assessed using two-way ANOVAs (Zar, 1984
). Nectar volume and leaf area data were log(x + 1) transformed to improve normality.
We used survival analysis (Muenchow, 1986
) to analyze hummingbird visitation because the observation periods were too short for all possible events to occur. For these data, the actual time of occurrence is not known; only a minimum length of time during which the event did not occur (censored data) is known. If an event occurred for a given plant, then it became uncensored data, and if it never occurred, then it became censored data. We used the Kaplan-Meier product-limit nonparametric method for the computation of the probability that hummingbirds had not yet visited a plant 90 min after the start of observation and the logrank (Mantel-Cox) statistic to test differences between floral morphs.
Lastly, the relationship between herbivory and reproductive performance was discerned using Spearman rank correlation and ANCOVAs. In the model, floral morph was a fixed factor, herbivory was the covariate, and the number and mass of fruits were the dependent variables. Data were log(fruit mass + 1) and square-root (number of fruits) transformed before the analyses.
All statistical analyses were run using general linear modeling with StatView and SuperANOVA (Abacus Concepts, 1989
, 1996
).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The morph of a plant was independent of the morph of its nearest neighbor. When an L-morph plant was the focal individual, its nearest neighbor was equally likely to be either an S-morph plant or another L-morph (28 vs. 22). Similarly, the nearest neighbor of an S-morph was equally likely to be either an L-morph or another S-morph (28 vs. 22). The segregation index was S' = 0.0, indicating no spatial affinity between floral morphs at the level of the first neighbor. Therefore, there was not a significant population structure, and the association between opposite morphs is random. Distance between a focal plant and its closest neighbor was statistically similar (one-way ANOVA, F3,76 = 1.02, P = 0.38, N = 80) among all possible floral morph combinations (mean ± SE, L-morph 
L-morph = 4.06 ± 0.7 m, N = 15; L-morph S-morph = 3.05 ± 0.4 m, N = 21; S-morph S-morph = 3.05 ± 0.4 m, N = 26; S-morph L-morph = 2.30 ± 0.4 m, N = 18).
Flower and fruit standing crop
Total number of inflorescences/infructescences produced per plant (mean ± 1 SE, L-morph = 74.5 ± 3.1; S-morph = 66.4 ± 3.1) and number of open flowers (L-morph = 1.9 ± 0.2; S-morph = 2.5 ± 0.3) produced by either morph were not statistically different over time (Table 1). The L-morph plants produced more buds per inflorescence (36.8 ± 1.6) than the S-morph plants (32.6 ± 1.8), but these differences were marginally significant (P = 0.043) (Table 1). Nonsignificant variation in flower standing crop was observed between morphs. There was a significant year effect in number of inflorescences, floral buds, and ripe fruits (Table 1) but the year x floral morph interactions were not or were marginally significant. In contrast, significant differences between floral morphs were observed in the overall number of developing fruits, independently of year (Table 1). The S-morph plants developed more fruits over time (11.1 ± 0.5) than the L-morph plants (7.6 ± 0.4). No statistical differences in the number of ripe fruits per infructescence were observed between L-morph (0.3 ± 0.05) and S-morph plants (0.3 ± 0.07; Table 1).
|
|
2 BRIX units by mid-day (time-of-day effect, F5,407 = 2.34, P = 0.04). Lastly, there were no significant differences between L-morph (0.137 ± 0.007 mg, N = 231) and S-morph flowers (0.139 ± 0.012 mg, N = 188) in the total mass of sugar per volume over time (floral morph effect, F1,407 = 0.01, P = 0.74). The amount of sugar varied significantly over time (time-of-day effect, F5,407 = 6.04, P = 0.0001), and the floral morph x time-of-day interaction was significant (F5,407 = 2.96, P = 0.012; Fig. 2).
|
2 = 2.24, P = 0.65).
|
2 = 9.05, df = 1, P = 0.002, N = 129 observations; Fig. 4). These differences occurred mainly during the first 60 min of observation (2 = 5.83, df = 1, P = 0.015, N = 71 observations). Waiting time for a given L-morph plant to be visited by hummingbirds averaged 27.5 ± 2.9 min (mean ± 1 SE), whereas for an S-morph plant the average was significantly longer (42 ± 2.5 min) (one-way ANOVA, F1,69 = 13.46, P = 0.0005, N = 71 observations). These results suggest that hummingbirds visited flowers of L-morph plants sooner than they did those of S-morph plants.
|
Leaf area consumed by herbivores over time was significantly higher among L-morph (2.4 ± 0.3 cm2) than among S-morph plants (1.2 ± 0.2 cm2) (F1,346 = 7.84, P = 0.0054), and branches with inflorescences suffered a higher herbivore attack (2.6 ± 0.4 cm2) than those without (1.3 ± 0.2 cm2) (F1,346 = 7.15, P = 0.0079). The floral morph x type of branch interaction was not significant (F1,346 = 1.33, P = 0.2504).
Number of fruits and fruit mass decreased significantly with the proportion of damaged leaves, but the relationship was stronger for fruit number (r = 0.63) than for fruit mass (r = 0.46). Equations describing these relationships are: number of fruits, Y = 4.71 – 3.12X; r2 = 0.39, P < 0.0001; fruit mass, Y = 0.42 – 0.76X; r2 = 0.21, P < 0.0001). Untransformed data split by floral morph are shown in Fig. 5. In both cases, the relationships are stronger in L-morph plants than in S-morph plants (Fig. 5A and B). A weaker trend was observed for leaf area consumed (Fig. 5C and D), and the relationship was only significant for fruit number (number of fruits, Y = 2.34 – 0.94X; r2 = 0.07, P = 0.034; fruit mass, Y = 0.14 – 0.08X; r2 = 0.05, P = 0.089). Based on the ANCOVAs, only the proportion of leaves damaged was useful in predicting fruit production (Table 2). Its very low P value is a clear indication that this herbivory measure is useful in predicting fruit production. The L-morph plants set significantly less fruit mass than the S-morph plants, and differences in fruit number were marginally significant (Table 2). In contrast, leaf area consumed was a poorer predictor of fruit production and no differences between floral morphs were detected (Table 2).
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
suggested that corollas of S-morph flowers are larger in order to increase their attractiveness to pollinators, thus encouraging more frequent visitation and pollen deposition and thereby compensating for that reproductive imbalance. Also, the 1 : 1 morph ratio observed in the Clavijero population is consistent with the prediction of a balanced equilibrium of compatibility phenotypes, assuming assortative mating (Ganders, 1979
). An isoplethic condition is also predicted to be a stable evolutionary strategy from the viewpoint of sexual selection theory (Casper, 1992
). Our finding of random distribution of nearest neighbor and equal distances between morphs corroborates the idea that P. padifolia does not reproduce clonally to any great extent, as previously suggested by Ree (1997)
. Here, we showed that floral morphs respond differently in their phenological patterns, and the availability and attractiveness of resources offered by P. padifolia varied along the reproductive season. The number of inflorescences/infructescences, buds, and open flowers, and ripe fruits offered by either floral morph was statistically similar, suggesting equal attractiveness to floral visitors and fruit consumers on a daily basis. In contrast, the number of developing fruits among S-morph plants over time, as a measure of maximum fruit production, almost doubled those of L-morph plants, suggesting a higher overall female reproductive success among S-morph plants. Ree (1997)
reported the opposite pattern for a population in Costa Rica, where L-morph plants set more fruits than S-morph plants. He estimated reproductive output from immature infructescences that were past flowering (after 1–2 wk) but had not yet developed fruits ripe enough to attract dispersers in relation to the number of pedicels per inflorescence and assumed that each pedicel represents a flower produced at some time in the past. Our monthly censusing (8 mo) was a more accurate and realistic estimation of overall female reproductive success in our study site because inflorescences complete flowering after 2–3 mo, while fruits require 3–4 mo to become fleshy and turn purplish-black (A. Hernández and J. F. Ornelas, unpublished data). We failed to estimate accurately the overall number of ripe fruits produced, because infructescences were unbagged and ripe fruits were potentially removed and consumed by frugivores between phenological censuses. Therefore, the number of ripe fruits available over time is not an accurate estimation of female reproductive success. Besides, fruit maturation rate may depend on fruit removal rates, as shown for bird-dispersed Hamelia patens (Rubiaceae) (Zurovchak, 1997
). A drawback of all these methods is that post-pollination processes can subtract from potential fruit set leading to an underestimation of pollination efficacy (see also Cane and Schiffhauer, 2003
). One apparent explanation for the differential reproductive success (number of developing fruits) between floral morphs in P. padifolia is an altered pollinator regime (i.e., asymmetrical pollen transfer). In our companion paper, asymmetrical pollen transfer between floral morphs seemed to favor S-morph plants, but the observed variation in pollen removal and pollen receipt was not explained by variation in hummingbirds' bill morphology (Ornelas et al., 2004
). Nor did we find evidence that hummingbird bill morphology solely explained the differences in fruit production between L- and S-morph individuals (Ornelas et al., 2004
). Lastly, Ree's results of a higher seed production for L-morph individuals could result from a different pollinator regime with higher bee visitation frequency (>40%) than our study site that promotes pollen transfer from S-morph to L-morph flowers because of the anther position and, therefore, accessibility to pollen grains (see also Harder and Barrett, 1993
).
The influence of pollinators
Nectar production
By repeatedly removing nectar, we stimulated replenishment of the fluid. The cumulative amount of nectar was significantly higher among L-morph flowers. However, natural secretion patterns may be obscured with repeated nectar removals in flowers that respond positively to removal (Castellanos et al., 2002
). To avoid this problem, we further measured nectar production among flowers allowed to accumulate nectar for several hours and found also that L-morph flowers secrete more fluid and sugar over time than those of S-morph plants. The asymmetrical morph difference in reward throughout the day may generate the observed flip-flop in natural pollen deposition documented for this population (Ornelas et al., 2004
). Although evaporation and/or reabsorption were not directly evaluated in our study, we believe these nectar-saving mechanisms do not affect the overall results because the amount of fluid differed between floral morphs throughout the day. Sexual differences in nectar production have been recorded for many dioecious and protandrous species (Devlin and Stephenson, 1985
; Klinkhamer and de Jong, 1990
; Delph and Lively, 1992
; Aizen and Basilio, 1998
) but are not known for distylous species (Sobrevila et al., 1983
; Pérez-Nasser et al., 1993
; Passos and Sazima, 1995
; Ree, 1997
; Contreras and Ornelas, 1999
; Leege and Wolfe, 2002
; Lau and Bosque, 2003
). Variation in nectar secretion associated with intrinsic flower traits may represent the evolutionary response to diverse selective pressures imposed by the requirements of pollinator regimes (Aizen and Basilio, 1998
). The observed differences between floral morphs in nectar production, in which L-morph flowers secreted higher volumes, may translate into differential pollinator visitation and entail a reproductive cost. If so, differences in nectar production rates can evolve through natural selection. Although hummingbirds prefer individuals with more nectar (e.g., Mitchell, 1993
), we need to further demonstrate experimentally if they respond to the observed differences in nectar production between L- and S-morph flowers and whether this differential allocation to rewarding pollinators translates into a reproductive cost.
Hummingbird behavior
Hummingbirds seem to respond to differences in nectar presentation by P. padifolia floral morphs, but whether they affect plant fitness awaits further investigation. Our censored data on hummingbird foraging behavior suggest that L-morph individuals have a higher probability of being visited first by hummingbirds than S-morph individuals. If so, this may result in more pollen transfer in one direction (long-styled short-styled flowers). The most common forager in P. padifolia (A. cyanocephala) established and defended feeding territories composed of 1–3 plants. This feeding behavior should increase the chances for geitonogamous crosses (>30 flowers probed · foraging bout–1 · plant–1) and may influence gender function (intramorph compatibility and self-compatibility). Lasso and Naranjo (2003)
have shown that two species of Amazilia are aggressive defenders of territories and the most frequent visitors in Hamelia patens (Rubiaceae) but the least effective pollinators. Because we have previously shown intramorph incompatibility (Contreras and Ornelas, 1999
), then discrimination against less rewarding flowers (S-morph flowers) by the most common hummingbirds may translate into hummingbirds first establishing territories in more rewarding L-morph plants, and then, as nectar resources diminish through the day, moving into less rewarding S-morph plants. A similar pattern has been found in some dioecious species (e.g., Armstrong, 1997
). This hypothesis is supported by data on stigmatic pollen loads and rates of pollen accumulation throughout the day, in which S-morph stigmas end up with more legitimate pollen grains (Ornelas et al., 2004
).
The influence of herbivores
Male and female reproductive effort can be negatively affected by foliar and floral herbivores (Hendrix and Trapp, 1989
; Wolfe, 1997
; Krupnick and Weis, 1999
). In addition, the timing and the intensity of attack by herbivores may have direct consequences on flowering phenology (Aide, 1993
; Sagers and Coley, 1995
; Pilson, 2000
). Leege and Wolfe (2002)
found that morph-specific differences in floral morphology of distylous Gelsemium sempervirens (Loganiaceae) directly affected the pattern of herbivory; flowers of the L-morph had more pistil damage and the S-morph had more stamen damage. They suggested that differential floral herbivory based on the position of reproductive organs might affect the mating patterns within distylous populations. In P. padifolia, branches with inflorescences suffered a higher herbivore attack than those without, suggesting that they were more conspicuous and attractive to herbivores (Krupnick et al., 1999
). We also found that fruit production was negatively correlated with the attack of foliar herbivores (proportion of damaged leaves), and L-morph plants experienced the strongest negative effect with a marginally significant reduction in fruit number and a significant reduction in fruit mass. Morph-specific herbivory would result in gender specialization in our P. padifolia population because L-morph plants had a reduction in female fitness. We attribute the morph differences in resource allocation to fruit production because plants varied similarly in their attractiveness (size of their floral display) at the inflorescence and plant level. If so, female reproductive fitness of P. padifolia may be indirectly affected when foliar herbivores diminish resources otherwise allocated to reproduction (see also Mothershead and Marquis, 2000
). The role of foliar herbivores in explaining morph differences in reproductive effort need to be explored further for P. padifolia because herbivory attack can be extremely variable among individuals, populations, and years, from very low frequency (<6%; Williams-Linera and Herrera, 2003
) to intense defoliation in some individuals. Also, we failed to estimate accurately fruit production in relation to foliar herbivory because fruits were exposed to frugivory, seed predation, and diseases, and were harvested until November. This could explain why we found no differences between floral morphs in fruit production. Harvesting developing fruits from nonmanipulated branches would be a more accurate method for estimating female reproductive output in relation to foliar herbivory in future observational studies.
In conclusion, our overall results suggest that resources allocated to attract and reward pollinators differ between floral morphs, and morph differences in female reproductive effort suggest that gender specialization is evolving in this population. The evolution of gender specialization in distylous plants has been traditionally understood in relation to their floral morphology and the ecology of pollen transfer. We have shown that pollinators and herbivores may exert selective pressures on other floral and vegetative traits that could also influence gender function.
|
|
FOOTNOTES |
|---|
2 E-mail: ornelasj{at}ecologia.edu.mx
3 Current address: Laboratorio de Ecología del Comportamiento, CentroTlaxcala de Biología de la Conducta, Universidad Autónoma de Tlaxcala, Carretera Tlaxcala-Puebla, Km 1.5 s/n Tlaxcala, Tlaxcala 90070, Mexico
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Abacus Concepts. 1996 Abacus Concepts, StatView Reference. Abacus Concepts, Berkeley, California, USA
Aide T. M. 1993 Patterns of leaf development and herbivory in a tropical understory community. Ecology 74: 455-466[CrossRef][ISI]
Aizen M. A. A. Basilio 1998 Sex differential nectar secretion in protandrous Alstroemeria aurea (Alstroemeriaceae): is production altered by pollen removal and receipt?. American Journal of Botany 85: 245-252[Abstract]
Armstrong J. E. 1997 Pollination by deceit in nutmeg (Myristica insipida, Myristicaceae): floral displays and beetle activity in male and female trees. American Journal of Botany 84: 1266-1274[Abstract]
Ávila-Sakar G. C. A. Domínguez 2000 Parental effects and gender specialization in a tropical heterostylous shrub. Evolution 54: 866-877[ISI][Medline]
Barrett S. C. H. 1990 The evolution and adaptive significance of heterostyly. Trends in Ecology and Evolution 5: 144-148[CrossRef]
Barrett S. C. H. 1992 Heterostylous genetic polymorphisms: model systems for evolutionary analysis. In S. C. H. Barrett [ed.], Evolution and function of heterostyly, 1–29. Springer Verlag, New York, New York, USA
Beach J. H. 1981 Pollinator foraging and the evolution of dioecy. American Naturalist 118: 572-577[CrossRef][ISI]
Beach J. H. K. S. Bawa 1980 Role of pollinators in the evolution of dioecy from distyly. Evolution 34: 1138-1142[CrossRef][ISI]
Cahill J. F. J. P. Castelli B. B. Casper 2001 The herbivory uncertainty principle: visiting plants can alter herbivory. Ecology 82: 307-312[ISI]
Cane J. H. D. Schiffhauer 2003 Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). American Journal of Botany 90: 1425-1432
Casper B. B. 1992 The application of sex allocation theory to heterostylous plants. In S. C. H. Barrett [ed.], Evolution and function of heterostyly, 209–223. Springer Verlag, New York, New York, USA
Castellanos M. C. P. Wilson J. D. Thomson 2002 Dynamic nectar replenishment in flowers of Penstemon (Scrophulariaceae). American Journal of Botany 89: 111-118
Charlesworth D. B. Charlesworth 1979 A model for the evolution of distyly. American Naturalist 114: 467-498[CrossRef][ISI]
Contreras P. S. J. F. Ornelas 1999 Reproductive conflicts of Palicourea padifolia (Rubiaceae) a distylous shrub of a tropical cloud forest in Mexico. Plant Systematics and Evolution 219: 225-241[CrossRef][ISI]
Darwin C. 1877 The different forms of flowers on plants of the same species. Murray, London, UK
Delph L. F. C. M. Lively 1992 Pollinator visitation, floral display, and nectar production of the sexual morphs of a gynodioecious shrub. Oikos 63: 161-170[CrossRef][ISI]
Devlin B. A. G. Stephenson 1985 Sex differential floral longevity, nectar secretion, and pollinator foraging in a protrandrous species. American Journal of Botany 72: 303-310[CrossRef][ISI]
Domínguez C. A. G. Ávila-Sakar S. Vázquez-Santana J. Márquez-Guzmán 1997 Morph-biased male sterility in the tropical distylous shrub Erythroxylum havanense (Erythroxylaceae). American Journal of Botany 84: 626-632[Abstract]
Ganders F. R. 1974 Disassortative pollination in the distylous plant Jepsonia heterandra. Canadian Journal of Botany 52: 2401-2406[ISI][Medline]
Ganders F. R. 1979 The biology of heterostyly. New Zealand Journal of Botany 17: 607-635[ISI]
Harder L. D. S. C. H. Barrett 1993 Pollen removal from tristylous Pontederia cordata: effects of anther position and pollinator specialization. Ecology 74: 1054-1072
Hendrix S. D. E. J. Trapp 1989 Floral herbivory in Pastinaca sativa: do compensatory responses offset reductions in fitness?. Evolution 43: 891-895[CrossRef][ISI]
Kearns C. A. D. W. Inouye 1993 Techniques for pollination biologists. University Press of Colorado, Niwot, Colorado, USA
Klinkhamer P. G. L. T. J. de Jong 1990 Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous Echium vulgare (Boraginaceae). Oikos 57: 399-405[CrossRef][ISI]
Krupnick G. A. A. E. Weis 1999 The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80: 135-149[ISI]
Krupnick G. A. A. E. Weis D. R. Campbell 1999 The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80: 125-134[ISI]
Lasso E. M. L. Naranjo 2003 Effect of pollinators and nectar robbers on nectar production and pollen deposition in Hamelia patens (Rubiaceae). Biotropica 35: 57-66[CrossRef][ISI][Medline]
Lau P. C. Bosque 2003 Pollen flow in the distylous Palicourea fendleri (Rubiaceae): an experimental test of the disassortative pollen flow hypothesis. Oecologia 135: 593-600
Leege L. M. L. M. Wolfe 2002 Do floral herbivores respond to variation in flower characteristics in Gelsemium sempervirens (Loganiaceae), a distylous vine?. American Journal of Botany 89: 1270-1274
Lloyd D. G. 1979 Evolution towards dioecy in heterostylous populations. Plant Systematics and Evolution 131: 71-80[CrossRef][ISI]
Lloyd D. G. C. J. Webb 1992 The evolution of heterostyly. In S. C. H. Barrett [ed.], Evolution and function of heterostyly, 151–178. Springer Verlag, New York, New York, USA
Mitchell R. J. 1993 Adaptive significance of Ipomopsis aggregata nectar production: observation and experiment in the field. Evolution 47: 25-35[CrossRef][ISI]
Mothershead K. R. J. Marquis 2000 Fitness impacts of herbivory through indirect effects on plant–pollinator interactions in Oenothera macrocarpa. Ecology 81: 30-40[CrossRef][ISI]
Muenchow G. 1986 Ecological use of failure time analysis. Ecology 67: 246-250[CrossRef][ISI]
Olesen J. M. 1979 Differential anther eating by snails in the heterostylous plant species, Primula elatior (L.) Hill. Acta Botanica Neerlandica 28: 519-521[ISI]
Ornduff R. 1975 Heterostyly and pollen flow in Hypericum aegypticum (Guttiferae). Botanical Journal of the Linnean Society 71: 51-57
Ornelas J. F. L. Jiménez C. González A. Hernández 2004 Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane forest. I. Hummingbirds' effectiveness as pollen vectors. American Journal of Botany 91: 1052-1060
Passos L. M. Sazima 1995 Reproductive biology of the distylous Manettia luteo rubra (Rubiaceae). Botanica Acta 108: 309-313[ISI]
Pérez-Nasser N. L. E. Eguiarte D. Piñero 1993 Mating system and genetic structure of the distylous tropical tree Psychotria faxlucens (Rubiaceae). American Journal of Botany 80: 45-52[CrossRef][ISI]
Pielou E. C. 1961 Segregation and symmetry in two-species populations as studied by nearest-neighbour relationships. Journal of Ecology 49: 255-269[CrossRef][ISI]
Pilson D. 2000 Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122: 72-82[CrossRef][ISI]
Ree R. H. 1997 Pollen flow, fecundity, and the adaptive significance of heterostyly in Palicourea padifolia (Rubiaceae). Biotropica 29: 298-308[CrossRef][ISI]
Sagers C. L. P. D. Coley 1995 Benefits and costs of defense in a neotropical shrub. Ecology 76: 1835-1843[CrossRef][ISI]
Sobrevila C. N. Ramírez N. Xena de Enrech 1983 Reproductive biology of Palicourea fendleri and P. petiolaris (Rubiaceae), heterostylous shrubs of a tropical cloud forest in Venezuela. Biotropica 15: 161-169
Taylor C. M. 1989 Revision of Palicourea (Rubiaceae) in Mexico and Central America. Systematic Botany Monographs 26: 1-102
Webb C. J. 1999 Empirical studies: evolution and maintenance of dimorphic breeding systems. In M. A. Geber, T. E. Dawson, and L. F. Delph [eds.], Gender and sexual dimorphism in flowering plants, 61–95. Springer, Berlin, Germany
Williams-Linera G. F. Herrera 2003 Folivory, herbivores, and environment in the understory of a tropical montane cloud forest. Biotropica 35: 67-73[ISI][Medline]
Wolfe L. M. 1997 Differential flower herbivory and gall formation on males and females of Neea psychotrioides, a dioecious tree. Biotropica 29: 169-174[CrossRef][ISI][Medline]
Wolfe L. M. 2001 Associations among multiple floral polymorphisms in Linum pubescens (Linaceae), a heterostylous plant. International Journal of Plant Sciences 162: 335-342[CrossRef]
Wyatt R. 1983 Pollinator–plant interactions and the evolution of plant breeding systems. In L. Real [ed.], Pollination biology. Academic Press, Orlando, Florida, USA
Zar J. H. 1984 Biostatistical analysis. Simon & Schuster, Englewood Cliffs, New Jersey, USA
Zurovchak J. G. 1997 Hamelia patens (Rubiaceae) accelerates fruit maturation rate in response to increased fruit removal. Biotropica 29: 229-231[CrossRef][ISI][Medline]
This article has been cited by other articles:
|
|
 |
|
  U. Effmert, C. Dinse, and B. Piechulla Influence of Green Leaf Herbivory by Manduca sexta on Floral Volatile Emission by Nicotiana suaveolens Plant Physiology, April 1, 2008; 146(4): 1996 - 2007. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. E. Irwin and L. S. Adler Correlations among traits associated with herbivore resistance and pollination: implications for pollination and nectar robbing in a distylous plant Am. J. Botany, January 1, 2006; 93(1): 64 - 72. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. GONZALEZ, J. F. ORNELAS, and L. JIMENEZ Between-year Changes in Functional Gender Expression of Palicourea padifolia (Rubiaceae), a Distylous, Hummingbird-pollinated Shrub Ann. Bot., January 2, 2005; 95(2): 371 - 378. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Ornelas, L. Jimenez, C. Gonzalez, and A. Hernandez Reproductive ecology of distylous Palicourea Padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds' effectiveness as pollen vectors Am. J. Botany, July 1, 2004; 91(7): 1052 - 1060. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||
