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(American Journal of Botany. 2002;89:1270-1274.)
© 2002 Botanical Society of America, Inc.

Reproductive Biology

Do floral herbivores respond to variation in flower characteristics in Gelsemium sempervirens (Loganiaceae), a distylous vine?1

Lissa M. Leege2 and Lorne M. Wolfe

Department of Biology, P.O. Box 8042, Georgia Southern University, Statesboro, Georgia 30460 USA

Received for publication November 6, 2001. Accepted for publication April 26, 2002.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
We tested the hypothesis that traits traditionally thought to function in pollination can also influence attack by floral herbivores. Because distylous species produce two different flower types, we used Gelsemium sempervirens, a distylous vine of southeastern USA, to examine the frequency and pattern of floral herbivory in relation to floral characteristics. Flowers of the short-styled morph had larger corollas but showed no difference in the volume or concentration of nectar produced. Over the 2 yr of this study, 20–30% of plants suffered floral herbivory. The pattern of damage was morph-specific. Long-styled flowers were more likely to have damaged pistils, while stamens were more often damaged in short-styled flowers. In this distylous species, exserted flower organs were more likely to be eaten. Such differential herbivory based on the position of floral organs within a flower may result in reduced fitness via either male (short-styled morph) or female function (long-styled morph).

Key Words: distyly • floral herbivory • flower predation • flower size • Gelsemium sempervirens • heterostyly • nectar production


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
In animal-pollinated plant species, pollinators can select for floral traits that influence pollen receipt and removal. Pollinators respond to variation in traits such as flower size, color, scent, and reward (Waser and Price, 1981 ; Schemske and Horvitz, 1984 ; Nilsson, 1988 ; Harder, 1990 ; Young and Stanton, 1990 ; Herrera, 1993 ; Hodges, 1995 ; Campbell, Waser, and Price, 1996 ; Conner et al., 1996 ; Galen, 1996 ). Yet traits that attract insect pollinators might at the same time act as advertisement for other animals that destructively feed on flowers (Armbruster, 1997 ; Puterbaugh, 1997 ; Galen and Cuba, 2001 ). Herbivores can have either direct or indirect effects on plant fitness (Pettersson, 1991 ; Cunningham, 1995 ; Strauss, 1997 ). For example, plants with flowers damaged by herbivores may produce less nectar, receive fewer pollinator visits, and experience a significant reduction in fruit set (Krupnick, Weiss and Campbell, 1999 ; Mothershead and Marquis, 2000 ). Yet the question remains as to whether floral herbivores are sensitive to variation in floral traits that function to attract pollinators.

An ideal system to study the influence of floral traits on herbivory would be one in which floral traits exhibit significant variation. Distyly is a floral polymorphism in which populations contain individuals that produce one of two types of flowers (Barrett, 1992 ). The two floral morphs differ principally in the arrangement of their floral organs. Individuals of the short-styled morph (S morph) produce flowers that contain a stigma deep in the corolla and anthers at the tip of long filaments. The long-styled morph (L morph) has the reciprocal arrangement; anthers remain deep in the corolla while the stigma protrudes from the flower. Due to the presence of a self- and intra-morph incompatibility system, only matings between the two morphs produce seed (Ganders, 1979 ). In addition to variation in the primary sexual organs, the morphs may also differ in ancillary traits such as flower size, flower color, pollen production, and pollen size (Darwin, 1877 ; Dulberger, 1992 ; Lloyd and Webb, 1992 ; Wolfe, 2001 ). Darwin (1877) was the first to elucidate the adaptive significance of the floral polymorphism and reasoned that it served as a system to promote efficient pollen transfer. Despite the fact that distyly has served as a model system for understanding polymorphisms, virtually no work has focused on whether pollinator-selected floral traits influence the degree of damage to flowers in distylous species.

The purpose of our study was to examine the distylous polymorphism in light of floral herbivory. Our study species was Gelsemium sempervirens, a distylous vine that grows in the southeastern coastal plain of North America. Owing to fundamental differences in the construction of flowers of the S and L morphs, we hypothesized that there would be differences in the frequency and pattern of enemy attack. Specifically, we addressed two questions. First, do the floral morphs differ in characteristics that could be responsible for attracting pollinators and herbivores? The traits of interest were: flower size, size of primary reproductive organs (pistils and stamens), and nectar concentration and volume. Second, do the S and L morphs differ in the frequency and pattern of damage they suffer from floral herbivores? Here we distinguished between damage to attractive parts (corolla) and reproductive organs.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study species and study site
Gelsemium sempervirens (L.) (Loganiaceae, Carolina Jessamine) is a woody, evergreen vine that occurs in pine and deciduous woods in the southeastern USA and in the mountains of Mexico and Guatemala (Gleason and Cronquist, 1963 ). This species is characterized by a distylous breeding system (Ornduff, 1970 , 1979 , 1980 ) and produces sweet-smelling, tubular yellow flowers from February to April (Radford, Ahles, and Bell, 1968 ). All parts of the plant contain toxic alkaloids (Gleason and Cronquist, 1963 ).

This study was conducted in two populations of Gelsemium sempervirens (Herty Woods and Highway 301) in Bulloch County, Georgia, USA, during the period of peak flowering (March) in 1999–2001. Because G. sempervirens is capable of clonal growth, the individuals we sampled were either clearly arising from separate roots or were located at least 10 m apart from each other to ensure that they were separate individuals.

Flower size
To determine flower size, we sampled flowers from nine individuals of each of the S and L morphs in the Herty Woods and Highway 301 populations (N = 445 flowers) in March 2000. We measured the length and width of the corolla tube on each fully opened flower in the laboratory using digital calipers. In March 2001, we measured the length of the ovary, pistil, and stamen of one flower from each individual in the Herty Woods population (N = 135 flowers).

Nectar
All nectar measurements were taken from 18 plants (nine per morph) in Herty Woods and Highway 301 populations during a 4-wk period at peak flowering in March 2000. Nectar was extracted from flowers (N = 225 flowers/morph) that had been enclosed in mesh bags prior to the opening of buds to exclude flower visitors. We measured nectar volume by inserting a calibrated capillary tube into a flower. It was necessary to destructively sample each flower in order to remove all the nectar in a flower. Nectar sugar concentration was measured with a hand-held sugar refractometer (Technika, Phoenix, Arizona, USA). We determined nectar volume and concentration at different stages of the individual flower anthesis period: (1) closed bud (immediately prior to opening), (2) opening, (3) fully open, (4) old (flowers wilting). Treatments were randomly assigned to the 450 flowers prior to opening. Flowers advanced from bud to wilting in about 4 d.

Floral herbivory
Floral herbivory was quantified in 1999 and 2001 by noting the presence/absence of herbivory on flowers and flower buds. We collected one inflorescence from each plant in flower in Herty Woods and surrounding populations during a 4-wk period at peak flowering in both years (1999, N = 93 L and 69 S individuals; 2001, N = 46 L and 34 S individuals). Plants were not marked, and we most likely sampled some of the same individuals in both years. Inflorescences were placed in separate bags and brought to the laboratory for immediate inspection. In the laboratory we examined each flower for evidence of herbivory on petals, pistils, and stamens. Damage (evident on buds and open flowers) was clearly due to a chewing herbivore and was indicated by the presence of chew marks on petals, as well as the absence of stamens and pistils. We never observed any herbivores throughout the 2 yr of the study.

Statistical analysis
We used Student's t tests to compare floral traits between morphs. The frequency and pattern of damage to different flower parts was compared between morphs with a series of chi-square tests (all tests were based on one degree of freedom). Nectar volume and concentration were analyzed with two-way ANOVA to examine the effect of morph and stage of anthesis. Relationships among nectar volume, sugar concentration, and flower size (corolla length and width) were examined with Pearson product-moment correlations. All traits were normally distributed except nectar volume, which was natural log-transformed prior to analysis. All statistical analyses were conducted with JMP version 3.1.6 (SAS, 1995 ). Throughout this paper we report the mean ±1 SE.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Characteristics of S and L flowers
The frequency distributions of pistil length, stamen length, and stigma-anther separation were bimodal, indicating that there were consistent differences between the L and S morphs (Fig. 1). Flowers of the two morphs differed in pistil length, stamen length, and stigma-anther separation (Table 1). Corolla size differed as well. Flowers of the S morph were significantly longer and wider than those of the L morph (Table 1). In contrast, ovary length was greater in the L morph (Table 1).



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  		Fig. 1. Distribution of (A) pistil lengths, (B) stamen lengths, and (C) stigma-anther separation in long and short morphs of Gelsemium sempervirens. Dark bars represent short-styled morph, open bars represent long-styled morph

 

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  		Table 1. Descriptive statistics (in millimeters) of floral traits in short- and long-styled flowers of Gelsemium sempervirens. Values are means (SE)

 
Nectar
Nectar volume increased through the anthesis period and dropped off in wilting flowers (F3,151 = 4.41, P = 0.005). Generally, closed buds and senescing flowers had less nectar, with a peak of 14.2 ± 1.1 µL in fully opened flowers (Fig. 2A). Nectar volume was positively correlated with corolla width (r = 0.28, N = 160, P = 0.0003), but not length (r = 0.12, P = 0.13). Even when controlling for differences in flower size, nectar volume did not differ by morph (F1,151 = 1.01, P = 0.316). Sugar concentration averaged 20.6% and followed the same course through the anthesis period as did nectar volume (F3,151 = 4.23, P = 0.006). Sugar concentration was positively correlated with both corolla length (r = 0.27, N = 152, P = 0.001) and corolla width (r = 0.22, N = 160, P = 0.006). However, there was no significant difference between morphs in nectar sugar concentration (F1,151 = 0.885, P = 0.348; Fig. 2B). There was no relationship between nectar volume and sugar concentration (r = 0.025, N = 152, P = 0.76), nor was there significant variation among individual plants sampled for either nectar volume (F12,43 = 1.15, P = 0.355) or sugar concentration (F12,41 = 0.517, P = 0.886).



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  		Fig. 2. (A) Volume and (B) concentration of nectar produced by flowers of Gelsemium sempervirens ±1 SE. Measurements were made at four different stages of the anthesis period of an individual flower (see MATERIALS AND METHODS for description)

 
Floral herbivory
Floral herbivory was a consistent feature in both years, but the frequency of herbivory was generally higher in 2001. We examined the data at the level of the plant, flower, and specific floral structure. At the plant level, at least one flower was damaged in 22% of 161 individual plants sampled in 1999 and in 31% of 80 plants sampled in 2001. At the individual flower level (including unopened buds), 4.4% (N = 1240) and 10% (N = 375) experienced herbivory in 1999 and 2001, respectively. In some cases, damage had already occurred during the bud stage with 4% of 318 buds damaged in 1999 and 8% of 214 buds damaged in 2001. Petals were more frequently damaged than sexual organs in both years (Fig. 3).



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  		Fig. 3. Flower parts damaged by floral herbivory in Gelsemium sempervirens in 1999 and 2001. Percentages are derived from flowers experiencing some type of floral herbivory

 
There were significant differences between the two morphs in the pattern of herbivory. Of the flowers that were damaged, pistil damage was more common in flowers of the L morph in both years (1999: {chi}2 = 5.73, P < 0.03; 2001: {chi}2 = 4.63, P < 0.05; Fig. 3). Stamen damage was more common in the S morph in one year (1999: {chi}2 = 5.37, P < 0.02; 2001: {chi}2 = 0.056, P > 0.5, Fig. 3). Petal damage was consistently greater in the larger-flowered S morph although this was only marginally significant (1999: {chi}2 = 3.69, P > 0.07; 2001: {chi}2 = 1.06, P > 0.10). The frequency of floral herbivory was not morph-specific in either year (1999: {chi}2 = 0.26, P > 0.5; 2001: {chi}2 = 1.62, P > 0.5).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Plants have a variety of interactions with insects in addition to mutualistic relationships with pollinators. Negative interactions can take several different forms. Visitors to flowers that are ineffective as pollen vectors usurp resources like pollen and nectar without providing any service (Maloof and Inouye, 2000 ). In this regard, flower visitors that are not effective pollinators act as herbivores. Insects are also significant consumers of vegetative plant parts (Crawley, 1983 ). When consuming flowers and flower parts, insect herbivores may indirectly impact plant fitness (Breedlove and Ehrlich, 1968 ) by reducing pollinator attraction (Krupnick, Weis, and Campbell, 1999 ; Mothershead and Marquis, 2000 ). In addition, floral herbivores may directly impact fitness by removing male and/or female gametes (Muenchow and Delesalle, 1992 ; Krupnick and Weis, 1999 ). If indeed flowers are differentially attractive to pollinators, they may also be differentially attractive to floral herbivores, resulting in countervailing selective pressures on reproductive features.

By definition, the floral morphs of distylous species differ in flower architecture. Yet, because cross-pollination is necessary for reproductive success in both morphs, they should not differ in attributes that contribute to attracting or rewarding flower visitors. The two morphs should be similar in vegetative and floral traits. This assumes, of course, that the morphs achieve fitness equally through male and female function, and this assumption has been violated in some species (Opler, Baker, and Frankie, 1975 ; Lloyd, 1979 ). In our study, the morphs of G. sempervirens did not differ in the quality or quantity of nectar they produced. Indeed, nectar production and quality usually does not differ between the morphs of heterostylous species (Wolfe and Barrett, 1989 ; Passos and Sazima, 1995 ; but see Arroyo and Dafni, 1995 ). However, there are consistent differences in pollen production in distylous taxa: typically the short-level anthers of the L morph produce greater numbers of smaller individual pollen grains (Dulberger, 1992 ). Ornduff (1979) found the same pattern in G. sempervirens where the L morph produced 1.2 times more pollen than the S morph for this species. We found no differences in nectar reward structure in our study, but individual flower size did differ significantly between the morphs of G. sempervirens. Flowers of the S morph were significantly larger than flowers of the L morph. A similar flower size dimorphism has been reported in other distylous species (Levin, 1968 ; Ornduff, 1980 ; Richards and Koptur, 1993 ; Pailler and Thompson, 1997 ). Therefore, we expected that the combined differences between the morphs in flower size and positioning of reproductive organs in G. sempervirens will set up the potential for differential attraction of pollinators and floral herbivores.

The differences in flower architecture among the morphs are known to result in altered pollinator behavior in some heterostylous species (Wolfe and Barrett, 1989 ; Harder and Barrett, 1993 ; Arroyo and Dafni, 1995 ; Stone, 1996 ; but see Dominguez et al., 1997 ). In our study, the morph-specific differences in floral morphology directly affected the pattern of herbivory. Flowers of the L morph experienced more pistil damage than S flowers. This would likely reduce their ability to produce fruits and seeds. In contrast, the frequency of herbivory on stamens was higher in the S morph in 1999, potentially reducing male function of the S morph. We suspect that the inter-morph differences in consumption of male and female parts is a by-product of the distylous architecture. Although we never observed the floral herbivores, we noted that they commonly chewed an entry hole into the tip of the bud before the flower opened. This damaged the petals and any other flower parts present at the tip of the bud. Thus, the pistil was likely to be eaten along with the petals in the L morph, whereas the anthers of the S morph were more likely to be damaged. In the only other documented case of differential effects of floral herbivores on distylous flowers, Oleson (1979) reported a selective loss of 3–5% of anthers of the S morph of Primula elatior to anther-eating snails and no loss of anthers from flowers of the L morph. Thus, reproductive parts that protrude from corollas seem to be more susceptible to being eaten by floral herbivores.

Differential floral herbivory based on the position of reproductive organs may have implications for mating patterns within distylous populations. If L flowers suffer a reduction in female function, they obtain proportionately greater fitness via male function. On the other hand, S flowers function more as females if they lose male gametes to herbivory. This leads to the prediction that intense position-specific herbivory will result in sexual specialization in a distylous population.


   FOOTNOTES
 
1 The authors thank the 1999–2001 GSU Biology of Plants classes, Catherine Prior, and Jeremy Rayfield for help with field work; and Ray Chandler, Danny Gleason, Alan Harvey, Bruce Schulte, GSU's Ecology and Evolution discussion group, and three anonymous reviewers for providing helpful comments on the manuscript. Back

2 Author for reprint requests (leege{at}gasou.edu ) Back


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 DISCUSSION
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