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(American Journal of Botany. 2008;95:706-712.) doi: 10.3732/ajb.2007329 © 2008 Botanical Society of America, Inc. |
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Reproductive Biology |
2 CESAM and Department of Biology, University of Aveiro, Campus Universitário de Santiago 3810-193 Aveiro, Portugal 3 Department of Plant Biology and Soil Sciences, Faculty of Biology, University of Vigo, As Lagoas-Marcosende 36200 Vigo, Spain
Received for publication 15 October 2007. Accepted for publication 6 March 2008.
ABSTRACT
Secondary pollen presentation is the relocation and presentation of pollen in floral structures (termed pollen presenters) other than the anthers. These pollen presenters are often found close to the stigma and have been hypothesized to increase the accuracy of pollen transfer, although no experimental studies have been done. We examined the function of the pollen presenter and its efficiency in pollen dispersal, female fitness, and the degree of interference created by self-pollen in the shrublet Polygala vayredae, an insect-pollinated species with secondary pollen presentation. Herkogamy, a mechanism generally involved in the reduction of self-interference, was also evaluated. Significant pollen was lost (49% of total pollen) during the secondary relocation in the pollen presenter. However, pollen was exported from the pollen presenter, and subsequent pollen losses were similar to those in species with primary pollen presentation. Despite the presence of a self-incompatibility system, the numbers of developed pollen tubes as well as fruit and seed production were significantly reduced by the self-pollen interference created at the stigmatic papillae level. The extent of herkogamy correlated positively with female fitness. The secondary pollen presentation mechanism may in fact be an accurate system for pollen transport, but it may also have its costs. Further comparative studies involving species with primary and secondary pollen presentation are needed to fully understand the advantages and disadvantages of secondary pollen presentation.
Key Words: female fitness • herkogamy • pollen dispersal • pollen presenter • pollen relocation • Polygalaceae • self-incompatibility • self-interference
The study of floral trait efficiency is important for identifying the role of adaptive evolution in floral diversification. To understand the evolution of floral traits, we must first identify the various elements involved in the process. In several plant species, pollen is presented in floral structures other than the anthers, either by simple deposition or by special expulsion mechanisms, causing the pollen to come into contact with other floral parts. This floral mechanism is known as secondary pollen presentation (hereafter called SPP), and the structure where pollen is presented to pollinators is referred to as the pollen presenter (hereafter called PP; following Faegri and van der Pijl, 1979
; Yeo, 1993; Inouye et al., 1994; Ladd, 1994). The mechanisms through which pollen is secondarily presented are highly variable, with pollen being transferred to different areas of the style or stigma (e.g., Nilsson et al., 1990; Vaughton and Ramsey, 1991; Imbert and Richards, 1993; Nyman, 1993; Westerkamp and Weber, 1997), usually before flower opening. Pollen is then exposed in the PP during floral development or the mechanism is triggered by the pollination vectors (e.g., Brantjes, 1982, 1983; Nyman, 1993; Smith and Gross, 2002).
Secondary pollen presentation has traditionally been described as a mechanism that enhances the efficiency and accuracy of pollen exportation and/or pollen reception, thus increasing male and/or female fitness of the plant (Carolin, 1960; Lloyd and Yates, 1982; Ladd, 1994). Nevertheless, very few studies have experimentally assessed the effects of this mechanism on plant fitness (e.g., Lloyd and Yates, 1982; Imbert and Richards, 1993; Nyman, 1993). Moreover, a clash of interests may exist because the proximity of pollen-receiving and pollen-donating surfaces could result in self-interference, i.e., a conflict between male and female functions (Webb and Lloyd, 1986; Ladd, 1994; Barrett, 2002), with subsequent detrimental effects on plant fitness (e.g., Cesaro et al., 2004; Kawagoe and Suzuki, 2005; Waites and 
gren, 2006). Several functional or adaptive floral traits, such as self-incompatibility, dichogamy, and herkogamy, have evolved to avoid or minimize the effects of self-interference and thus improve outcrossing rates (Lloyd and Webb, 1986; Webb and Lloyd, 1986). Nonetheless, to date, self-interference has only been studied in species with primary pollen presentation, and all the functional and evolutionary assumptions made regarding SPP are based mainly on morphological descriptions.
The species belonging to Polygala L. (the largest genus of Polygalaceae comprising around 725 species; Paiva, 1998) have been described as presenting a SPP mechanism in which pollen is released before anthesis in a PP located on a sterile branch of the stigma (e.g., Ladd and Donaldson, 1993; Westerkamp and Weber, 1997; Fig. 1). The gynoecium, composed by two carpels, presents one sterile stigma functioning as PP and one fertile stigma with receptive papillae. However, there are some species in the genus that still present the ancestral gynoecia with two fertile stigmas, where the SPP mechanism is absent (P. persicariaefolia DC.; Venkatesh, 1956); in others the sterile stigma is reduced in size or has even disappeared (African Polygala sp.; Ladd and Donaldson, 1993); and in some derived species the sterile stigma has reevolved and functions as a pollen presenter (P. vauthieri Chodat; Ladd, 1994). Because the ancestral condition in Polygalaceae is probably the occurrence of two carpels, the PP most likely originated from the sterilization and specialization of one of the ancestral stigmas (Ladd, 1994), but comparative analyses are still needed to confirm these observations. The stigmatic region is highly diversified with structures in the shape of a basket, spoon, brush, or hair crown, and in several species of this family, the PP is slightly displaced in relation to the stigma (for illustrations, see Paiva, 1998; Castro, 2007). Ladd (1994) proposed that in species with SPP, herkogamy may minimize the effects of self-interference due to the proximity of the self-pollen and the stigma, but this theory has never been investigated experimentally. Moreover, the efficiency of pollen export/receipt by this mechanism has been questioned on theoretical grounds by Brantjes (1982) and Ladd and Donaldson (1993), who argued that stigma clogging and self-pollination would be difficult to avoid in several species of Polygala.
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), the function of herkogamy was also investigated for the first time in a species with SPP. To analyze the function of herkogamy, we assessed the variability in the distance between the PP and the stigmatic papillae and its consequences on female fitness. MATERIALS AND METHODS
Plant and study area
Polygala vayredae is an early-flowering perennial plant, endemic to the eastern Pre-Pyrenees (Alta Garrotxa, Girona, Spain). Because of its narrow distribution (approximately 12 km2), the species has been classified as vulnerable by IUCN categories (VV.AA, 2000). It is entomophilous, with large zygomorphic flowers and a self-incompatibility system at the stigmatic papillae level, strictly relying on pollinators to set seeds (Castro et al., 2008a). In the study area the main pollinator was Bombus pascuorum Scopoli (Apoidea, Hymenoptera), which visits intensively a large number of flowers in a patch and subsequently distances itself from the area (Castro, 2007).
As a result of the fusion of two monospermic carpels, the stigma is divided into two regions, a sterile one in shape of a basket (the PP) where SPP occurs, and a fertile region with the stigmatic papillae (see Fig. 1 and Castro, 2007). The curved style runs along the corolla tube and fits inside the keel. The anthers open introrsely toward the PP, which is recharged in subsequent pollinator visits through the downward movement of the keel activated by the pressure applied by the insect on the crest (this mechanism is illustrated in Fig. 2). Despite the deposition of the pollen close to the stigma, no spontaneous self-pollination occurs (Castro et al., 2008a).
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Functioning of the PP as a self-pollen receptor
Thirty-five flowers were bagged prior to anthesis. After anthesis, the number of pollen grains deposited in the PP was quantified in the first charge, i.e., after pollen dehiscence from the anthers to the pollen presenter (R1), and in subsequent recharges, i.e., after successive downward movements of the keel (R2, R3, R4), until pollen deposition was no longer observed (Fig. 2). The movement of the keel made by B. pascuorum was simulated by pressing on the crest. Pollen deposited in the PP after each movement of the keel was carefully removed with a needle to a microscope slide and mounted in a drop of 50% glycerine. This procedure was carried out under a stereobinocular microscope to guarantee that all the pollen grains were removed from the PP. Finally, pollen grains were counted under an Olympus CX31 light microscope (Olympus America, Center Valley, Pennsylvania, USA).
Efficiency of the PP in pollen dispersal
To evaluate the dispersal of the pollen deposited in the PP, fluorescent powdered dyes (Radiant Color, Richmond, California, USA) were used as pollen analogues (Waser and Price, 1982). Although dye and pollen dispersal properties differ (Thomson et al., 1986), dye transfer closely resembles pollen transfer when bumblebees, the main pollinators of P. vayredae, are the pollen vectors (e.g., Waser, 1988; Rademaker et al., 1997; Adler and Irwin, 2006). Fluorescent dyes were applied to the PP of 30 newly opened flowers after self-pollen had been removed. Flowers belonged to several individual plants arranged in clusters of roughly 0.25 m2. Three replicates clusters, each separated by at least 100 m, were selected along a single transect within the population. Because the sampling of the intermediate replica overlapped with the remaining two, a different colored dye was used to avoid contamination between replicas. After 8 d, 45–50 flower samples were collected at several distances from each cluster source (1, 2, 3, 4, 5, 10, 25–50, 50–100 m) and then preserved at –4°C. In the laboratory, flowers were examined under UV light using a stereobinocular microscope. The dye powder grains deposited in the stigma were classified into categories by number (class 0, zero; class 1, 
10 grains; class 2, 11–100 grains; class 3, 101–500 grains; class 4, >500 grains). The proportion of flowers with fluorescent dye was calculated for each distance interval.
SPP, degree of self-interference and female fitness
The influence of SPP on female fitness and on the degree of self-interference were evaluated using the following treatments: (1) open pollinated flowers, i.e., with the possibility of both self- and out-crossed pollen reception; (2) flowers emasculated in bud and open pollinated, i.e., excluding the possibility of self-pollen reception; and (3) the control group, i.e., bagged and manually self-pollinated flowers. At the onset of fruit development, the corollas (with the style and stigma) were collected and preserved in 70% ethanol to assess the pollen load on the stigmas and the development of pollen tubes through the style. To prevent pollen loss during pistil treatment, pollen loads were evaluated after cutting and squashing the stigmatic papillae on a microscope slide. Styles were then softened with 8 M sodium hydroxide for 4 h, stained with 0.05% aniline blue (w/v, in 0.1 M potassium phosphate) overnight and squashed in a drop of 50% glycerine (v/v) (Dafni et al., 2005). Samples were observed through a Nikon Eclipse 80i epifluorescence microscope equipped with a UV-2A filter cube (330–380 nm excitation; Nikon Instruments, Kanagawa, Japan). The number of pollen tubes that successfully developed through the stigmatic papillae and style was recorded. Fruit and seed set were recorded when mature. In these experiments, only visited flowers were considered. Because no spontaneous self-pollination occurs in this species, the presence of pollen on the stigmatic papillae clearly indicates the visit of a pollinator (for details, see Castro et al., 2008a, 2008b).
Distance between the PP and stigmatic papillae and effects on pollen tube development
Flower samples were randomly collected throughout the population during the flowering peak and preserved in 70% ethanol. The length of the corolla, stigmatic papillae, and PP, as well as the distance between the last two structures were measured in 100 flowers. Measurements were taken on microphotographs using the program ImageTool 3.0 for Windows (University of Texas Health Science Center, San Antonio, Texas, USA). Pollen tube development was evaluated in all flowers using the procedure described.
Statistical analysis
Differences among the number of pollen grains deposited in the PP after each movement of the keel (groups with equal sample sizes) were evaluated with a Kruskal–Wallis one-way ANOVA on ranks followed by a Tukey test for all multiple pairwise comparisons. A previous estimate of total pollen production per flower in the same population (5001 ± 90.1, mean ± SE; Castro et al., 2008a) was used to calculate the cumulative proportions of the pollen deposited in the PP after successive movements of the keel.
The proportions of flowers with fluorescent dye among distances (categorical data adjusted to a binomial distribution) were analyzed with generalized linear/nonlinear models using a logit link function; the type 3 likelihood-ratio test was run (MacCullagh and Nelder, 1989; Dobson, 1990). The proportion of total delivered pollen was also estimated by inferring the total amount of pollen potentially available in the three clusters (90 flowers with 
5000 pollen grains per flower) and estimating the delivered pollen using the proportion of flowers with fluorescent dye and its amount.
To evaluate the influence of SPP on female fitness, we analyzed differences among treatments in the number of pollen grains on the stigmas and pollen tubes in the styles with a Kruskal–Wallis one-way ANOVA on ranks followed by Dunn’s method (which takes into account the different sample sizes of the treatments). The effect of self-interference on fruit and seed production was evaluated with a 
2 test for the comparison of more than two proportions and multiple comparison tests for proportions according to Zar (1984).
A Spearman’s rank order correlation coefficient was calculated to evaluate the relationship between female fitness (number of developed pollen tubes below the stigmatic papillae) and the distance between the PP and stigmatic papillae. Because no correlation was found between the PP–stigmatic papillae distance and corolla length (R2 = 0.161, P = 0.109), the values were not corrected with this parameter. The mean, standard deviation of the mean (SD), and coefficient of variation (CV) of the PP–stigmatic papillae distance were also calculated. All statistical analyses were performed using the program STATISTICA (StatSoft., Tulsa, Oklahoma, USA).
RESULTS
Functioning of the PP as a self-pollen receptor
Pollen grains were deposited in higher numbers on the pollen presenter during the first charge of the PP than in subsequent movements of the keel (H = 101.03, P 0.001; Fig. 3A). When the results are analyzed using cumulative proportions of the total pollen produced, 48.6% of the pollen grains remained inside the keel until flower senescence (Fig. 3B).
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2 = 87.34; P < 0.001). A particularly low proportion of delivered pollen was obtained (0.44%) as estimated from the transfer of dye particles (see Materials and Methods).
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DISCUSSION
In outcrossing species, a conflict often arises between selection to present pollen and stigmas in similar positions to improve pollination success and selection to keep them apart to minimize or avoid interference between pollen export and pollen receipt on the stigma (Lloyd and Webb, 1986; Webb and Lloyd, 1986). Secondary pollen presentation, which has evolved in several groups of angiosperms, allows the pollen and stigmas to be presented in similar positions within a blossom (Carolin, 1960; Yeo, 1993; Ladd, 1994). Nevertheless, even though this is a widespread, highly diversified and morphologically studied feature (for a review, see Yeo, 1993), the functional aspects and consequences of such a mechanism on plant fitness are still largely unknown. The current study is the first evaluation of the consequences of SPP in both pollen exportation and pollen reception, in addition to the possible detrimental effects of the proximity of the self-pollen and stigmatic area.
Flowering plants that rely on animal vectors to transport pollen grains to conspecific stigmas of other flowers are exposed to great uncertainty and are frequently subjected to high rates of pollen loss (e.g., Inouye et al., 1994; Morris et al., 1994). Several different pollen fates may occur in this pathway, ranging from non-exportable pollen to pollen deposition on their own stigmas during removal and transport or at the presentation site (Inouye et al., 1994; Harder and Wilson, 1998). Our results showed that in P. vayredae the SPP mechanism results in considerable pollen loss within the flowers. The flowers produced roughly 5000 pollen grains, but only around 51% became available on the PP for export during flower’s life span. The remaining pollen (non-exportable pollen) remained inside the corolla without the possibility of being exposed and dispersed. Compared with the total amount of pollen produced by the flower, this pollen loss due to the SPP mechanism reduced the opportunities for mating by half before the pollen had the chance to be presented to the vector. Pollen losses before collection by pollinators (pre-collection losses, following Inouye et al. 1994) are generally overlooked in the studies performed so far, yet have been found in both species with primary (e.g., Harder and Thomson, 1989; Rademaker et al., 1997) and secondary pollen presentation (e.g., Vaughton and Ramsey, 1991; and results in the present work). Nonetheless, pre-collection pollen losses must be carefully analyzed when assessing the efficiency of the SPP mechanism because secondary relocation of the pollen constitutes an additional step in the process of pollination. Consequently, more studies on pre-collection pollen losses involving species with primary and secondary pollen presentation are needed to fully understand the degree of pollen loss due to the mechanism of SPP.
In P. vayredae the downward movement of the keel activated by a legitimate visitor of some mass (such as the long-tongued bumblebee B. pascuorum) exposes the PP and allows for the dispersal of pollen among flowers. The results of this study show that in the Colldecarrera population pollen flow and the proportion of pollen received were low in 2006. This reduced pollen flow is in accordance with pollinator activity reported for this year in this population. Although P. vayredae was the main flowering plant in the study area and B. pascuorum was its main pollinator, B. pascuorum interacted infrequently (0.088 for 15 min using the methodology in Herrera [1989]) with P. vayredae flowers (Castro, 2007). Thus, the low pollen flow was due to pollinator limitation and, in the focal flowers that were visited, to high pollen losses by the pollen vector during pickup, transport, and delivery. Intrinsic pollen losses due to the SPP mechanism, pollinator limitation (both cases of pre-collection pollen losses) and subsequent losses during transport on the pollen vector (pre-deposition pollen loss) were observed in P. vayredae. Despite this, the observed efficiency of pollen transport (estimated with fluorescent dyes dispersal) was similar to what has been reported for species with similar granular pollen (percentage of removed pollen delivered to stigmas below 0.5%; Thomson and Thomson, 1989; Galen, 1992; Rademaker et al., 1997). If only the pollen available for transportation is considered, pollen transfer efficiency was slightly higher than what was observed in species with primary pollen presentation (e.g., Harder and Thomson, 1989; Thomson and Thomson, 1989; Galen, 1992; Rademaker et al., 1997). It is important to note that the use of powdered fluorescent dyes as pollen analogues provide only a good qualitative prediction of pollen movement (Waser and Price, 1982; Thomson et al., 1986; Waser, 1988; Campbell et al., 1991; Rademaker et al., 1997; Adler and Irwin, 2006), and the pattern of dye and pollen movement may vary among the study species (Waser and Price, 1982; Thomson et al., 1986; Waser, 1988).
Self-interference has been described as the conflict between male and female functions due to their close proximity (Webb and Lloyd, 1986; Ladd, 1994; Barrett, 2002). In P. vayredae we observed that the presence of self-pollen in the stigmatic papillae reduced the number of pollen tubes in the style and the number of fruits and seeds as a result of interference with outcross pollen, although a self-incompatibility system possibly limits the negative effects of self-pollen interference. As suggested by Webb and Lloyd (1986) and recently shown empirically by Koelling and Karoly (2007), the presence of a self-incompatibility system may minimize or eliminate this conflict of interests. Additionally, temporal separation of male and female functions may also limit interference (Lloyd and Yates, 1982; Lloyd and Webb, 1986; Routley and Husband, 2006). In the few available studies involving species with SPP, these species have floral features similar to the ones described here. For example, in Cephalanthus occidentalis L. (Rubiaceae) a higher growth rate of outcrossed pollen tubes and an inhibition of self-pollen tubes at the base of the style largely prevented selfing (Imbert and Richards, 1993), and in Rauvolfia grandiflora Mart. ex A. DC. (Apocynaceae), a late acting self-incompatibility mechanism was also found (Lopes and Machado, 1999). In several species of Campanula L. (Campanulaceae), on the other hand, the tactile stimulation of the style hairs, where SPP occurs, controlled the male and female phases, reducing the maturation of the male phase while accelerating that of the female (Nyman, 1993). In P. vayredae a mechanism of self-incompatibility prevents self-fertilization, with rejection occurring at the stigmatic papillae level (results herein and Castro et al., 2008a). This mechanism does not avoid self-interference, but could mitigate the potential negative effects by limiting pollen tube growth in the style.
Somewhat paradoxically, considering the proximate female and male functions in species with SPP, herkogamy has also been suggested as another mechanism that may emerge to avoid self-interference (Ladd, 1994; Lopes and Machado, 1999). In P. vayredae it was previously observed that stigmatic papillae are located somewhat in a higher position on their stigmatic branch in relation to the PP (Castro, 2007). In this study, the relationship between the PP–stigmatic papillae distance and female fitness (measured by the number of pollen tubes growing in the style) revealed a slight increase in fitness with increased distance. Thus, this separation appears to be slightly advantageous for plant fitness. In experiments with Narcissus assoanus Dufour (Amaryllidaceae), a species lacking SPP, floral traits like herkogamy limited the cost of self-interference, which exerted a detrimental effect on seed set (Cesaro et al., 2004). Because self-pollination can reduce opportunities for outcrossing, selection will favor floral traits that reduce self-interference and improve outcrossing (Webb and Lloyd, 1986). This selection could be of special importance in xenogamous species with SPP mechanisms, where self-interference has significant detrimental consequences.
Although the current study has provided new insights into the function of SPP in P. vayredae, further comparative studies on the efficiency of pollen transfer, female fitness and presence of herkogamy involving related taxa with primary and secondary pollen presentation would be useful to assess the selective advantages and disadvantages of the SPP mechanism. As a result of the high diversity in SPP structures, Polygalaceae are very interesting and valuable for evaluating differences in the efficiency of pollen transfer among species with distinct pollen presentation structures and provide new insights into the adaptive significance of secondary pollen presentation.
FOOTNOTES
1 The authors thank the Departamento de Medi Ambient of Generalitat de Cataluña, Consorsi d’ Alta Garrotxa and Parc Natural de la Zona Volcànica de la Garrotxa for making this research possible, J. Loureiro for his critical reading of the manuscript, and C. Teed for assistance with the English. This research was supported by the Portuguese Foundation for Science and Technology (FCT, grant FCT/BD/10901/2002), the Xunta de Galicia (PGIDT04PXIC31003PN), and the Spanish DGICYT (BOS2003-07924-CO2-02). 
4 Author for correspondence (e-mail: scastro{at}ua.pt)
LITERATURE CITED
Adler, L. S., AND R. E. Irwin. 2006. Comparison of pollen transfer dynamics by multiple floral visitors: Experiments with pollen and fluorescent dye. Annals of Botany 97: 141–150.
Barrett, S. C. H. 2002. Sexual interference of the floral kind. Heredity 88: 154–159.[CrossRef][Web of Science][Medline]
Brantjes, N. B. M. 1982. Pollen placement and reproductive isolation between two Brazilian Polygala species (Polygalaceae). Plant Systematics and Evolution 141: 41–52.[CrossRef][Web of Science]
Brantjes, N. B. M. 1983. Regulated pollen issue in Isotoma, Campanulaceae, and evolution of secondary pollen presentation. Acta Botanica Neerlandica 32: 213–222.[Web of Science]
Campbell, D. R., N. M. Waser, M. V. Price, E. A. Lynch, AND R. J. Mitchell. 1991. Components of phenotypic selection: pollen export and lower corolla width in Ipomopsis aggregata. Evolution 45: 1458–1467.[CrossRef][Web of Science]
Carolin, R. C. 1960. The structure involved in the presentation of pollen to visiting insects in the Order Campanales. Proceedings of the Linnean Society of New South Wales 85: 197–207.
Castro, S. 2007. Reproductive biology and conservation of the endemic Polygala vayredae. Ph.D. dissertation, University of Aveiro, Aveiro, Portugal.
Castro, S., P. Silveira, AND L. Navarro. 2008a. How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae). Botanical Journal of the Linnean Society 157: 67–81.[CrossRef][Web of Science]
Castro, S., P. Silveira, AND L. Navarro. 2008b. Floral traits variation, pollinator attraction, and nectar robbing in Polygala vayredae (Polygalaceae). Ecological Research. doi:10.1007/s11284-008-0481-5.
Cesaro, A. C., S. C. H. Barrett, S. Maurice, B. E. Vaissiere, AND J. D. Thompson. 2004. An experimental evaluation of self-interference in Narcissus assoanus: Functional and evolutionary implications. Journal of Evolutionary Biology 17: 1367–1376.[CrossRef][Web of Science][Medline]
Dafni, A., P. Kevan, AND B. C. Husband. 2005. Practical pollination biology. Enviroquest, Cambridge, UK.
Dobson, A. J. 1990. An introduction to generalized linear models. Chapman and Hall, New York, New York, USA.
Faegri, K., AND L. van der Pijl. 1979. The principles of pollination ecology. Pergamon Press, Oxford, UK.
Galen, C. 1992. Pollen dispersal dynamics in an alpine wildflower Polemonium viscosum. Evolution 46: 1043–1051.[CrossRef][Web of Science]
Harder, L. D., AND J. D. Thomson. 1989. Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. American Naturalist 133: 323–344.[CrossRef][Web of Science]
Harder, L. D., AND W. G. Wilson. 1998. A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. American Naturalist 152: 684–695.[CrossRef][Web of Science][Medline]
Herrera, C. M. 1989. Pollinator abundance, morphology, and flower visitation rate: Analysis of the "quantity" component in a plant-pollinator system. Oecologia 80: 241–248.[Web of Science]
Imbert, F. M., AND J. H. Richards. 1993. Protandry, incompatibility, and secondary pollen presentation in Cephalanthus occidentalis (Rubiaceae). American Journal of Botany 80: 395–404.[CrossRef][Web of Science]
Inouye, D. W., D. E. Gill, M. R. Dudash, AND C. B. Fenster. 1994. A model and lexicon for pollen fate. American Journal of Botany 81: 1517–1530.[CrossRef][Web of Science]
Kawagoe, T., AND N. Suzuki. 2005. Self-pollen on a stigma interferes with outcrossed seed production in a self-incompatible monoecious plant, Akebia quinata (Lardizabalaceae). Functional Ecology 19: 49–54.[CrossRef]
Koelling, V., AND K. Karoly. 2007. Self-pollen interference is absent in wild radish (Raphanus raphanistrum, Brassicaceae), a species with sporophytic self-incompatibility. American Journal of Botany 94: 896–900.
Ladd, P. G. 1994. Pollen presenters in the flowering plants—form and function. Botanical Journal of the Linnean Society 115: 165–195.[CrossRef][Web of Science]
Ladd, P. G., AND J. S. Donaldson. 1993. Pollen presenters in the South African flora. South African Journal of Botany 59: 465–477.[Web of Science]
Lloyd, D. G., AND C. J. Webb. 1986. The avoidance of interference between the presentation of pollen and stigmas in Angiosperms. 1. Dichogamy. New Zealand Journal of Botany 24: 135–162.[Web of Science]
Lloyd, D. G., AND J. M. A. Yates. 1982. Intra-sexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36: 903–913.[CrossRef][Web of Science]
Lopes, A. V., AND I. C. Machado. 1999. Pollination and reproductive biology of Rauvolfia grandiflora (Apocynaceae): Secondary pollen presentation, herkogamy and self-incompatibility. Plant Biology 1: 547–553.[CrossRef]
Morris, W. F., M. V. Price, N. M. Waser, J. D. Thomson, B. Thomson, AND D. A. Stratton. 1994. Systematic increase on pollen carryover and its consequences for geitonogamy in plant populations. Oikos 71: 431–440.[CrossRef][Web of Science]
Nilsson, L. A., E. Rabakonandrianina, B. Pettersson, AND J. Ranaivo. 1990. Ixoroid secondary pollen presentation and pollination by small moths in the Malagasy treelet Ixora platythyrsa (Rubiaceae). Plant Systematics and Evolution 170: 161–175.[CrossRef][Web of Science]
Nyman, Y. 1993. The pollen-collecting hairs of Campanula (Campanulaceae). 2. Function and adaptive significance in relation to pollination. American Journal of Botany 80: 1437–1443.[CrossRef][Web of Science]
Paiva, J. A. R. 1998. Polygalarum africanarum et madagascariensium prodromus atque gerontogaei generis Heterosamara Kuntze, a genere Polygala L. segregati et a nobis denuo recepti, synopsis monographica. Fontqueria 50.
Rademaker, M. C. J., T. J. De Jong, AND P. G. L. Klinkhamer. 1997. Pollen dynamics of bumblebee visitation on Echium vulgare. Functional Ecology 11: 554–563.[CrossRef]
Routley, M. B., AND B. C. Husband. 2006. Sexual interference within flowers of Chamerion angustifolium. Evolutionary Ecology 20: 331–343.[Web of Science]
Smith, J. A., AND C. L. Gross. 2002. The pollination ecology of Grevillea beadleana McGillivray, an endangered shrub from northern New South Wales, Australia. Annals of Botany 89: 97–108.
Thomson, J. D., M. V. Price, N. M. Waser, AND D. A. Stratton. 1986. Comparative studies of pollen and fluorescent dye transport by bumblebees visiting Erythronium grandiflorum. Oecologia 69: 561–566.[CrossRef][Web of Science]
Thomson, J. D., AND B. A. Thomson. 1989. Dispersal of Erythronium grandiflorum pollen by bumblebees: Implications for gene flow and reproductive success. Evolution 43: 657–661.[CrossRef][Web of Science]
Vaughton, G., AND M. Ramsey. 1991. Floral biology and inefficient pollen removal in Banksia spinulosa var. neoanglica (Proteaceae). Australian Journal of Botany 39: 167–177.[CrossRef][Web of Science]
Venkatesh, C. S. 1956. The special mode of dehiscence of anthers of Polygala and its significance in autogamy. Bulletin of the Torrey Botanical Club 83: 19–26.[CrossRef]
VV.AA. 2000. Lista roja de flora vascular Española (valoración según categorías UICN). Conservación Vegetal 6: 11–36.
Waites, A. R., AND J. gren. 2006. Stigma receptivity and effects of prior self-pollination on seed set in tristylous Lythrum salicaria (Lythraceae). American Journal of Botany 93: 142–147.
Waser, N. M. 1988. Comparative pollen and dye transfer by pollinators of Delphinium nelsonii. Functional Ecology 1: 41–48.
Waser, N. M., AND M. V. Price. 1982. A comparison of pollen and fluorescent dye carryover by natural pollinators of Ipomopsis aggregata (Polemoniaceae). Ecology 63: 1168–1172.[CrossRef][Web of Science]
Webb, C. J., AND D. G. Lloyd. 1986. The avoidance of interference between the presentation of pollen and stigmas in Angiosperms. 2. Herkogamy. New Zealand Journal of Botany 24: 163–178.[Web of Science]
Westerkamp, C., AND A. Weber. 1997. Secondary and tertiary pollen presentation in Polygala myrtifolia and allies (Polygalaceae, South Africa). South African Journal of Botany 63: 254–258.[Web of Science]
Yeo, P. 1993. Secondary pollen presentation. Springer-Verlag, Wien, Austria.
Zar, J. H. 1984. Biostatistical analysis. Prentice-Hall, Engelwood Cliffs, New Jersey, USA.
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