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Flower Visitation, Pollen Deposition, and Pollen-Tube Competition in Hibiscus Moscheutos (Malvaceae)

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Flower Visitation, Pollen Deposition, and Pollen-Tube Competition in Hibiscus Moscheutos (Malvaceae) American Journal of Botany 79(4): 428-433. 1992. FLOWER VISITATION, POLLEN DEPOSITION, AND POLLEN-TUBE COMPETITION IN HIBISCUS MOSCHEUTOS (MALVACEAE) 2Smithsonian Environmental Research Center, Box 28, Edgewater, Maryland 21037; 3Department of Biology, Georgia Southern University, Statesboro, Georgia 30460; and 4Department of Plant Biology, Ohio State University, Columbus, Ohio 43210 The potential influence of pollen-tube competition on offspring "quality" has received considerable attention in recent years. Yet the prevalence of pollen competition in natural populations is largely unknown because few investigators have actually measured rates of pollen deposition on stigmas. In this study, we assess the potential for pollen-tube competition in natural populations of the self-compatible, pollinator-dependent herbaceous perennial, Hibiscus moscheutos. Individual flowers averaged two to four visits per 15 min by potential pollinators (Ptilothrix and Bombus), and about 34% of these visits involved contact with a stigma. The median number of pollen grains deposited on virgin stigmas per contact visit was 70 grains (values ranged from 0 to 889), and flowers averaged about four contact visits per hour. Approximately 360 pollen grains must reach stigmas for full seed set to occur in a typical flower (an average ovary has 139 ovules, and 2.6 pollen grains are required per seed). Within 2 and 3 hr exposure to pollinators, 65% and 97% of the flowers received excess pollen (>360 grains) and median stigmatic pollen loads exceeded the number of ovules by a factor of 4.0 and 5.4, respectively. Based on 3 yr observations, it is concluded that pollen competition may frequently occur in this species. Gametophytic selection due to pollen competition may most likely to fertilize ovules. Another potential effect of be an important component of natural selection in plants pollen-tube competition is nonrandom mating, which (Mulcahy, 1979; Snow, 1986; Mulcahy and Mulcahy, 1987; could influence both outcrossing rates and paternal re- Walsh and Charlesworth, in press). One consequence of productive success (Snow and Spira, 199 la, b). pollen-tube competition is its potential effect on seed A prerequisite for pollen-tube competition is that flow- "quality." Several investigators have found that seeds ers receive excess pollen relative to the amount needed produced under intense pollen-tube competition have sig- for full seed set to occur. In some populations, only small nificantly better germination, seedling growth, or seedling amounts of pollen are deposited on stigmas, and seed set survivorship than those produced with little or no pollen- per fruit is actually pollen-limited (e.g., Bierzychudek, tube competition (reviewed in Mulcahy and Mulcahy, 198 1; Spira and Pollak, 1986). In a review of the literature, 1987; but see Snow, 1990). Snow (1 986) found that in most cases, pollinators deliv- It is well documented that large numbers of genes are ered more than enough pollen to sire a full complement expressed by the microgametophyte (the germinated pol- of seeds per fruit (see also Levin, 1990). len grain) and that there is substantial overlap in gene The fact that seed set is generally not pollen-limited expression between the gametophyte and sporophyte gen- suggests the potential for pollen competition but provides erations (Tanksley, Zamir, and Rick, 198 1; Willing and little insight into its magnitude (Mulcahy and Mulcahy, Mascarenhas, 1984; Willing, Bashe, and Mascarenhas, 1987). The intensity of pollen competition is influenced 1988). Moreover, the genes expressed by the microga- not only by the number of pollen grains reaching stigmas, metophyte that contribute to fast-growing pollen tubes but also by their rate of arrival. If pollen grains arrive may also facilitate more vigorous sporophytes (e.g., Mul- gradually over time, then pollen tubes from separate pol- cahy, 1974; Ottaviano, Sari-Gorla, and Mulcahy, 1980; len loads may not compete; consequently, many ovules Winsor, Davis, and Stephenson, 1987). Consequently, may be fertilized from a random population of pollen pollen-tube competition may result in increased seed grains rather than by those with the fastest growth. "quality" because the fastest growing pollen-tubes are With the exception of studies on Geranium maculatum (Mulcahy, Curtis, and Snow, 1983) and Epilobium canum (Snow, 1986), detailed studies on the timing and amount Received for publication 3 May 199 1; revision accepted 27 Novem- ber 1991. of pollen deposited on stigmas over time are rare. More- The authors thank D. Charlesworth and 0. J. Blanchard for reviewing over, we know little about other factors influencing the the manuscript; J. O'Neill, E. Turner, and L. Wagner for field assistance magnitude of pollen competition, such as the number of and logistical support; and 0. J. Blanchard and R. W. Thorp for iden- pollen grains required per seed, and the extent to which tification of flower visitors. This research was supported by NSF grants pollen-tube growth rates vary. Consequently, the preva- BSR 8906667 to AAS and BSR 8906959 to TPS; grants from the White- lence of pollen competition in natural populations is large- hall Foundation, the Georgia Southern University Faculty Research Committee, and the Smithsonian Environmental Research Center to ly unknown. TPS; and the Environmental Sciences and Work-learn Programs of the The purpose of this paper is to describe pollination Smithsonian Institution. rates in natural populations ofHibiscus moscheutos within Author for correspondence (Georgia Southern address). the context of pollen competition. Data are presented on April 19921 SPIRA ET AL. -POLLEN-TUBE COMPETITION 429 flower visitation rates, the proportion of flower visitors contacted a stigma during single flower visits (N = 375) that contact a stigma, and the amount of pollen deposited was recorded and the rate that stigmas of individual flow- on stigmas per contact visit and over time. Based on ers were contacted per 15-min observation period (N = stigmatic pollen loads and the number of pollen grains 129) was quantified. required per developed seed, the proportion of flowers that received excess pollen is estimated. Stigmatic pollen loads-The amount of pollen depos- ited on stigmas was determined after flower visitors con- MATERIALS AND METHODS tacted a stigma once, twice, or three times (N = 72, 3 1, and 13 flowers). The stigmas were then collected, stained The study species -Hibiscus moscheutos L. (Malvaceae) with aniline blue, and the pollen grains counted as de- (hereafter referred to as Hibiscus) is a herbaceous peren- scribed above. Stigmas of 13 other flowers were harvested nial found in freshwater and brackish marshes of the and pollen counts were made after the flower had been eastern United States (Brown and Brown, 1984). The main visited, but contact with the stigma did not appear to have research site is a freshwater wetland (locally known as occurred. A previous study had shown that few, if any, Mill Swamp) at the Smithsonian Environmental Research grains reach stigmas in the absence of pollinator visits Center in Edgewater, Maryland where more than 300 due to spatial separation of anthers from stigmas (Spira, individuals of Hibiscus occur. Additional data were col- 1989).-. lected in large populations of Hibiscus near North Beach Stigmatic pollen loads were also quantified after various and off Hwy 450 adjacent to the North River (unless stated time intervals in 1985 and 1990. Freshly opened flowers otherwise, data pertain to Mill Swamp; all three sites are from separate plants were tagged along transects, and stig- in Anne Arundel County, MD). mas from alternate flowers were harvested 1, 2, 3, or 10 Hibiscus plants have few to many upright stems, 1-2 hr after exposure to pollinators. Stigmatic pollen loads m tall, which emerge each spring from a perennial root- were assessed for 63 flowers sampled during 3 d in 1985 stock. The flowering season extends from late July to early and 60 flowers sampled during 2 d in 1990. In 1991, September, and the flowers are large (10-15 cm across) flowers were sampled after about 10 hr exposure to pol- with white or pink petals that remain open for a single linators at two additional sites-North Beach (N = 20) day. Hibiscus is self-compatible, but spatial separation of and North River (N = 10). Stigmas were harvested, stained, anthers from stigmas prevents automatic self-pollination and scored as described above. Heterospecific pollen grains (Spira, 1989). The main pollinator, Ptilothrix bombifor- were rarely observed on stigmas and were not included mis, is a specialist anthophorid bee that utilizes Hibiscus in pollen grain counts. pollen as its primary larval food and has a distribution that extends throughout the range of Hibiscus (Blanchard, RESULTS 1976; Rust, 1980). Moreover, the emergence and foraging of adult Ptilothrix is closely synchronized with the flow- Pollen-seed ratios-The number of pollen grains re- ering period of Hibiscus (Blanchard, 1976; Rust, 1980; quired per developed seed was 2.6 +- 0.3 (2+ 1 SE) based Spira, personal observation). The large flat stigmas, on 19 hand-pollinated flowers in which the ratio of pollen 6-cm-long style, large pollen grains (1 50 pm diam), and grains on stigmas to ovules in the ovary varied from 0.5 five stylar branches per pistil makes this an attractive to 1.5 pollen grains per ovule. This suggests that fewer species for pollen competition studies. than half the pollen grains deposited on stigmas were capable of fertilizing an ovule (seed abortion rates are low; Pollen-seed ratios-Unknown but variable amounts of Snow and Spira, 1991a). If each seed requires about 2.6 outcrossed pollen were added to stigmas of pollinator- pollen grains, and ovaries have an average of 138.5 k 2.9 excluded (bagged) flowers shortly after anthesis. After ap- ovules (X +- SE; N = 25), then approximately 360 pollen proximately 24 hr, stigmas were harvested, stored in a grains must be deposited on the stigmas of an average refrigerator, and then stained with aniline blue.
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