Pollen presentation and pollination syndromes, with special reference to Penstemon

Abstract

Pollen presentation theory (PPT) allows for a re-examination of some classic themes in pollination biology. Here, we outline its implications in the context of bee-and birdadapted species of Penstemon and Keckiella (Scrophulariaceae). PPT models the optimal schedule of pollen presentation, based on the frequency of visits by pollinators, and the capacities of those pollinators to remove and deposit pollen. High visitation rates, high removal and low deposition all favor plants that present pollen in many small doses. Dosing is achieved through gradual opening of anthers and through anthers opening only narrowly. We hypothesize that bees have higher rates of removal and lower rates of deposition than birds; therefore, bee-pollinated species should have anthers that open more gradually and less completely than bird-pollinated species. Before presenting preliminary results that affirm this prediction, we critically discuss the characterization of species by pollination syndrome. PPT sheds new light on why plants may specialize on particular pollinators. Stebbins' most effective pollinator can be recast as the pollinator that deposits more of the pollen that it removes, thereby making other visitors into conditional parasites. Pollinator shifts might occur when a pollinator with low removal and high deposition becomes abundant; the plants would then be selected to discourage their previous pollinators who are now parasites. Bird-pollination may favor anthers that open quickly and widely, thereby making bees wasteful parasites. Bee-pollination may favor anthers that open slowly and narrowly, thereby making birds ineffective pollinators. In paired comparisons of closely related species, the hummingbird-visited species were redder, had narrower or longer floral tubes, more exserted anthers and stigmas, less pronounced landing platforms, more inclined orientation, produced more nectar of a lower concentration, and had anthers that dehisce faster and more extensively. Extending pollen presentation theory to syndromesThis paper attempts to link classical themes in floral evolution to a new body of theory, using examples from the large genus Penstemon and its segregate genus Keckiella. Adaptation of flowers to pollinators traditionally has been considered in terms of characters such as corolla shape, color, and the placement of sexual organs, but 'pollen presentation theory' (PPT) (Percival 1955) suggests that the scheduling and control of pollen release to visitors should also reflect selection for successful pollination. We first outline the most relevant insights from PPT then review the classical notion of pollination syndromes, to which we add new characters derived from PPT. Turning to organisms, we consider seven pairs of plant species that probably represent independent evolutionary transitions between bee pollination and hummingbird pollination. We gauge the conformity of each P O L L E N P R E S E N TAT I O N A N

Flower Color, Hummingbird Pollination, and Habitat Irradiance in Four Neotropical Forests1

“…Many of the hummingbird-pollinated flowers were further protected from bee visitation by long, tubular corollas as is typical of this syndrome (Feinsinger 1987). This pattern fits the hypothesis recently posed by James D. Thomson, namely, hummingbird flowers are really "not-bee" flowers (Thomson et al 2000). In other words, hummingbirds will visit most flowers, but some flowers are visited only by hummingbirds.…”

Resource partitioning among flower visitors and evolution of nectar concealment in multi–species communities

“…and when X bees are conditional parasites (Thomson et al 2000), fitness increases with visits by X and Y bees, but the positive effect of Y bees is greater: Regardless of whether we are dealing with absolute (Appendix A) or conditional parasites (Appendix B), the model has no evolutionarily stable strategy (ESS); whatever the value of nectar concealment in the population, h, there are values of h 0 ¼ h þ dh, with dh > 0, such that a mutant with nectar concealment h 0 can invade the populations and drive the wild-type morph to extinction. Hence, h will increase for ever unless increasing the level of nectar concealment has some additional cost not related to pollination (e.g.…”

Factors limiting hybridization betweenPenstemon spectabilisandPenstemon centranthifolius

“…Nectaring Hymenoptera included Bombus, Anthophora, Osmia, Centris, Xylocopa, Apis, and the wasp Pseudomasaris vespoides; these nectaring insects often had pollen on their heads and the backs of their thoracies. We also saw a number of small pollen-collecting bees that would turn upside down, manipulating the anthers with their mouth parts and legs; however, we believe that when visitation by nectaring animals is high, pollen collectors are probably parasitic "pollen thieves" (Thomson et al 2000;Wilson and Thomson 1991). Pollen collectors visited both P. spectabilis and P. centranthifolius, and since the animals are small, there are no physical barriers preventing them from reaching the anthers (Mitchell 1989).…”