Animal pollination is a mixed blessing for angiosperms. Animals carry pollen readily because they are mobile and large relative to pollen grains. Furthermore, animals learn to associate floral signals with the presence of food and so move between conspecific plants relatively consistently (Chittka et al., this volume; Gegear & Laverty, this volume; Giurfa, this volume; Menzel, this volume). However, animals act in their own interests, which often conflict with successful pollen transport (e.g., only about 1% of a plant's pollen production reaches stigmas; Harder 2000). Consequently, manipulation of pollinator behavior to promote cross-pollination is a prevailing theme in the evolution of floral design (form, color, nectar, and fragrance production) and display (inflorescence size and architecture).

This chapter reviews three aspects of pollinator manipulation by plants and their effects on pollen dispersal. First, because pollen dispersal for most animal-pollinated plants depends on the general responses of feeding pollinators to their foraging environment, we consider the underlying economic principles that establish the opportunities for floral manipulation. Second, we outline influences on the typical pattern of pollen dispersal among flowers for plants with granular pollen, and summarize how flower design affects this pattern (for a review of dispersal of orchid pollen, see Harder 2000). Finally, because pollination and mating success are characteristics of entire plants, rather than individual flowers, we consider how floral display affects pollinator attraction and within-plant behavior to determine pollen dispersal.

Almost all pollination studies neglect the possible effects of predation on flower visitors. Various authors have even claimed that predation is too infrequent to influence pollinator behavior. It is tempting to dismiss the role of predation because it is rarely observed. In the past two decades, however, ecologists have learned to appreciate the central role that predation risk plays in animal behavior and ecology, mostly through a variety of measures animals take to minimize predation. Studies on a wide variety of animals from zooplankton to mammals have suggested that predation risk affects: diurnal patterns of activity; choice of diet, habitat, food patches, and food type; ways of handling food items; social organization; choice of nest sites; and various physiological factors such as diurnal and seasonal levels of fat reserves and respiration patterns (Price et al. 1980; Lawton 1986; Bernays & Graham 1988; Lima & Dill 1990; Clark 1993; Martin 1995; Lima 1998a, b; Ydenberg 1998).

Are flower-visiting animals really immune to predation, or does the prevailing view about the unimportance of predation in pollination systems merely reflect researchers' inattention? In this chapter, I shall review some of the literature and argue that pollination ecologists have mostly overlooked a central factor influencing pollinator traits and pollination systems. Specifically, I ask: (1) Are there significant levels of predation on pollinators? (2) How might predation affect pollinator traits? And, (3) how might predation influence pollinator–plant interactions?

It often is claimed that Darwin had little to say about the evolution of species, in spite of the title of his 1859 book. This is not strictly true: a close reading of the Origin of Species reveals that Darwin envisioned speciation for the most part as the eventual extension of a process of divergence beginning at a much smaller scale within a single species, and driven for the most part by natural selection. What is true, however, is that a detailed understanding of speciation in its many forms remains an elusive and desirable prize: speciation is, so to speak, the holy grail of evolutionary biology. Many questions confront us still.

Flowers are unreliable, widely distributed food sources, normally offering minute rewards. Flowers of the same kind tend to bloom in close proximity, because plants of the same species growing in patches often bloom simultaneously, or a single plant has many blossoms. Thus, a patch of flowers of the same kind has a location in space and exists for some time, perhaps longer than the lifespan of an insect pollinator. A typical habitat consists of several to many patches of flowers, some of the same species, some of others; pollinators must choose between them.

Hymenopteran pollinators visit flowers to provide food for themselves and their brood. They frequently travel long distances between the nest site and the flower patches, carrying pollen and nectar. Since they must visit many flowers per foraging bout, they need to decide between different flowers in quick succession. Both innate preferences and experience guide the decision-making process (Menzel 1985). Since most of the approach flights are either return visits to a plant or first visits to nearby ones, pollinators are guided mainly by their memories of the location of productive flowers and the particular features of the flowers (signals, manipulatory properties, reward conditions) that the insects learned during previous visits.

Insects' learning capacity and richness of memories are usually underestimated, but studies of learning and memory in honeybees (under both natural and laboratory conditions) demonstrate that learning is fast, and comprises various levels of cognitive processing, such as generalization, categorization, concept formation, configuration, and context-dependency (Menzel & Giurfa 2001).

Ask a member of the general public what kinds of insects pollinate flowers and chances are she'll say bees. Certainly hymenopterans pollinate a tremendous variety of plant taxa, and honeybees and bumble bees in particular are economically important and visible pollinators (McGregor 1976; Buchmann & Nabhan 1996; Proctor et al. 1996). However, studies of social bees have long dominated academic and applied pollination arenas (Lindauer 1963; von Frisch 1967; Menzel 1967), to the relative neglect of other taxa. Insects in three major orders, Coleoptera, Diptera, and Lepidoptera, are key pollinators of a broad range of angiosperm taxa (Kevan & Baker 1983; Proctor et al. 1996), but in comparison with bees, much less is known about their effectiveness as pollinators, or about the sensory attributes and learning abilities that guide their behaviors. This lack of study has several causes, including the lesser importance of non-hymenopteran insects as pollinators of crop plants (notwithstanding their role in pollination of mangos, cacao, papayas, parsnips, pomegranates, carrots, and onions; McGregor 1976), their relative infrequency as major pollinators in European and North American systems (Johnson & Steiner 2000), and the difficulty in raising and studying solitary rather than social insects.

Further study of these neglected pollinators will help us to understand the breadth and diversity of insect sensory systems and learning abilities.

Enthusiasm for optimal foraging theory in the 1970s and 1980s stimulated much work on foraging by bees and, to a lesser extent, hummingbirds. These animals were assumed to be energetically stressed because they were nectarivorous, small, and dependent on costly forms of flight. Researchers sought to explain foraging in terms of movement patterns that saved energy. For example, Pyke (1981) derived movement rules both within and between inflorescences. He compared observed directions and distances of movements following departure from a flower to optimal predictions, under the assumption that the animals should maximize their net rate of energy intake. Pyke (and many others) also assumed that animals would have imperfect knowledge about their environments, particularly with regard to predictions as to what and where to find food in the future. In addition to using statistical rules (Pyke 1984), such animals should always sample in order to track an ever-changing world. Despite the power and appeal of this viewpoint, we now see growing evidence that simple rules and patterns alone cannot explain foraging in hummingbirds. Here, we review how learning and memory influence hummingbird foraging and how memory might affect the ways in which hummingbirds pollinate plants.

Much of a hummingbird's diet is derived from the nectar of flowers that, in turn, rely on hummingbirds for pollination. These flowers frequently provide only a few mg of sugar daily (Kodric-Brown & Brown 1978). Hummingbirds therefore must visit many flowers on each feeding bout, transferring pollen among flowers in the process.

A typical animal pollinator forages non-randomly among plants in a community, using floral cues to recognize the available options. The tendency of individual foragers to restrict their visits to a subset of the available flowering species increases the proportion of pollen grains that arrive on appropriate stigmas. Pollinators partition themselves among plants in several ways, with the common result of assortative mating according to floral type. First, I discuss the evolutionary implications of assortative mating, in light of recent models that emphasize its importance for species divergence, then review the ways in which pollinator behavior contributes to assortative mating among floral types. Finally, I consider how the different forms of non-random pollinator behavior might influence floral evolution and plant speciation.

There is a long-standing tradition of thought that visitation by different pollinators drives divergence of floral form and provides reproductive isolation among incipient plant species (reviewed by Waser, this volume). However, pollinators rarely specialize completely on a single floral type (plant species or distinct phenotype within a species), leading some investigators to question the role of pollinators in the radiation of the angiosperms, and to suggest that floral evolution is largely decoupled from plant speciation (Waser 1998; Chittka et al. 1999). None the less, the remarkable radiation of angiosperms in parallel with pollinators (Grimaldi 1999), and findings that plant families with animal pollination are more speciose than those with abiotic pollination (Dodd et al. 1999), suggest that animal pollination was a key innovation in flowering plant evolution.

The interaction between floral traits and pollinator behavior has been an important force in the coevolution of plants and their animal pollinators. An element of conflict underlies this interaction because the ideal behavior of the pollinator from the plant's point of view may often diverge from that dictated by the pollinator's own self-interest. Because of their immobility, outcrossed plants require a reliable courier that has a high probability of placing their pollen where it has a chance of fertilizing a conspecific ovule. Pollen finding an inappropriate stigma is effectively wasted, and deposition of heterospecific pollen may block receptive sites on the stigma and reduce seed set (e.g., Waser 1978, 1983; Thomson et al. 1981; Campbell & Motten 1985). Thus, plants should benefit if pollinators tend to move sequentially among flowers of the same species, a pattern that an optimally foraging pollinator should rarely adopt unless energetic returns from one plant species regularly exceed those from a mixed diet of some or all of the flower species available. More often, pollinators distribute themselves in an ideal free pattern across resources (Dreisig 1995), thereby minimizing differences in rewards among many different plant species, a pattern that should make generalist foraging the best option.

Yet pollinators often sequentially visit the flowers of one species even though they are bypassing flowers of other available, rewarding plant species (e.g., Grant 1950; Manning 1957; Free 1970; Waser 1983, 1986; Lewis 1989; Goulson & Cory 1993; Laverty 1994b).

We commonly think that biological signals and receivers are mutually tuned to one another. Flower colors and pollinator color vision are not exceptions. The diversity of flower colors and the differences in color vision between different classes of pollinators make speculations about their mutual adaptation tempting. Yet close inspection reveals that we know very little about evolutionary changes in flower color induced by selection pressures related to pollination, nor is there much evidence to show that color vision systems of pollinators have been tuned to flower color. We shall review cases where we think such changes have occurred, and other cases where they have not, even where a purely adaptationist scenario would predict evolutionary tuning.

The idea of making this book arose from a symposium at the XVI International Botanical Congress in St. Louis, USA in August 1999, which brought together some of the contributors of this book. The idea, then, was to inform botanists of important recent developments in pollinator behavior, cognition, and sensory biology. These new findings and perspectives have numerous implications for the evolution of plants and the shaping of plant community structure. Our rationale for such a symposium was that we thought that many botanists are hard-pressed to keep up with the literature concerning pollinator neuroethology and behavioral ecology. Therefore, the field of plant–pollinator interactions is somewhat hobbled by stereotyped, anachronistic, scale-limited, or just simplistic views of how animals really interact with flowering plants.

Our discussions during the symposium (and with other contributors outside the symposium), however, revealed much more profound gaps than just the one between botanists and zoologists. Pollination biology is poised at the boundary between two different traditions, those of proximate and ultimate reasoning in biology. On the one hand, evolutionary ecologists tend to seek adaptive explanations for biological characters – how do the observed traits benefit the animal or plant? Physiologists and neuroethologists, on the other hand, prefer to consider the mechanisms by which environmental stimuli provoke or modify behavior. Unfortunately, these two groups of scientists have little commerce; they publish in different journals, attend different conferences, and tend to disparage each other's views. This was how the biological world was divided until a few years ago.

During the last 30 years, animal behaviorists have become serious players in the quest to understand the interaction between plants and their flower-visiting, foraging pollinators (Waddington 1983, 1997; Barth 1985). Flower-visiting bees, flies, butterflies, and beetles are the sole agents for reproduction in many species of plants. Through the larder of pollen and nectar they provide, plants also affect the foraging success and reproductive output of these insects. The pollinator and the plant, each of separate evolutionary lineages, are in a long-term game where each is dependent on the other and each affects the evolution of the other (Selten & Shmida 1991).

On a local scale, in a field of flowers, a forager such as a nectar-collecting bee makes thousands of sequential decisions during a foraging trip. These decisions are reflected in the choice of flowers visited. These decisions determine: which flowers receive visits and which do not; who mates with whom; the distance between mating plants; the transfer of intra- or interspecific pollen; and the amount of self-pollination and outcrossing. The decisions also affect the bee's success on its foraging foray. Through experience, the bee makes associations between different kinds of flowers (e.g., species) and the rewards they provide, and it seeks out the flowers with the greatest net rewards. Animal behaviorists have played an important role in learning how pollinators make these choices among flowers.

Although general patterns of pollinator foraging behavior have been found, variation among individual foragers has not been well studied.

Pollinator responses to frequency – definitions and importance

Frequency-dependent selection (FDS) occurs when the relative fitness of a genotype or phenotype is a function of its frequency in the population (Wright 1948; Clarke 1962). In behavioral ecology, FDS usually indicates that the identity of the fittest genotype (or phenotype) reverses at some intermediate frequency (Heino et al. 1998). When rare genotypes have an advantage, in this narrow sense of FDS, such selection will result in stable polymorphic equilibria (Clarke & O'Donald 1964). This “negative” FDS has captured the interest of many evolutionary biologists (Ayala & Campbell 1974).

An example of a floral polymorphism believed to be maintained by FDS is heterostyly, a suite of floral traits including reciprocal style- and stigma-length polymorphisms. These polymorphisms can increase the amount of pollen carried to alternative phenotypes, causing rare morphs to have increased outcross mating opportunities (Heuch 1979; Eckert et al. 1996). Such selection arises purely from the architecture of the sexual organs, even if pollinators forage randomly among phenotypes. Levin (1972), however, suggested that behavioral preferences of the pollinators themselves might induce FDS among floral traits.

During the 1960s and early 1970s, a number of studies suggested that behavioral preferences were frequency-dependent (Ayala & Campbell 1974). Allen & Clarke (1968) showed that predators, especially birds, selected proportionately more of the most common prey types in a color-varying prey population, even if energetic rewards were equivalent for the different types.

In a social insect such as the honeybee, the survival of the colony depends on the success of its foragers. The bee optimizes its foraging success by returning to flowers of the species at which it has previously found food. This so-called flower constancy (see Chittka et al. 1999 for references) is based on the bee's capacity to learn and memorize specific flower signals (Menzel et al. 1993; Menzel & Müller 1996; Menzel 1999 and this volume) and to discriminate among different species by their different signals.

A bee returning to the feeding site in search of a flower, be it natural or artificial, must first detect the target from a distance. Once the flower has been detected, the bee will approach it up to a distance at which it is able to recognize whether or not the flower is similar to that stored in memory. Among the different sensory cues used, visual cues are of fundamental importance. In the rich market of coexisting and competing flower species, flower colors, shapes, and patterns are the visual cues that allow bees to recognize and discriminate profitable species.

Here we review studies concerned with the bee's use of visual signals for detecting and recognizing food sources. In the first part of the chapter, we examine the role of the bee's color vision in these tasks. In the second part, we look at the role of several spatial parameters contained in achromatic (black-and-white) stimuli.