Fig. 1.2. Degree of pollinator (a) preference, (b) constancy (both expressed as a percentage of bees showing the behavior in each experiment), and (c) Bateman's Index values (based on pooled data for the 10 bees in each experiment) for bees foraging on mixed arrays varying within and between different floral traits. Refer to Table 1.1 for the flower state and traits that were manipulated in each experiment.

Fig. 1.2. Degree of pollinator (a) preference, (b) constancy (both expressed as a percentage of bees showing the behavior in each experiment), and (c) Bateman's Index values (based on pooled data for the 10 bees in each experiment) for bees foraging on mixed arrays varying within and between different floral traits. Refer to Table 1.1 for the flower state and traits that were manipulated in each experiment.

Why are pollinators constant?

The tendency of pollinators to move sequentially among the flowers of the same species has attracted attention since Aristotle's observations of honeybee foraging behavior (Grant 1950). Why insects demonstrate this behavior still remains a mystery, and there are probably multiple factors that promote flower constancy (Chittka et al. 1999). In the simple experiments reported here, we were able to control many of the factors thought to be important in causing selective foraging behavior (e.g., flower spacing, abundance, tube depth, floral complexity, reward quality and quantity, and incomplete information about those rewards on the part of the pollinator). Under these standardized conditions, we were able to induce both constancy and preference in foragers by increasing the variation among floral traits. What general mechanisms could account for these observations.?

All of the hypotheses considered here assume that pollinators are limited in their ability to process, store, or recall information about flowers (for reviews of bee learning see Menzel et al. 1974, 1993; Dukas & Real 1993; Gould 1993; Menzel, this volume). As flowers become more and more dissimilar in display, pollinators should become more efficient if they selectively attend to one or a few key traits on which to base decisions, while ignoring variation in other traits (e.g., Manning 1957; Dukas & Ellner 1993; Dukas & Waser 1994; Wilson & Stine 1996). Although this mechanism is plausible, it does not account for the observation that among-trait variation was more effective in promoting constancy and preference than within-trait variation. Many experiments have suggested that when bees displayed constancy and preference, the selectivity was almost invariably based on flower color. But does this mean that they ignored variation in the other traits besides color. In our experiments, bees sometimes formed secondary preferences based on flower size or complexity or both of these traits together; therefore, these bees did process information on traits besides color.

Once information on floral signals associated with rewarding flowers is stored in short-term memory, it may enter long-term memory through consolidation (Menzel et al. 1974; see Menzel, this volume). Honeybees can learn to associate several colors with reward (Menzel 1969), but if a flower type has not been visited for a critical amount of time, the probability that the next visit will be to the same flower type diminishes (Greggers & Menzel 1993). Studies of honeybee choices on artificial flowers (Marden & Waddington 1981; Greggers & Menzel 1993)

and bumble bee foragers in the field (Chittka et al. 1997) suggest that whether a bee is constant or switches to a different flower type may depend partly on the time (distance) after departing a particular type until the forager encounters another target flower of the same type. If a bee encounters a match with its current flower target within a short time window (3 s of flight), it has a high probability of visiting the same flower type and constancy will be observed; if no matching target is encountered within 4-5 s, a switch of flower types becomes much more likely. These findings suggest that bees are searching for a remembered image as they leave a flower, but that this image decays within a few seconds if the forager does not detect a similar target. This may explain why honeybees are notoriously constant, and why variation within a single trait like color often seems to be sufficient to induce constancy to one color on closely spaced arrays of artificial flowers (e.g., Wells et al. 1983, Wells & Wells 1985), even if alternate colors had a greater reward (Hill etal. 1997). This sort of mechanism fits less well with observations of bumble bees foraging on mixed arrays. They have been reported to switch among flower types differing in single traits such as color, size, shape, and scents, whereas honeybees on the same arrays were constant to one flower type (e.g., Manning 1957). In experiments discussed here, most bumble bees foraged randomly on arrays with variation within single traits. Because flowers were close together in arrays (within 10 cm), foragers would typically have encountered a matching target well within the 3 s window, so it is difficult to reconcile the observed behavior with the above target-matching rule. Comparative studies of both honeybees and bumble bees foraging on the same experimental arrays confirm that there are consistent differences in their learning abilities and foraging patterns (R. J. Gegear & T. M. Laverty, unpublished data).

Selective foraging behavior in pollinators: implications for floral diversity

An obvious characteristic of many natural plant assemblages is the astounding variation of flower types differing in color, shape, scent, size, complexity, etc. Traditionally, this diversity has been seen as driven by the advantages of floral specialization associated with distinct pollinator groups, a process giving rise to "syndromes of pollination" as species diverge through adaptation to the sensory and morphological features of their most effective pollinators (Stebbins 1970; Faegri & van der Pijl 1971; Proctor & Yeo 1973). Paradoxically, however, floral diversity remains high even when most plants in a community are pollinated by the same pollinator group (e.g. Heinrich 1975). Furthermore, field observations usually indicate that most plant species receive visits from a variety of pollinator species and vice versa (Heinrich 1975, 1976; Waser 1983, 1998; Ollerton 1996; Chittka et al., this volume).

An additional explanation is that floral diversity is primarily a means of promoting selectivity by individual pollinators in their choices of flowers, thereby increasing the efficiency of pollination (Heinrich 1975). In this view, floral diversity may not necessarily represent adaptation to specific pollinator species, but rather could be largely an incidental outcome of the typical behavioral response of individual pollinators to variation in floral traits. How do pollinators respond to floral variation.? Our results suggest that, other things being equal, floral variation within a single trait should be less effective at promoting selective foraging behavior in individual pollinators than variability in two or more floral traits. It is tempting to consider these trends with reference to divergence among co-flowering plants in the same area. One of the key components in sympatric divergence is the effectiveness of natural floral variation and pollinator selectivity as a potential isolating mechanism (Chittka et al. 1999). These topics are reviewed below.

Intraspecific variation

Intraspecific floral variation in single traits, particularly in flower color, has been well documented (Kay 1978). In some cases, pollinators seem indifferent to the variation (e.g., Darwin 1876; Manning 1957; Waser 1983; Goulson & Wright 1998). However, other studies report preferential foraging towards different color morphs (e.g., Levin 1972; Kay 1976; Heinrich et al. 1977; Waser & Price 1981; Stanton 1987; see Smithson, this volume) or scent morphs (Galen & Kevan 1980; Galen 1985) of the same species. Preferences for particular morphs may vary from site to site, among different pollinator groups, and at different times of the year. Overall, there seems to be no consistent pattern in these studies, and it is unlikely that such variation could lead to reproductive isolation of different morphs (Waser, this volume). Possibly, examples that have documented selective foraging behavior on different morphs of a single floral trait have overlooked less obvious variation in other traits besides the one of interest, but this needs to be examined in future studies.

Interspecific variation

Much evidence suggests that pollinators do become more selective as flowers become more dissimilar in their traits (e.g., Grant 1950, 1994; Pleasants 1980; Waser 1986; Chittka et al., this volume; Jones, this volume). Examples of cases where flowers differ in two or more floral traits often appear to involve separate races or species. When hybridization is rare despite interfertility of floral forms, workers have often identified at least two traits that supposedly account for the behavioral selectivity shown by the pollinators (e.g., Mather 1947; Grant 1950; McNaughton & Harper 1960; Levin 1972; Jones 1978). Bradshaw et al. (1995) reported that reproductive isolation in two interfertile species of monkeyflowers (the Mimulus lewisii-cardinalis complex) was likely based on differences in quantitative trait loci for eight floral traits, including color, nectar reward, and flower shape. Hybrids between these two species are never found in the wild, perhaps because the two combinations of traits are each preferred by bumble bees or hummingbirds (Schemske & Bradshaw 1999). However, since both types of pollinators have been recorded on each species (Sutherland & Vickery 1993; Waser 1998), the isolation may also be explained by strong constancy shown by individuals visiting flowers differing in multiple traits. This explanation is consistent with observations of bumble bees visiting mixed arrays of both species: individual bees were constant to flowers of one species or the other at a time (R. J. Gegear & T. M. Laverty, unpublished data). More recently, Stout etal. (1998) tested bees on arrays of pairwise combinations of flowers differing in their floral complexity. Bees tended to be more constant to the flowers in the array if the flowers also differed in other traits (such as shape and size) besides the traits (handling method) that were manipulated.

Collectively, these studies support the idea that pollinators become more selective when flower types differ in multiple traits, and that assor-tative movements of individual pollinators could potentially provide effective isolation of cross-fertile forms (see Jones, this volume). Future studies should examine the importance of floral-trait covariation on the selective behavior of pollinators, and also the genetic mechanisms governing the expression of floral traits.

Floral diversity in communities

An attractive proposition is that pollinator behavior, through the benefits of constancy, has selected for divergence of floral traits among co-occurring outcrossed plants. Plant species that competed with each other because they shared pollinators that were inconstant could be "moved" by natural selection to a more isolated location (phenotype) in the space defined by floral traits and sensorimotor learning capabilities ofpollina-tors. This floral-trait niche could represent many dimensions, as long as they interacted to influence sensorimotor learning. Gumbert etal. (1999) recently asked whether flower colors (as defined according to properties of bee color vision) of co-flowering species showed evidence of divergent structure, compared to a random model. At two of five sites, rare plants were more distinct than expected by chance, but common plants at all sites had flower colors that were not distinguishable from chance. Though many reasons could account for not finding strong evidence of divergence in flower colors (see review by Chittka et al. 1999), it is also possible that divergence would not be evident within a single floral trait. Rather, co-flowering species may be distinct when viewed over several floral traits (e.g., color, scent, complexity) because variation in several traits seems most effective in promoting a strong constancy response in pollinators.

Studies looking for structure in floral signals have often focused on single traits such as color, but there is a least one data set that examined community-level patterns of several floral traits among outcrossed species. Ostler & Harper (1978) analyzed floral features of co-occurring (not necessarily co-flowering) plant species in 25 plant communities. Floral-trait diversity was strongly correlated with the number of co-occurring outcrossed species. Flower-color diversity (as assessed by human eyes) in 14 open communities was positively associated with the number of co-occurring species. More important, other floral traits associated with flower-handling methods also showed the same trends. The frequency of restrictive corolla tubes and flowers with bilateral symmetry (which require more elaborate flower-handling techniques) both increased with the diversity of animal-pollinated flowers. That both these traits show the same trend suggests that co-occurring plants are isolated in sensorimotor space. Not only do they vary in several traits, they vary in combinations of traits that are well suited to induce flower selectivity in individual pollinators. Multivariate analyses of floral-trait diversity in plant communities may detect non-randomness that would not necessarily be evident from analyses of a single floral trait such as color.


We thank Lars Chittka, Reuven Dukas, James Thomson, and an anonymous reviewer for their helpful comments on the manuscript. This work was supported by an NSERC operating grant to T. M. Laverty.


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