Frequency-dependent foraging is defined as the tendency of an individual to selectively forage on a certain species or morph based on its relative frequency within a population.Levin 1972. Low frequency disadvantage in the exploitation of pollinators by corolla variants in Phlox. Am. Nat., 106: 453-460. Specifically for pollinators, this refers to the tendency to visit a particular floral morph or plant species based on its frequency within the local plant community, even if nectar rewards are equivalent amongst different morphs. Pollinators that forage in a frequency-dependent manner will exhibit flower constancyChittka, L, JD Thomson and NM Waser. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften, 86: 361-377. for a certain morph, but the preferred floral type will be dependent on its frequency. Additionally, frequency-dependent foraging differs from density-dependent foraging as the latter considers the absolute number of certain morphs per unit area as a factor influencing pollinator choice.Bosch, M and NM Waser. 1999. Effects of local density on pollination and reproduction in Delphinium nuttallianum and Aconitum columbianum (Ranunculaceae). Am. J. Bot. 86: 871-879. Although density of a morph will be related to its frequency, common morphs are still preferred when overall plant densities are high.Smithson, A and MR Macnair. 1997a. Density-dependent and frequency-dependent selection by bumblebees Bombus terrestris (L.) (Hymenoptera: Apidae). Biol J Linn Soc., 60: 401-417.
Background
Floral traits, such as corolla color, flower shape, size and scent, appear to have evolved primarily for the purpose of attracting pollinatorsWaser, NM. 1983. The adaptive nature of floral traits: ideas and evidence. 242-285. In LA Real (Ed.). Pollination Biology. Academic Press, New York. and many pollinators have learned to associate these floral signals with the reward that is present there.Menzel, R. 1985. Learning in honey bees in an ecological and behavioural context. 55-74. In B Holldobler and M Lindauer (Eds.). Experimental Behavioral Ecology. Stuttgart: Gustav Fischer. As pollinators are essential in the process of pollen transfer (and therefore, reproductive success) of many angiosperms, visitation behavior will impose frequency-dependent selection on the flower morphs that they visit. If pollinators selectively visit a particular morph, this will cause this morph to increase in frequency, and may ultimately lead to the fixation of this phenotype,Thompson, V. 1984. Polymorphism under apostatic and aposematic selection. Heredity, 53: 677-686. known as directional selection. Alternatively, if rare morphs are preferred, this should promote phenotypic diversity, known as balancing or stabilizing selection.Clarke, B. 1962a. Balanced polymorphism and the diversity of sympatric species, 47-70. In D Nichols (Ed.). Taxonomy and Geography. Systematics Association, Oxford.Clark, B. 1962b. Natural selection in mixed populations of two polymophyic snails. Heredity, 17: 319-345.
Interest in frequency-dependent selection dates back to the time of Charles Darwin, who predicted that insects should demonstrate flower constancyDarwin, C. 1876. The effects of cross- and self-fertilization in the animal kingdom. and puzzled over the occurrence of deceptive orchid species.Darwin, C. 1888. Fertilisation of orchids: the various contrivances by which orchids are fertilised by insects, 2nd ed. London: John Murray. This phenomenon received little attention until the 1970s when Donald Levin suggested that one of the most important factors determining pollinator visitation behavior is the floral trait's frequency in the population relative to other floral elements. Since this time, attention has focussed on understanding how obligately pollinated, unrewarding species can persist as they offer pollinators no incentive to visit.Smithson, A and MR Macnair. 1997b. Negative frequency-dependent selection by pollinators on artificial flowers without rewards. Evolution, 51: 715-723. Much less research has been conducted on frequency-dependent foraging on rewarding species, but experiments using bumblebees have illustrated that frequency likely plays a role in reproductive success of flowering plants.Smithson, A and MR Macnair. 1996. Frequency-dependent selection of pollinators: mechanisms and consequences with regard to behaviour in bumblebees Bombus terrestris (L.) (Hymenoptera: Apidae). J. Evol. Biol., 9: 571-588.
Experimental evidence Researchers studying frequency-dependent visitation behavior seek to understand if pollinator preference is strong enough to induce fixation of traits or to maintain floral polymorphisms observed in natural populations.Smithson, A. 2001. Pollinator preference, frequency dependence, and floral evolution. 237-258. In LD Chittka and JD Thomson (Eds.). Cognitive ecology of pollination: animal behaviour and floral evolution. Cambridge, UK: Cambridge University Press Laboratory experiments use artificial flowers to test how pollinator preference varies with frequency. Typical experiments use two or more colored discs or artificial flowers (to represent flower morphs) that are arranged in various patterns and frequencies. It is predicted that if pollinators do not exhibit frequency-dependent foraging, morph preference will not correlate with the relative frequency of that morph. Instead, this preference may depend on some frequency-independent quality, such as an innate attraction toward a certain color.Lunau, K and EJ Maier. 1995. Innate colour preferences of flower visitors. J. Comp. Physiol. A., 177: 1-19.
Bumblebees
Laboratory experiments Frequency-dependent foraging has most often been observed and studied in bumblebees (Bombus) as they tend to forage for long periods of time without becoming satiated, making them ideal experimental subjects. Simple experiments using two morphs have revealed that after visiting many flowers (more than 100) bumblebees tend to prefer to visit the common morph when rewards associated with both morphs are equal. This pattern is consistent for a variety of nectar concentrations. An exception to this pattern occurs when one morph contains variable amounts of nectar. This reward variability tends to cause the strength of the observed frequency dependence to decrease. However, when both rare and common morphs are unrewarding, bumblebees tend to reverse their behavioral pattern and demonstrate rare morph preference.
Even though these experiments demonstrate that bumblebees forage in a frequency-dependent manner, the strength of this response can be asymmetric for different colors. For example, experiments using blue and yellow discs to represent corolla colors demonstrated that, although bumblebees preferentially foraged on the most common morph when rewards were present, the threshold for switching to the common morph was different for both colors. Bumblebees exhibit an innate preference for blue corollas, as this color is very conspicuous to bees against green-colored backgrounds. It was observed that in order for bees to switch from blue flowers to yellow, the yellow-to-blue ratio had to be much higher than the ratio of blue-to-yellow flowers that were required for the opposite switch. In other words, bees would forage on blue flowers until morphs of this colour reached relatively lower frequencies compared to yellow flowers. However, this preference for blue was not as pronounced when both morphs contained high levels of nectar. Therefore, frequency-dependent preferences must be considered along-with frequency-independent preferences to truly understand the visitation behavior of pollinators. Additionally, when density of equally rewarding color morphs were manipulated, bumblebees still preferred to forage on the common morphs, even at high densities.
Field experiments Experiments conducted in the field have yielded mixed results. Some studies have demonstrated that bumblebees prefer the relatively common corolla color,Epperson, BK and MT Clegg. 1987. Frequency-dependent variation for outcrossing rate among flower-color morphs of Ipomoea purpurea. Evolution, 41: 1302-1311. but in other studies there did not appear to be any observable pattern of bee visitation behavior.Jones, KN. 1996. Pollinator behavior and postpollination reproductive success in alternative floral phenotypes of Clarkia gracilis (Onagraceae). Int J Plant Sci., 157: 733-738. This discrepancy between laboratory and field studies may be due to the fact that laboratory studies use highly contrasting corolla colors and it is likely that color polymorphisms in the wild are not this distinct, making frequency-dependence weaker in natural settings. Additionally, in natural populations multiple traits that are attractive to pollinators may be genetically correlated with one another (pleiotropyWaser, NM and MV Price. 1981. Pollinator choice and stabolizing selection for flower color in Delphinium nelsonii. Evolution, 35: 376-390.), so looking at pollinator response to a single trait in isolation may not be appropriate under these circumstances. Also, frequency-dependent foraging is not apparent until many flowers have been visited (more than 100). Therefore, considering morph frequency within localized patches of flowers in natural settings may not be sufficient. Instead, morph frequency may need to be calculated over large spatial ranges to determine the extent to which pollinators are foraging in a frequency-dependent manner.
Other insects Although studies of frequency-dependent foraging in other pollinator groups seems to be rare, at least one study has demonstrated that butterflies prefer to visit common corolla shapes. This observation was based on reduced seed set of rare morphs in field studies.
Mechanisms
Positive frequency-dependent foraging Foraging on common morphs will be beneficial if these common morphs are associated with a higher reward than rare morphs. However, if rare morphs have similar nectar quality, skipping over these equally rewarding flowers appears to be inconsistent with optimal foraging theory.MacArthur, RH and ER Pianka. 1966. On the optimal use of a patchy environment. Am. Nat., 100. Several hypotheses have been proposed to suggest how this visitation pattern is maintained.
Search image hypothesis