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Frequency-dependent foraging by pollinators
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 constancy〔Chittka, 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). Amer. 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 pollinators〔Waser, 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 floral constancy〔Darwin, 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.〕
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