Frequency-dependent foraging by pollinators

Last updated
Wildflowers of various corolla colours, shapes and sizes. Lake elsinore wildflowers.jpg
Wildflowers of various corolla colours, shapes and sizes.

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. [1] 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 [2] 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. [3] Although density of a morph will be related to its frequency, common morphs are still preferred when overall plant densities are high. [4]

Contents

Background

Bumblebee (probably Bombus terrestris) with collected pollen visible on hind leg. Bumblebee 05.JPG
Bumblebee (probably Bombus terrestris ) with collected pollen visible on hind leg.

Floral traits, such as corolla color, flower shape, size and scent, appear to have evolved primarily for the purpose of attracting pollinators [5] and many pollinators have learned to associate these floral signals with the reward that is present there. [6] 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. [1] 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, [7] known as directional selection. Alternatively, if rare morphs are preferred, this should promote phenotypic diversity, known as balancing or stabilizing selection. [8] [9]

Interest in frequency-dependent selection dates back to the time of Charles Darwin, who predicted that insects should demonstrate flower constancy [10] and puzzled over the occurrence of deceptive orchid species. [11] 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. [1] Since this time, attention has focussed on understanding how obligately pollinated, unrewarding species can persist as they offer pollinators no incentive to visit. [12] 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. [13]

Bumblebee with tongue extracted about to visit a Heuchera plant for nectar. Bumblebee heuchera.jpg
Bumblebee with tongue extracted about to visit a Heuchera plant for nectar.

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. [14] 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. [4] [12] [13] 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. [15]

Honeybee on a blue flower. Western honey bee.jpg
Honeybee on a blue flower.

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. [13] 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. [13] This pattern is consistent for a variety of nectar concentrations. [14] 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. [12]

Corolla morphs may not be as distinctly colored in natural populations as they are in laboratory experiments. Dawn Endico Bee.jpg
Corolla morphs may not be as distinctly colored in natural populations as they are in laboratory experiments.

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. [13] Bumblebees exhibit an innate preference for blue corollas, as this color is very conspicuous to bees against green-colored backgrounds. [15] 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. [13] 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. [14] Additionally, when density of equally rewarding color morphs were manipulated, bumblebees still preferred to forage on the common morphs, even at high densities. [4]

Field experiments

Experiments conducted in the field have yielded mixed results. Some studies have demonstrated that bumblebees prefer the relatively common corolla color, [16] but in other studies there did not appear to be any observable pattern of bee visitation behavior. [17] 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. [14] Additionally, in natural populations multiple traits that are attractive to pollinators may be genetically correlated with one another (pleiotropy [18] ), so looking at pollinator response to a single trait in isolation may not be appropriate under these circumstances. [14] 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. [13]

A monarch butterfly drinking nectar from a Zinnia flower. Monarch Butterfly Pink Zinnia 1800px.jpg
A monarch butterfly drinking nectar from a Zinnia flower.

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. [1]

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. [19] Several hypotheses have been proposed to suggest how this visitation pattern is maintained.

Search image hypothesis

It has been observed that predators tend to select the most common morph in a population or species. [20] The search image hypothesis proposes that an individual's sensory system becomes better able to detect a specific prey phenotype after recent experience with that same phenotype. [21] It is clear that plant-pollinator interactions differ from predator-prey relationships, as it is beneficial to both the plant and animal for the pollinator to locate the plant. However, it has been suggested that cognitive constraints on short-term memory capabilities may limit pollinators from identifying and handling more than one floral type at a time, [22] [23] making plant-pollinator relationships theoretically similar to predator-prey relationships in regards to the ability to identify food sources. [13] Although plant traits that have evolved to attract pollinators are not cryptic, corolla colors can be more or less conspicuous with the background [24] and pollinators that are more efficient at detecting a particular morph will minimize their search time. Studies have demonstrated that the degree of frequency-dependence increases with the number of flowers visited, which suggests this is a learned response that develops gradually. [13]

Flower morphs may differ in their relative conspicuousness against the background. Wildflowers in SNRA 2.JPG
Flower morphs may differ in their relative conspicuousness against the background.

Search rate hypotheses

Alternative mechanisms, such as the optimal search rate hypothesis [25] and the stare duration hypothesis [26] both propose that there is a tradeoff between search time and the probability of detecting prey. It has been demonstrated that when both density and frequency were manipulated, the strength of the preference for the common morph does not weaken with increased overall density, even when colors that are not innately preferred are the common morph. [13] These results are consistent with both of these search time hypotheses, as bees tend to decrease their speed travelling between flowers when density is high, and therefore, may be more efficient at recognizing less conspicuous yellow flowers at lower speeds. [4]

Switching attention hypothesis

Studies on other organisms have provided evidence that foraging can occur in long runs, but this preference develops after only visiting a few morphs. [27] When presented with two equally rewarding morphs, it has been demonstrated that an organism may select to exclusively forage on one morph for a variable amount of time, and then switch to the alternative morph and repetitively forage on this morph. [27] Under this switching attention hypothesis, selectively foraging on the common morph can occur without invoking a learned response, as the probability of visiting a particular morph first increases as the relative frequency of that morph increases. In other words, it is likely pollinators will select common morphs first due to chance since they are more common and will continue to forage on these morphs during foraging bouts. [13]

Negative frequency-dependent foraging

Pollinators appear to forage in a negative frequency-dependent manner when flowers do not provide nectar rewards, likely to avoid unrewarding morphs. This behaviour results in disassortative mating between different morph types. [12] However, it seems likely that deceptive species would have low reproductive success as pollinators would learn to avoid areas where only unrewarding species are present. [28]

A deceptive orchid, Dactylorhiza sambucina, does not provide a nectar reward for its pollinators. Dactylorhiza sambucina pink NRM.jpg
A deceptive orchid, Dactylorhiza sambucina , does not provide a nectar reward for its pollinators.

Naive pollinators

One hypothesis as to how unrewarding species can persist in the population is that they only receive visits from naive pollinators. [29] As pollinators do not appear to be able to distinguish between rewarding and unrewarding flowers prior to landing, [30] they need to make test visits so they can learn to avoid particular morph types. [31] When a preferred rewarding morph type becomes locally depleted, pollinators may be initially attracted to unrewarding morphs if these morphs exploit signals that are innately attractive [29] or closely mimic rewarding species. [32] However, under this hypothesis, the pollinator should learn to associate this morph with no reward and consequently avoid it on future foraging bouts.

Negative frequency-dependent selection

A different hypothesis does not assume that only naive pollinators visit deceptive species. Instead, the negative reinforcement associated with visiting an unrewarding flower is assumed to be stored in short-term memory. [12] This causes the pollinator to go to a different morph type on its next visit. In other words, if deceptive species were to occur at a low enough frequency that pollinators do not encounter them very often, it is unlikely they will have the opportunity to relocate this information to their long-term memory. Studies have shown that the number of flowers of an unrewarding morph type that are sampled depends on the frequency of those morphs within a population. [14] For example, many species of obligately animal-pollinated, deceptive orchids that co-occur with rewarding flowers are only reproductively successful when they occur at low frequencies. [12] These two hypotheses are not mutually exclusive, in that morph populations that are visited by naive pollinators are also likely to be found at low frequencies relative to rewarding morphs.

Implications

Regardless of the mechanism, pollinators foraging in a frequency-dependent manner on common morphs will lead to assortative mating between similar phenotypes. [33] Additionally, rare morphs may be at a disadvantage if reproductive success is correlated with number of pollinator visits, and this may lead to higher rates of selfing and ultimately inbreeding depression, in self-compatible plants. [12] The potential for a decrease in genetic diversity due to assortative mating can have negative implications.

Lady orchid (left) and naturally occurring lady/monkey hybrid (right). Lady Orchid and Lady-Monkey Orchid hybrid - geograph.org.uk - 1314589.jpg
Lady orchid (left) and naturally occurring lady/monkey hybrid (right).

Climate change

In response to climate change, plants may begin to flower earlier in the season due to regional aridification and a rise in mean global temperature. [34] However, reproductive success of flowering plants that are obligately pollinated ultimately depends on a corresponding change in the timing of pollinator visitors. [35] The earliest bloomers of any species will be rare since the majority of conspecific plants have not yet flowered. Since many pollinators prefer to forage on common phenotypes, the flowers that bloom earliest in the season may be skipped. [35] This may lead to a constraint on plant flowering evolution and the inability of flowering plants to adapt to changing environmental conditions. [14]

Hybrid zones

Additionally, positive frequency-dependent foraging may help maintain hybrid zones between closely related species. [36] Hybrid zones generally contain a wide variety of phenotypes, including novel or extremely rare morphs. Since certain pollinators tend to prefer common morphs, there is a low probability that they will visit rare morphs in the hybrid zone, thus keeping gene flow between species relatively low. [36]

See also

Related Research Articles

<span class="mw-page-title-main">Hypanthium</span> Structure in angiosperms where basal portions form a cup-shaped tube

In angiosperms, a hypanthium or floral cup is a structure where basal portions of the calyx, the corolla, and the stamens form a cup-shaped tube. It is sometimes called a floral tube, a term that is also used for corolla tube and calyx tube. It often contains the nectaries of the plant. It is present in many plant families, although varies in structural dimensions and appearance. This differentiation between the hypanthium in particular species is useful for identification. Some geometric forms are obconic shapes as in toyon, whereas some are saucer-shaped as in Mitella caulescens.

<span class="mw-page-title-main">Pollinator</span> Animal that moves pollen from the male anther of a flower to the female stigma

A pollinator is an animal that moves pollen from the male anther of a flower to the female stigma of a flower. This helps to bring about fertilization of the ovules in the flower by the male gametes from the pollen grains.

<span class="mw-page-title-main">Bumblebee</span> Genus of insect

A bumblebee is any of over 250 species in the genus Bombus, part of Apidae, one of the bee families. This genus is the only extant group in the tribe Bombini, though a few extinct related genera are known from fossils. They are found primarily in higher altitudes or latitudes in the Northern Hemisphere, although they are also found in South America, where a few lowland tropical species have been identified. European bumblebees have also been introduced to New Zealand and Tasmania. Female bumblebees can sting repeatedly, but generally ignore humans and other animals.

<span class="mw-page-title-main">Buzz pollination</span> Technique used by bees to release pollen

Buzz pollination or sonication is a technique used by some bees, such as solitary bees and bumblebees, to release pollen which is more or less firmly held by the anthers. The anthers of buzz-pollinated plant species are typically tubular, with an opening at only one end, and the pollen inside is smooth-grained and firmly attached. With self-fertile plants such as tomatoes, wind may be sufficient to shake loose the pollen through pores in the anther and accomplish pollination. Visits by bees may also shake loose some pollen, but more efficient pollination of those plants is accomplished by a few insect species who specialize in sonication or buzz pollination.

<span class="mw-page-title-main">Entomophily</span> Form of pollination by insects

Entomophily or insect pollination is a form of pollination whereby pollen of plants, especially but not only of flowering plants, is distributed by insects. Flowers pollinated by insects typically advertise themselves with bright colours, sometimes with conspicuous patterns leading to rewards of pollen and nectar; they may also have an attractive scent which in some cases mimics insect pheromones. Insect pollinators such as bees have adaptations for their role, such as lapping or sucking mouthparts to take in nectar, and in some species also pollen baskets on their hind legs. This required the coevolution of insects and flowering plants in the development of pollination behaviour by the insects and pollination mechanisms by the flowers, benefiting both groups. Both the size and the density of a population are known to affect pollination and subsequent reproductive performance.

<i>Bombus terrestris</i> Species of bee

Bombus terrestris, the buff-tailed bumblebee or large earth bumblebee, is one of the most numerous bumblebee species in Europe. It is one of the main species used in greenhouse pollination, and so can be found in many countries and areas where it is not native, such as Tasmania. Moreover, it is a eusocial insect with an overlap of generations, a division of labour, and cooperative brood care. The queen is monogamous which means she mates with only one male. B. terrestris workers learn flower colours and forage efficiently.

<span class="mw-page-title-main">Ornithophily</span> Pollination by birds

Ornithophily or bird pollination is the pollination of flowering plants by birds. This sometimes coevolutionary association is derived from insect pollination (entomophily) and is particularly well developed in some parts of the world, especially in the tropics, Southern Africa, and on some island chains. The association involves several distinctive plant adaptations forming a "pollination syndrome". The plants typically have colourful, often red, flowers with long tubular structures holding ample nectar and orientations of the stamen and stigma that ensure contact with the pollinator. Birds involved in ornithophily tend to be specialist nectarivores with brushy tongues and long bills, that are either capable of hovering flight or light enough to perch on the flower structures.

<span class="mw-page-title-main">Palynivore</span> Group of herbivorous animals

In zoology, a palynivore /pəˈlɪnəvɔːɹ/, meaning "pollen eater" is an herbivorous animal which selectively eats the nutrient-rich pollen produced by angiosperms and gymnosperms. Most true palynivores are insects or mites. The category in its strictest application includes most bees, and a few kinds of wasps, as pollen is often the only solid food consumed by all life stages in these insects. However, the category can be extended to include more diverse species. For example, palynivorous mites and thrips typically feed on the liquid content of the pollen grains without actually consuming the exine, or the solid portion of the grain. Additionally, the list is expanded greatly if one takes into consideration species where either the larval or adult stage feeds on pollen, but not both. There are other wasps which are in this category, as well as many beetles, flies, butterflies, and moths. One such example of a bee species that only consumes pollen in its larval stage is the Apis mellifera carnica. There is a vast array of insects that will feed opportunistically on pollen, as will various birds, orb-weaving spiders and other nectarivores.

<span class="mw-page-title-main">Pollination syndrome</span> Flower traits that attract pollinators

Pollination syndromes are suites of flower traits that have evolved in response to natural selection imposed by different pollen vectors, which can be abiotic or biotic, such as birds, bees, flies, and so forth through a process called pollinator-mediated selection. These traits include flower shape, size, colour, odour, reward type and amount, nectar composition, timing of flowering, etc. For example, tubular red flowers with copious nectar often attract birds; foul smelling flowers attract carrion flies or beetles, etc.

<span class="mw-page-title-main">Nectar robbing</span> Foraging behavior

Nectar robbing is a foraging behavior used by some organisms that feed on floral nectar, carried out by feeding from holes bitten in flowers, rather than by entering through the flowers' natural openings. Nectar robbers usually feed in this way, avoiding contact with the floral reproductive structures, and therefore do not facilitate plant reproduction via pollination. Because many species that act as pollinators also act as nectar robbers, nectar robbing is considered to be a form of exploitation of plant-pollinator mutualism. While there is variation in the dependency on nectar for robber species, most species rob facultatively.

<i>Bombus lapidarius</i> Species of bee

Bombus lapidarius is a species of bumblebee in the subgenus Melanobombus. Commonly known as the red-tailed bumblebee, B. lapidarius can be found throughout much of Central Europe. Known for its distinctive black and red body, this social bee is important in pollination.

<i>Bombylius major</i> Species of fly

Bombylius major is a parasitic bee mimic fly. B. major is the most common type of fly within the Bombylius genus. The fly derives its name from its close resemblance to bumblebees and are often mistaken for them.

<i>Bombus hortorum</i> Species of bee

Bombus hortorum, the garden bumblebee or small garden bumblebee, is a species of bumblebee found in most of Europe north to 70°N, as well as parts of Asia and New Zealand. It is distinguished from most other bumblebees by its long tongue used for feeding on pollen in deep-flowered plants. Accordingly, this bumblebee mainly visits flowers with deep corollae, such as deadnettles, ground ivy, vetches, clovers, comfrey, foxglove, and thistles. They have a good visual memory, which aids them in navigating the territory close to their habitat and seeking out food sources.

<i>Bombus pensylvanicus</i> Species of bee

Bombus pensylvanicus, the American bumblebee, is a threatened species of bumblebee native to North America. It occurs in eastern Canada, throughout much of the Eastern United States, and much of Mexico.

<span class="mw-page-title-main">Flower constancy</span> Tendency to visit certain flower species

Flower constancy or pollinator constancy is the tendency of individual pollinators to exclusively visit certain flower species or morphs within a species, bypassing other available flower species that could potentially contain more nectar. This type of foraging behavior puts selective pressures on floral traits in a process called pollinator-mediated selection. Flower constancy is different from other types of insect specialization such as innate preferences for certain colors or flower types, or the tendency of pollinators to visit the most rewarding and abundant flowers.

<i>Bombus vosnesenskii</i> Species of bee

Bombus vosnesenskii, the yellow-faced bumblebee, is a species of bumblebee native to the west coast of North America, where it is distributed from British Columbia to Baja California. It is the most abundant species of bee in this range, and can be found in both urban and agricultural areas. Additionally, B. vosnesenskii is utilized as an important pollinator in commercial agriculture, especially for greenhouse tomatoes. Though the species is not currently experiencing population decline, urbanization has affected its nesting densities, and early emergence of the B. vosnesenskii has been implicated in the increasing lack of bee diversity on the West coast.

<i>Bombus fervidus</i> Species of bee

Bombus fervidus, the golden northern bumble bee or yellow bumblebee, is a species of bumblebee native to North America. It has a yellow-colored abdomen and thorax. Its range includes the North American continent, excluding much of the southern United States, Alaska, and the northern parts of Canada. It is common in cities and farmland, with populations concentrated in the Northeastern part of the United States. It is similar in color and range to its sibling species, Bombus californicus, though sometimes also confused with the American bumblebee or black and gold bumblebee. It has complex behavioral traits, which includes a coordinated nest defense to ward off predators. B. fervidus is an important pollinator, so recent population decline is a particular concern.

Sexual selection is described as natural selection arising through preference by one sex for certain characteristics in individuals of the other sex. Sexual selection is a common concept in animal evolution but, with plants, it is often overlooked because many plants are hermaphrodites. Flowering plants show many characteristics that are often sexually selected for. For example, flower symmetry, nectar production, floral structure, and inflorescences are just a few of the many secondary sex characteristics acted upon by sexual selection. Sexual dimorphisms and reproductive organs can also be affected by sexual selection in flowering plants.

<span class="mw-page-title-main">Pollinator-mediated selection</span> Process in which pollinators effects a plants evolution

Pollinator-mediated selection is an evolutionary process occurring in flowering plants, in which the foraging behavior of pollinators differentially selects for certain floral traits. Flowering plant are a diverse group of plants that produce seeds. Their seeds differ from those of gymnosperms in that they are enclosed within a fruit. These plants display a wide range of diversity when it comes to the phenotypic characteristics of their flowers, which attracts a variety of pollinators that participate in biotic interactions with the plant. Since many plants rely on pollen vectors, their interactions with them influence floral traits and also favor efficiency since many vectors are searching for floral rewards like pollen and nectar. Examples of pollinator-mediated selected traits could be those involving the size, shape, color and odor of flowers, corolla tube length and width, size of inflorescence, floral rewards and amount, nectar guides, and phenology. Since these types of traits are likely to be involved in attracting pollinators, they may very well be the result of selection by the pollinators themselves.

Bombus hypocrita, also known as the short-tongued bumblebee, is a Japanese bumblebee commonly used in commercial pollination. These short-tongued bumblebees have a proboscis about 7-9mm long, which is folded under their head when flying. Bumblebees are a small fuzzy insect with yellow and black banding along their abdomen. They are round and covered in pile, the hair-like structures that give them their distinct fuzzy appearance.

References

  1. 1 2 3 4 Levin 1972. Low frequency disadvantage in the exploitation of pollinators by corolla variants in Phlox. Am. Nat., 106: 453-460.
  2. ↑ Chittka, L, JD Thomson and NM Waser. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften, 86: 361-377.
  3. ↑ 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.
  4. 1 2 3 4 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.
  5. ↑ Waser, NM. 1983. The adaptive nature of floral traits: ideas and evidence. 242-285. In LA Real (Ed.). Pollination Biology. Academic Press, New York.
  6. ↑ 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.
  7. ↑ Thompson, V. 1984. Polymorphism under apostatic and aposematic selection. Heredity, 53: 677-686.
  8. ↑ Clarke, B. 1962a. Balanced polymorphism and the diversity of sympatric species, 47-70. In D Nichols (Ed.). Taxonomy and Geography. Systematics Association, Oxford.
  9. ↑ Clark, B. 1962b. Natural selection in mixed populations of two polymophyic snails. Heredity, 17: 319-345.
  10. ↑ Darwin, C. 1876. The effects of cross- and self-fertilization in the animal kingdom.
  11. ↑ Darwin, C. 1888. Fertilisation of orchids: the various contrivances by which orchids are fertilised by insects, 2nd ed. London: John Murray.
  12. 1 2 3 4 5 6 7 Smithson, A and MR Macnair. 1997b. Negative frequency-dependent selection by pollinators on artificial flowers without rewards. Evolution, 51: 715-723.
  13. 1 2 3 4 5 6 7 8 9 10 11 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.
  14. 1 2 3 4 5 6 7 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
  15. 1 2 Lunau, K and EJ Maier. 1995. Innate colour preferences of flower visitors. J. Comp. Physiol. A., 177: 1-19.
  16. ↑ Epperson, BK and MT Clegg. 1987. Frequency-dependent variation for outcrossing rate among flower-color morphs of Ipomoea purpurea. Evolution, 41: 1302-1311.
  17. ↑ Jones, KN. 1996. Pollinator behavior and postpollination reproductive success in alternative floral phenotypes of Clarkia gracilis (Onagraceae). Int J Plant Sci., 157: 733-738.
  18. ↑ Waser, NM and MV Price. 1981. Pollinator choice and stabolizing selection for flower color in Delphinium nelsonii. Evolution, 35: 376-390.
  19. ↑ MacArthur, RH and ER Pianka. 1966. On the optimal use of a patchy environment. Am. Nat., 100.
  20. ↑ Allen, JA. 1988. Frequency-dependent selection by predators. Phil. Trans. R. Soc. Lond. B. 319: 485-503.
  21. ↑ Tinbergen, L. 1960. The natural control of insects in pinewoods. I. Factors influencing the intensity of predation by songbirds. Arch. Neerl. Zool., 13: 265-343.
  22. ↑ Dukas, R and LA Real. 1993. Learning constraints and floral choice behaviour in bumble bees. Anim. Behav., 46: 637-644.
  23. ↑ Chittka, L and JD Thomson. 1997. Sensori-moyor learning and its relevance for task specialization in bumble bees. Behav Ecol Sociobiol., 41: 385-398.
  24. ↑ Menzel, R and A Shmida. 1993. The ecology of flower colours and the natural colour vision of insect pollinators. The Israeli flora as a case study. Biol. Rev., 68: 81-120.
  25. ↑ Gendron, RP and JER Staddon. 1983. Searching for cryptic prey: the effect of search rate. Am. Nat., 121: 172-186.
  26. ↑ Endler, JA. 1991. Interactions between predators and prey, 169-196. In JR Krebs and NB Davies (Eds.). Behavioural Ecology, and Evolutionary Approach. 3rd edition. Blackwell Scientific Publications, Oxford.
  27. 1 2 Dawkins, M. 1971. Shifts of 'attention' in chicks during feeding. Anim. Behav., 19: 575-582.
  28. ↑ Gumbert, A and J Kunze. 2001. Colour similarity to rewarding model plants affects pollination in a food deceptive orchid, Orchis boryi. Biol J Linn Soc., 72: 419-433.
  29. 1 2 Nilsson, LA. 1980. The pollination ecology of Dactylorhiza sambucina (Orchidaceae). Botaniska Notiser, 133: 367-385.
  30. ↑ Thomson, JD. 1986. Pollen transport and deposition by bumble bees in Erythronium – Influences of floral nectar and bee grooming. J. Ecology, 74: 329-341.
  31. ↑ Heinrich, B. 1975. Bee flowers: a hypothesis on flower variety and blooming times. Evolution, 29: 325-334.
  32. ↑ Dafni, A. 1984. Mimicry and deception in pollination. Annual Review of Ecology and Systematics. 15: 259-278.
  33. ↑ Stanton, ML. 1987. Reproductive biology of petal colour variants in wild populations of Raphanus saticus: I. Pollinator response to color morphs. Am. J. Bot., 74: 178-187.
  34. ↑ IPCC. 2007. Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the IPCC. Cambridge, UK: Cambridge University press.
  35. 1 2 Forrest, J and JD Thomson. 2008. Pollinator experience, neophobia and the evolution of flowering time. Proc. R. Soc. B, 276: 935-943.
  36. 1 2 Tastard, E, C Andalo, M Giurfa, M Burrus and C Thebaud. 2008. Flower colour variation across a hybrid zone in Antirrhinum as perceived by bumblebee pollinators. Arthropod-Plant Interactions, 2: 237-246.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.