Accessibility / Report Error

Determining factors of flower coloration

ABSTRACT

Diversity and distribution of flower coloration is a puzzling topic that has been extensively studied, with multiple hypotheses being proposed to account for the functions of coloration, such as pollinator attraction, protection against herbivory, and prevention of damage by ultraviolet light. Recent methodologies have allowed studies to consider the visual system of animals other than humans, helping to answer questions regarding the distribution of flower coloration. A survey of keywords in Web of Science shows floral color to be mainly studied in relation to macroevolutionary traits and biochemistry of pigments, focusing on pollination and anthocyanins, respectively. The present paper reviews mechanisms that determine the color of flowers. First, it is discussed how pigment, visual systems and signaling environments influence flower color; secondly, patterns of convergent evolution of flower color is debated, including evolutionary history, pollinator preference, flower color change, flowering season, and habitat. Third and last, patterns of flower coloration that have been found around the globe are addressed. In short, the aim is to contribute to ongoing research, by underlining mechanisms that lead to global patterns of coloration and indicating perspectives for future study on the topic.

Keywords:
floral color; flower coloration; color vision; pollination ecology; sensory drive; flower color change; pollinator preference; color preference; flowering season

Introduction

There are an estimated 308,000 plant species in the world which depend on animals for pollination (Ollerton et al. 2011Ollerton J, Winfree R, Tarrant S. 2011. How many flowering plants are pollinated by animals? Oikos 120: 321-326.) and, hence, need to communicate effectively with different pollinator species to reproduce. Color is a perceptual experience characterized by the interpretation of different wavelengths of light seen by eyes and processed by the brain of an individual (Kemp et al. 2015Kemp DJ, Herberstein ME, Fleishman LJ, et al. 2015. An integrative framework for the appraisal of coloration in nature. American Naturalist 185: 705-724. ; Garcia et al. 2020Garcia JE, Phillips RD, Peter CI, Dyer AG. 2020. Changing how biologists view flowers-color as a perception not a trait. Frontiers in Plant Science 11: 1775. doi:10.3389/fpls.2020.601700
https://doi.org/10.3389/fpls.2020.601700...
). Flowers are sexual organs of plants and contain gametes which can be sensible to the environment (Mu et al. 2017Mu J, Yang Y, Luo Y, Su R, Niklas KJ. 2017. Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb. Ecology and Evolution 7: 2947-2955. ). Flowers use color to communicate with different organisms such as pollinators and herbivores (Lev-Yadun & Gould 2007Lev-Yadun S, Gould KS. 2007. What do red and yellow autumn leaves signal? The Botanical Review 73: 279-289.; Schiestl & Johnson 2013Schiestl FP, Johnson SD. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology and Evolution 28: 307-315.). Pigments used to produce flower color may also function as stress mediators in response to environmental factors (Dalrymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ). Coloration will, then, be selected by several biotic and abiotic pressures throughout the evolutionary history of a plant. These pressures can lead flowers to diverge or converge in their colors within the community.

In order to understand how flower color has been studied in the past, we started by searching Web of Science for flower coloration (precise search terms were “Flower colo$r*” OR “floral colo$r*”). We then inputted articles in VOSviewer to conduct a keyword analysis (Fig. 1). We found that the 40 most used keywords formed two clusters, one focused on ecological and behavioral studies and the other on biochemistry and genetics. The ecology cluster had as its main keywords “evolution”, “pollination” and “bee”; and the biochemistry cluster “anthocyanin”, “flavonoid” and “biosynthesis”.

Figure 1
Word map of key-words associated with flower color. Search was conducted on web of science (21 august 2021) with the keywords: “Flower colo$r*” OR “floral colo$r*”. The $ was used to include the British variation on the word color, and the * was used so color, colors, and coloration would be included. Word map was created on VOSviewer (van Eck & Waltman 2010van Eck NJ, Waltman L. 2010. Software Survey: VOSviewer, a Computer Program for Bibliometric Mapping. Scientometrics: 84: 523-38.) using author keywords and keywords plus. Keywords were manually filtered to join synonyms (i.e. bee, bees, Apis, Bombus, bumblebees were all joined in bee; odour, fragrance, floral scent and scent were all joined in scent) and to exclude uninformative terms (i.e. origin, tool, angiosperm, complex, patterns). The keyword had to appear in at least 10 entries and the 40 most used keywords were selected. Proximity of terms indicate how often they appear together and thickness of line indicated strength of links. Keywords formed two clusters; the one on the left (green) is formed of keywords related to macroevolution and behaviour such as speciation, adaptation, foraging and pollinator-mediated selection. The cluster on the right (blue) is formed of keywords related to pigment synthesis and genetics such as anthocyanin, flavonoid, gene expression and cloning.

Based on this primary exploration, we were interested in three other questions: 1) How many articles are there on different pollinator groups?; 2) How does research on antagonists compare to that on pollination?; and 3) What is the discrepancy in the study of different kinds of pigments? To answer these questions, we ran a second search on Web of Science (all entries on the main collection over the last fifty years) adding different keywords to flower color (“Flower colo$r*” OR “floral colo$r*”) (Tab. 1). Although there might be articles that appear twice (i.e., an article about bees and birds), we do not consider this an issue because we are not directly comparing the literature, only showing how some terms are more common than others. We found that bees are by far the most researched pollinator (448 hits), followed by flies (113 hits) and birds (90 hits); the least researched being butterflies (70 hits), moths (51 hits) and beetles (43 hits). Studies on pollination (638 hits) outnumbered studies on antagonistic interactions (74 hits total with all keywords combined). Lastly, anthocyanin (1051 hits) was the most researched pigment, followed by flavonoid (635 hits), carotenoid (185 hits), and betalain (18 hits). Surprisingly, anthocyanin had more hits than pollination.

Moreover, according to our search outputs, the distribution of flower colors across habitats also appeared as a commonly occurring theme. Flowers can either converge or diverge in color with other flowers in their community. Having distinct coloration from neighbors helps with flower constancy, which is favorable for pollinators to consistently visit rewarding flowers, and for plants to avoid pollen wastage (Waser 1986Waser NM. 1986. Flower constancy: Definition, cause, and measurement. The American Naturalist 127: 593-603.; Chittka 1999Chittka L. 1999. Bees, white flowers, and the color hexagon - A reassessment? No, not yet. Comments on the contribution by Vorobyev et al. Naturwissenschaften 86: 595-597. ; Schaefer et al. 2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.). In this paper, however, we will discuss mechanisms that determine flower coloration. The review is divided in two main sections. The first, with three subsections, examines what factors give color to flowers. The first subsection (section II.a.) briefly states the importance of flower pigments for coloration and stress response. The second (section II.b.) discusses the importance of the viewer in interpreting color signals. The third (section II.c.) considers environmental conditions as an important factor for determining color and how sensory drive could be an interesting framework for the analysis of flower color. In the second section, we present different factors that can lead to flower color convergence, such as: evolutionary history (section III. a.), pollinator pressure (section III. b.), flower color change (section III. c.), flowering season and habitat (section III. d.), and what studies on flower color distribution have shown so far (section III. e.). Finally, we point out future perspectives regarding the study of floral color evolution (section IV).

Table 1
Number of entries on Web of Science of keywords associated with flower color over the last 50 years. Search was conducted on 21 August 2021.

What colors flowers

Pigments and flower coloration

Reflected wavelengths interpreted by visual systems give color to objects. Reflectance of flowers depends on the absorption of wavelengths by pigments (molecules that absorb specific wavelengths) and light scattering that occurs by irregular structured cell complexes (van der Kooi et al. 2014van der Kooi CJ, Wilts BD, Leertouwer HL, Staal M, Elzenga JTM, Stavenga DG. 2014. Iridescent flowers? Contribution of surface structures to optical signaling. New Phytologist 203: 667-673. ). Consequently, pigment strongly influences the reflectance of flowers (Chittka et al. 1994Chittka L, Shmida A, Troje N, Menzel R. 1994. Ultraviolet as a component of flower reflections, and the color perception of hymenoptera. Vision Research 34: 1489-1508. ). There are three major groups of plant pigment: flavonoids (including anthocyanins), carotenoids and betalains. Their core structures differ in light absorption properties and may also be attached to other chemical groups to form more variable flower coloration (Willmer 2011Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.). Pigments are deposited in layers in the petals, and the efficiency of pigment filtering is dependent on the concentration and location of each layer (van der Kooi et al. 2016van der Kooi CJ, Elzenga JTM, Staal M, Stavenga DG 2016. How to color a flower: On the optical principles of flower coloration. Proceedings of the Royal Society B 283: 20160429. doi:10.1098/rspb.2016.0429
https://doi.org/10.1098/rspb.2016.0429...
). Different concentrations of pigments may also affect most of the parameters used for studying flower coloration. These include physical parameters, such as dominant wavelength (hue) and spectral purity (saturation), as well as visual model outputs, such as green contrast (perceptual contrast of two stimuli according to green photoreceptors) and color contrast (perceptual contrast of two stimuli according to all photoreceptors) (Papiorek et al. 2013Papiorek S, Rohde K, Lunau K. 2013. Bees’ subtle color preferences: How bees respond to small changes in pigment concentration. Naturwissenschaften 100: 633-643.; van der Kooi et al. 2019van der Kooi CJ, Dyer AG, Kevan PG, Lunau K. 2019. Functional significance of the optical properties of flowers for visual signalling. Annals of Botany 123: 263-276. ).

Apart from contributing to flower coloration, pigments are also associated with chemical defense against herbivory, this being one of the hypotheses as to why there are different color morphs in the same species. In the wild radish, Raphanus sativus (Brassicaceae), pollinators prefer white and yellow morphs, which have a lower concentration of anthocyanins, in comparison to bronze and pink color morphs having higher concentrations of anthocyanins (Stanton 1987Stanton ML. 1987. Reproductive biology of petal color variants in wild populations of Raphanus sativus. I. Pollinator response to color morphs. American Journal of Botany 74:178-187.). The color morphs with lower anthocyanin concentration, however, are less resistant to herbivory, providing a selective pressure to maintain high pigment morphs (Irwin et al. 2003Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G. 2003. The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84: 1733-1743. ). In star-patterned petunia, Petunia hybrida (Solanaceae), flowers are multi-colored, having a white star pattern at the middle of the corolla, which can have multiple colors surrounding it. The colored part has a higher concentration of anthocyanins and was found to slow the development of lepidopteran larvae (Johnson et al. 2008Johnson ET, Berhow MA, Dowd PF. 2008. Colored and white sectors from star-patterned petunia flowers display differential resistance to corn earworm and cabbage looper larvae. Journal of Chemical Ecology 34: 757-765. ). Thus, it is likely that herbivores avoid plants colored by anthocyanins because they indicate the presence of defensive compounds (Schaefer & Rolshausen 2006Schaefer HM, Rolshausen G. 2006. Plants on red alert: Do insects pay attention? BioEssays 28: 65-71.), a tendency that might also be regarded as aposematism (Lev-Yadun & Gould 2007Lev-Yadun S, Gould KS. 2007. What do red and yellow autumn leaves signal? The Botanical Review 73: 279-289.; Lev-Yadun et al. 2018Lev-Yadun S, Ne’eman G, Keasar T. 2018. Differences in flower colors between spiny and non-spiny Asteraceae species: A possible case of aposematism? Flora 239: 98-103. ). Surprisingly, when evaluating the role of flower color on florivory, Boaventura et al. (2021Boaventura MG, Villamil N, Teixido AL, et al. 2021. Revisiting florivory: An integrative review and global patterns of a neglected interaction. doi: 10.1111/nph.17670
https://doi.org/10.1111/nph.17670...
) did not find color as factor influencing floral damage.

Environmental factors can also exert pressure in selection for pigments (Dalrymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ; Sullivan & Koski 2021Sullivan CN, Koski MH. 2021. The effects of climate change on floral anthocyanin polymorphisms. Proceedings of the Royal Society B 28: 20202693. doi:10.1098/rspb.2020.2693
https://doi.org/10.1098/rspb.2020.2693...
). Certain anthocyanins can block UV radiation and prevent DNA damage (Kootstra 1994Kootstra A. 1994. Protection from UV-B-induced DNA damage by flavonoids. Plant Molecular Biology 26: 771-774. ; Mori et al. 2005Mori M, Yoshida K, Ishigaki Y, et al. 2005. UV-B protective effect of a polyacylated anthocyanin, HBA, in flower petals of the blue morning glory, Ipomoea tricolor cv. Heavenly Blue. Bioorganic and Medicinal Chemistry 13: 2015-2020. ; Koski & Ashman 2015Koski MH, Ashman TL. 2015. Floral pigmentation patterns provide an example of Gloger's rule in plants. Nature Plants 1: 14007. doi:10.1038/nplants.2014.7
https://doi.org/10.1038/nplants.2014.7...
). Accumulation of protective anthocyanins caused by UV radiation produce red to purple colors in exposed tissue (Burger & Edwards 1996Burger J, Edwards GE. 1996. Photosynthetic efficiency, and photodamage by UV and visible radiation, in red versus green leaf coleus varieties. Plant and Cell Physiology 37: 395-399. ), as appears to be the case in Delachampia (Euphorbiaceae) and Acer (Aceraceae) (Armbruster 2002Armbruster WS. 2002. Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-color evolution in two genera. Journal of Evolutionary Biology 15: 468-486.). Plant pigments have also been associated with further functions such as drought resistance, temperature resistance, heavy metal resistance, and antioxidative capabilities (Chalker-Scott 1999Chalker-Scott L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70: 1-9. ; Gould 2004Gould KS. 2004. Nature’s Swiss army knife: The diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology 2004: 314-320. ; Pourcel et al. 2007Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I. 2007. Flavonoid oxidation in plants: From biochemical properties to physiological functions. Trends in Plant Science 12: 29-36.). Indeed, solar radiation was associated with an increase in color contrast in flowers (Darlymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ). Abiotic pressures could select for pigments that modify flower coloration causing convergence of colors in similar stressful environments. Interestingly, species exposed to aridity tended to increase frequency of pigmented morphs (morphs with petals other than white) over time, while species exposed to elevating temperatures tended to decrease frequency of pigmented morphs over time (Sullivan & Koski 2021Sullivan CN, Koski MH. 2021. The effects of climate change on floral anthocyanin polymorphisms. Proceedings of the Royal Society B 28: 20202693. doi:10.1098/rspb.2020.2693
https://doi.org/10.1098/rspb.2020.2693...
). Flower coloration is linked to many characteristics other than mating, being a magic trait (Servedio et al. 2011Servedio MR, Doorn GSV, Kopp M, Frame AM, Nosil P. 2011. Magic traits in speciation: ‘magic’ but not rare? Trends in Ecology and Evolution 26: 389-397.).

Other kinds of color signals include iridescence, gloss, polarization and fluorescence, though there is little evidence for their biological significance (van der Kooi et al. 2019van der Kooi CJ. 2019. The thermal ecology of flowers. Annals of Botany 124: 343-353. ). The presence of pigment alone, however, does not determine flower color. Vacuolar pH and cellular architecture may also have a major role in determining flower coloration (Grotewold 2006Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57: 761-780.; van der Kooi et al. 2019van der Kooi CJ. 2019. The thermal ecology of flowers. Annals of Botany 124: 343-353. ; Dyer et al. 2021Dyer AG, Jentsch A, Burd M, et al. 2021. Fragmentary blue: Resolving the rarity paradox in flower colors. Frontiers in Plant Science 11: 618203. doi: 10.3389/fpls.2020.618203
https://doi.org/10.3389/fpls.2020.618203...
). Varieties of Antirrhinum majus (Plantaginaceae) are perceived differently by their pollinators when having equal pigment concentration but differing cell shape (Glover & Martin 1998Glover BJ, Martin C. 1998. The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80: 778-784.). As it is commonly known, modification of soil pH, and consequently vacuolar pH, will cause a drastic color change in the hydrangea Hydrangea macrophylla, from red to purple or blue (Yoshida et al. 2003Yoshida K, Toyama-Kato Y, Kameda K, Kondo T. 2003. Sepal color variation of Hydrangea macrophylla and vacuolar pH measured with a proton-selective microelectrode. Plant and Cell physiology 44: 262-268. ). Likewise, purple and blue flower variants of Ipomoea nil (Convolvulaceae) do not differ in pigment concentration, but in sap pH (Fukada-Tanaka et al. 2000Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Saito N, Iida S. 2000. Color-enhancing protein in blue petals. Nature 407: 581-582. ). More recently, Stavenga et al. (2021Stavenga DG, Leertouwer HL, Dudek B, van der Kooi CJ. 2021. Coloration of flowers by flavonoids and consequences of pH dependent absorption. Frontiers in Plant Science 11: 600124. doi: 10.3389/fpls.2020.600124
https://doi.org/10.3389/fpls.2020.600124...
) found that changes in vacuolar pH changed the absorbance of several anthocyanins-based pigments. This reveals that flower color may be more flexible than previously thought (Stavenga et al. 2021Stavenga DG, Leertouwer HL, Dudek B, van der Kooi CJ. 2021. Coloration of flowers by flavonoids and consequences of pH dependent absorption. Frontiers in Plant Science 11: 600124. doi: 10.3389/fpls.2020.600124
https://doi.org/10.3389/fpls.2020.600124...
).

Eye of the beholder

Communication through color requires animals to have a visual system that can perceive different wavelengths and interpret them as color. The main flower visitors are insects, mostly because of their function as pollinators, but also because they are quite vicious herbivores, florivores, nectar-robbers, pollen thieves, sapsuckers, and parasites. Hence, animals with similar visual systems can be either beneficial or harmful to the same plant. Some pollinators can even act as nectar robbers depending on the flower visited (Irwin & Brody 2000Irwin RE, Brody AK. 2000. Consequences of nectar robbing for realized male function in a hummingbird-pollinated plant. Ecology 81: 2637-2643.). Although plants move through growth, they do so at a slower rate than animals move, so they cannot modulate visual signals depending on who is around. Color signals are then seen by mutualist and antagonist alike (Schaefer et al. 2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.). Through color, flowers can be conspicuous (Schaefer et al. 2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.), camouflaged (Niu et al. 2018Niu Y, Sun H, Stevens M. 2018. Plant Camouflage: ecology, evolution, and implications. Trends in Ecology and Evolution 33: 608-618.) and even aposematic (Lev-Yadum 2011Lev-Yadun S. 2011. Fearful symmetry in aposematic plants. Plant Signaling and Behavior 6:1739-1740.), but it all depends on who is looking and their sensory capabilities.

Pollinators have different visual systems, such that signal design (comprising what wavelengths it reflects, size, shape, where flowers are located within a plant, etc.) can make flowers cryptic or conspicuous to different organism. For instance, while most humans compare information from three types of photoreceptors (cones) and hence have trichromatic color vision (the exception being color-blind individuals), and can perceive wavelengths in the blue, green, and red range of the color spectrum (Bowmaker 1981Bowmaker JK. 1981. Visual pigments and color vision in man and monkeys. Journal of the Royal Society of Medicine 74: 348-356. ), pollinators usually have a wide range of photoreceptor types (from one to fifteen), often including UV photoreceptors (Herrera et al. 2008Herrera G, Zagal JC, Diaz M, et al. 2008. Spectral sensitivities of photoreceptors and their role in color discrimination in the green-backed firecrown hummingbird (Sephanoides sephaniodes). Journal of Comparative Physiology A 194: 785. doi:10.1007/s00359-008-0349-8
https://doi.org/10.1007/s00359-008-0349-...
; van der Kooi et al. 2021van der Kooi CJ, Stavenga DG, Arikawa K, Belušič G, Kelber A. 2021. Evolution of insect color vision: From spectral sensitivity to visual ecology. Annual Review of Entomology 66: 435-461.).

Most insects, including bees and moths, are trichromats with preserved photoreceptors that detect light in the UV, blue and green part of the electromagnetic spectrum (Peitish et al. 1992Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based color vision. Journal of Comparative Physiology A 170: 23-40.; Briscoe & Chittka 2001Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471-510. ). The most common change in photoreceptors within insects was the addition of a red receptor, which has happened independently many times within lepidoptera (Briscoe & Chittka 2001Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471-510. ). Butterflies may have from as few as three to as many as fifteen kinds of photoreceptors, though most butterflies have six different spectral sensitivities (Arikawa 2017Arikawa K. 2017. The eyes and vision of butterflies. The Journal of Physiology 595: 5457-5464. ). The number of photoreceptors does not necessarily mean better color vision, as they can be used for different mechanisms such as brightness perception (Cuthill et al. 2017Cuthill IC, Allen WL, Arbuckle K, et al. 2017. The biology of color. Science 357: eaan0221. doi:10.1126/science.aan0221
https://doi.org/10.1126/science.aan0221...
). Despite usually having six photoceptors, butterflies have tetrachromatic vision using UV, blue, green and red photoreceptors (Arikawa 2017Arikawa K. 2017. The eyes and vision of butterflies. The Journal of Physiology 595: 5457-5464. ). Hawkmoths are also important pollinators and capable to perceive colors in dim light, with trichromatic vision similar to bees in the UV, blue and green range (Stöckl & Kelber 2019Stöckl AL, Kelber A. 2019. Fuelling on the wing: Sensory ecology of hawkmoth foraging. Journal of Comparative Physiology A 205: 399-413.). Hoverflies also tend to have four photoreceptor varieties, but their color vision is still poorly studied (Lunau 2014Lunau K. 2014. Visual ecology of flies with particular reference to color vision and color preferences. Journal of Comparative Physiology A 200: 497-512. ). Among vertebrates, pollinators worth mentioning are birds and bats. Birds usually have four photoreceptors, tuned to UV, blue, green and red (Herrera et al. 2008Herrera G, Zagal JC, Diaz M, et al. 2008. Spectral sensitivities of photoreceptors and their role in color discrimination in the green-backed firecrown hummingbird (Sephanoides sephaniodes). Journal of Comparative Physiology A 194: 785. doi:10.1007/s00359-008-0349-8
https://doi.org/10.1007/s00359-008-0349-...
), so that they are able to detect the entire color spectrum, like butterflies. Bats, despite being nocturnal, can have cones, in the UV and green range, but there are not enough behavioral test to see if their vision is dichromatic (Müller et al. 2009Müller B, Gloann M, Peichl L, Knop GC, Hagemann C, Ammermüller J. 2009. Bat eyes have ultraviolet-sensitive cone photoreceptors. PLoS ONE 7: e6390. doi:10.1371/journal.pone.0006390
https://doi.org/10.1371/journal.pone.000...
; Kries et al. 2018Kries K, Barros MAS, Duytschaever G, et al. 2018. Color vision variation in leaf-nosed bats (Phyllostomidae): Links to cave roosting and dietary specialization. Molecular Ecology 27: 3627-3640.; Domingos-Melo et al. 2021Domingos-Melo A, Brito VLG, Sérsic A, Cocucci AA, Lunau K, Machado IC. 2021. Shining bright in the dusk: How do bat-pollinated flowers reflect light? Ecology 102: e03416. doi: doi.org/10.1002/ecy.3416
https://doi.org/doi.org/10.1002/ecy.3416...
).

Different visual systems perceive the same flower as different in color depending on their photoreceptors. This is beautifully illustrated by white flowers. For a flower to be white, it needs to activate all photoreceptors in equal proportions. That is, flowers need to reflect blue, green and red to be white for humans. To be perceived as white by bees and moths, a flower would need to reflect UV, blue and green in relatively equal proportions. Flowers need to reflect the entire color spectrum to be perceived as white by butterflies and birds. Therefore, most flowers which are white to humans are not white for any of the mentioned pollinators, because they do not reflect UV light (Kevan et al. 1996Kevan P, Giurfa M, Chittka L. 1996. Why are there so many and so few white flowers? Trends in Plant Science 1: 280-284. ).

Typically, the study of flower coloration has been conducted through behavioral and ecological experiments, which are relatively time-consuming, frequently demand complex logistics, and use human perspective. Nowadays there are methods that help to avoid human perception biases. By using spectrometers or cameras that can even be adapted to UV photography, it is possible to measure how much a certain surface (e.g. flower petals) reflects in every wavelength (reflectance), including the UV region of the spectrum (Stevens et al. 2009Stevens M, Stoddard MC, Higham JP. 2009. Studying primate color: Towards visual system-dependent methods. International Journal of Primatology 30: 893-917. ). Reflectance of objects coupled with visual system information can be input into different computational models that allow the use of animal’s point of view, and the extraction of different parameters such as color contrast, brightness, and even a standardized color category. To use these computational models properly is important to understand the visual system of the animal model, particularly by knowing photoreceptor peak sensitivity, noise and proportions in the retina (Kemp et al. 2015Kemp DJ, Herberstein ME, Fleishman LJ, et al. 2015. An integrative framework for the appraisal of coloration in nature. American Naturalist 185: 705-724. ; Olsson et al. 2018Olsson P, Lind O, Kelber A. 2018. Chromatic and achromatic vision: Parameter choice and limitations for reliable model predictions. Behavioral Ecology 29: 273-282. ).

Many studies refer to color as a categorical variable, but it is important to note that color categorization, that is, the capability to group distinguishable colors (Benard et al. 2006Benard J, Stach S, Giufa M. 2006. Categorization of visual stimuli in the honeybee Apis mellifera. Animal Cognition 9: 257-270. ), might not occur in organisms other than humans (Kelber & Osorio 2010Kelber A, Osorio D. 2010. From spectral information to animal colour vision: Experiments and concepts. Proceedings of the royal society 277: 1617-1625. ), although there is some evidence for it in bees and birds (Benard et al. 2006Benard J, Stach S, Giufa M. 2006. Categorization of visual stimuli in the honeybee Apis mellifera. Animal Cognition 9: 257-270. ; Kelber & Osorio 2010Kelber A, Osorio D. 2010. From spectral information to animal colour vision: Experiments and concepts. Proceedings of the royal society 277: 1617-1625. ). Even when considering human color categories (i.e., blue, yellow, red), there is no consensus on how many categories are used, numbers ranging from as few as four (Warren & Billington 2005Warren J, Billington T. 2005. Flower colour phenology in British mesotrophic grassland communities. Grass and Forage Science 60: 332-336.) to as many as eleven (Dyer et al. 2021Dyer AG, Jentsch A, Burd M, et al. 2021. Fragmentary blue: Resolving the rarity paradox in flower colors. Frontiers in Plant Science 11: 618203. doi: 10.3389/fpls.2020.618203
https://doi.org/10.3389/fpls.2020.618203...
). Furthermore, studies do not account for a clear description of categories, which might be a problem for flowers with transitional colors. If you include red and yellow categories, but not orange, how orange is categorized is a bias of the individual that categorized it. The same problem can be found with other common color descriptions, such as “cream” falling under white or yellow and “pink” falling under red or purple. This lack of concordance in methods makes it difficult to compare studies that use color as a category. It also highlights the importance of using a more standardized and replicable methodology, such as visual modeling.

In the past decade, visual modelling has been consolidated as a powerful tool (Stevens et al. 2009Stevens M, Stoddard MC, Higham JP. 2009. Studying primate color: Towards visual system-dependent methods. International Journal of Primatology 30: 893-917. ; Kemp et al. 2015Kemp DJ, Herberstein ME, Fleishman LJ, et al. 2015. An integrative framework for the appraisal of coloration in nature. American Naturalist 185: 705-724. ; Renoult et al. 2017Renoult JP, Kelber A, Schaefer HM. 2017. Color spaces in ecology and evolutionary biology. Biological Reviews 92: 292-315.; Gawryszewski 2018Gawryszewski FM. 2018. Color vision models: Some simulations, a general n-dimensional model, and the colorvision R package. International Journal of Business Innovation and Research 8: 8159-8170. ), especially when paired with behavioral data (Dyer 2012Dyer AG. 2012. The mysterious cognitive abilities of bees: Why models of visual processing need to consider experience and individual differences in animal performance. Journal of Experimental Biology 215: 387-95.; Olsson et al. 2018Olsson P, Lind O, Kelber A. 2018. Chromatic and achromatic vision: Parameter choice and limitations for reliable model predictions. Behavioral Ecology 29: 273-282. ). While taking into account the features of any visual system that might be of interest, a visual modelling study can measure and contrast the raw reflectance of flowers and their backgrounds (Chittka et al. 1994Chittka L, Shmida A, Troje N, Menzel R. 1994. Ultraviolet as a component of flower reflections, and the color perception of hymenoptera. Vision Research 34: 1489-1508. ; Arnold et al. 2009Arnold SEL, Le Comber SC, Chittka L. 2009b. Flower color phenology in European grassland and woodland habitats, through the eyes of pollinators. Israel Journal of Plant Sciences 57: 211-230. b), considering them to be illuminated by different ambient light conditions. Despite the limitation of visual information not being available for most species, visual modeling offers theoretical analyses that have potential to produce several important predictions, considering multiple kinds of pollinators and fostering future behavioral work.

The two most common models for analyses of flower coloration are the “color hexagon” and the “receptor noise limited”. The “color hexagon” is a model specific for bee vision. It employs opponency of the photoreceptors to create a 2D space comprised of six regions, representing bee color categories (blue, blue-green, green, UV-green, UV and UV-blue); and the distance between flowers within the space can also be used to distinguish two stimuli (Chittka 1992Chittka L. 1992. The colour hexagon: A chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. Journal of Comparative Physiology 170: 533-543. ). This model is the most commonly used to analyze flower coloration. The “receptor noise limited” (RNL) model is a generalist color model that can be applied to many different animals, given that proper parameters are known. It has already been validated for the visual system of bees, primates and birds (Osorio & Vorobyev 1996Osorio D, Vorobyev M. 1996. Colour Vision as an Adaptation to Frugivory in Primates. Proceeding of the Royal Society B 263: 593-599.; Vorobyev et al. 1998Vorobyev M, Osorio D, Bennett AT, Marshall NJ, Cuthill IC. 1998. Tetrachromacy, oil droplets and bird plumage colours. Journal of Comparative Physiology A 183: 621-633. ; Vorobyev et al. 2001Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R. 2001. Colour thresholds and receptor noise: Behaviour and physiology compared. Vision Research 41: 639-653. ). The RNL model determines if two surfaces might be distinguishable by the visual system of the modelled receiver, according to their color distance (i.e., color contrast). It may also be used to extract brightness information, though not originally design to do so (Olsson et al. 2018Olsson P, Lind O, Kelber A. 2018. Chromatic and achromatic vision: Parameter choice and limitations for reliable model predictions. Behavioral Ecology 29: 273-282. ). Both models allow users to input peak photoreceptors sensitivity, ambient light and background coloration, which factors are fundamental to simulate how color is perceived in natural environments, which often vary in light and background noise. R software includes a specific package for analyzing color vision: Pavo 2.0, which can easily calculate many different color models (Maia et al. 2013Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD. 2013. pavo: An R Package for the analysis, visualization and organization of spectral data. Methods in Ecology and Evolution 4:609-613.; 2019Maia R, Gruson H, Endler JA, White TE. 2019. pavo2: New tools for the spectral and spatial analysis of colour in r. Methods in Ecology and Evolution 10: 1097-1107. ). Color hexagon and RNL models have become the basis of other ways of analysing color (Garcia et al. 2020Garcia JE, Phillips RD, Peter CI, Dyer AG. 2020. Changing how biologists view flowers-color as a perception not a trait. Frontiers in Plant Science 11: 1775. doi:10.3389/fpls.2020.601700
https://doi.org/10.3389/fpls.2020.601700...
; van den Berg et al. 2020van den Berg CP, Troscianko J, Endler JA, Marshall NJ, Cheney KL. 2020. Quantitative Colour Pattern Analysis (QCPA): A comprehensive framework for the analysis of colour patterns in nature. Methods in Ecology and Evolution 11: 316-332. ).

Signaling environment

Adding to the reflection of objects and the sensory capabilities of the viewer, ambient light and background noise will also shape the perception of flower coloration (Fig. 2). The same flower can be perceived as pink by reflecting pink under white light or by being a white flower under pink light (Chittka et al. 2014Chittka L, Faruq S, Skorupski P, Werner A. 2014. Color constancy in insects. Journal of Comparative Physiology A 200: 435-448. ) (Fig. 2A). To solve the problem that natural illumination can vary in intensity and in spectral composition, organisms have developed color constancy, that is, the effect by which objects tend look the same color despite varying light (Foster 2011Foster DH. 2011. Color constancy. Vision Reserach 51: 674-700. ). In bees, color constancy is achieved by integrating visual information from the ocelli (Garcia et al. 2017Garcia JE, Hung YS, Greentree AD, Rosa MGP, Endler JA, Dyer AG. 2017. Improved color constancy in honey bees enabled by parallel visual projections from dorsal ocelli. PNAS 114: 7713-7718. ); it is not, however, perfect (Dyer 1998Dyer AG. 1998. The color of flowers in spectrally variable illumination and insect pollinator vision. Journal of Comparative Physiology A 183: 203-212. ). Indeed, bees have been shown to detect changes in ambient light and use them as contextual cues (Lotto & Chittka 2005Lotto RB, Chittka L. 2005. Seeing the light: Illumination as a contextual cue to color choice behavior in bumblebees. PNAS 102: 3852-3856. ). Furthermore, bees prefer to forage under brighter light, making it easier to distinguish flower colors (Arnold & Chittka 2012Arnold SEJ, Chittka L. 2012. Illumination preference, illumination constancy and color discrimination by bumblebees in an environment with patchy light. Journal of Experimental Biology 215: 2173-2180.). The filtering of ambient light in areas with abundance of woody long-lived plants, in comparison to herbaceous species, might explain why some flowers appear to have lighter corollas (Hensel & Sargent 2012Hensel LE, Sargent RD. 2012. A phylogenetic analysis of trait convergence in the spring flora. Botany 90:557-564.). Ambient light also varies across seasons, especially in deciduous or semi-deciduous forests, in which the falling of the leaves will cause a different light filtering (Endler 1993Endler JA. 1993. The color of light in forests and its implications. Ecological Monographs 63: 1-27. ).

Figure 2
Factors that influence light perception. A) Purple is a multispectral color composed of blue and red light. A flower can be perceived as purple by viewers that are sensitive to blue and red photoreceptors, such as hummingbirds. For a flower to be perceived as purple it can be a white flower (capable of reflecting all wavelengths) under red and blue illumination; or a purple flower (capable of reflecting red and blue light) under white illumination. Viewers that cannot capture red light, such as bees, would see a purple flower under white illumination as blue. B) Typical optical illusion highlighting the importance of background coloration on color perception. The flower on the left appears darker than the flower on the right even though they are the same color.

The background against which an object is presented can influence how we perceive certain colors, this being illustrated by several optical illusions (Fig. 2B) (Kelley & Kelley 2014Kelley LA, Kelley JL. 2014. Animal visual illusion and confusion: The importance of a perceptual perspective. Behavioral Ecology 25: 450-463. ). Likewise, depending on the background contrast, the same flower may be perceived as bearing different colors, so that pressure to overcome background noise might be crucial to the development of conspicuous colors (Bukovac et al. 2017Bukovac Z, Shrestha M, Garcia JE, Burd M, Dorin A, Dyer AG. 2017. Why background color matters to bees and flowers. Journal of Comparative Physiology A 203: 369-380. ). Plants that develop dense foliage might overcome visual background noise (Bukovac et al. 2017Bukovac Z, Shrestha M, Garcia JE, Burd M, Dorin A, Dyer AG. 2017. Why background color matters to bees and flowers. Journal of Comparative Physiology A 203: 369-380. ), helping bees, for instance, forage under more visually uniform conditions (Forrest & Thomsom 2009Forrest J, Thomson JD. 2009. Background complexity affects color preference in bumblebees. Naturwissenschaften 96: 921-925. ). For flower species that occur in more than one environment (e.g. one with dense foliage and spread out vegetation), and/or for backgrounds that go through seasonal changes (e.g. falling leaves), flower signals would also have to overcome varying background noise, which could impose important selective pressure on the evolution of flower coloration on different populations. In Eastern Mediterranean flora, in order to overcome background noise, red flowers bloom before the green foliage develops, enhancing red flower contrast against sandy background (Willmer 2011Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.).

According to Endler’s theory of sensory drive, environmental bias, noise and the receiver’s sensory capabilities tend to shape the evolution of signals by selecting signals and receivers that better overcome environmental noise, resulting in more conspicuous signals and more efficient receivers (Endler 1992Endler JA. 1992. Signals, signal conditions, and the direction of evolution. American Naturalist 139: 125-153. ). In pollination systems, plants emit signals via flowers and different species of pollinators receive those signals to interpret them in a foraging context. Predictively, bees prefer to forage in flowers that are more conspicuous in their background (Forrest & Thomson 2009Forrest J, Thomson JD. 2009. Background complexity affects color preference in bumblebees. Naturwissenschaften 96: 921-925. ). Since conspicuousness diminishes search time, we should expect the same for other pollinators. Pollinator receivers have a variety of visual systems that act as selective pressure for conspicuous flower coloration (Stournaras & Schaefer 2017Stournaras K, Schaefer HM. 2017. Does flower and fruit conspicuousness affect plant fitness? Contrast, color coupling and the interplay of pollination and seed dispersal in two Vaccinium species. Evolutionary Ecology 31: 229-247.; Koski 2020Koski MH. 2020. The role of sensory drive in floral evolution. New Phytologist 227: 1012-1024. ). Flowers of the same species are present in several different environments and, since they cannot relocate, are restricted to the signaling conditions of the given location. This suggests that environmental factors play a greater role in the evolution of plant signals than in that of animal signals (Koski 2020Koski MH. 2020. The role of sensory drive in floral evolution. New Phytologist 227: 1012-1024. ).

Sensory drive (Endler 1992Endler JA. 1992. Signals, signal conditions, and the direction of evolution. American Naturalist 139: 125-153. ) predicts that plants in the same signaling environments would converge in a conspicuous flower coloration determined by environmental signaling conditions. In the understory of a green forest, and according to the illuminant spectra registered by Endler (1993)Endler JA. 1993. The color of light in forests and its implications. Ecological Monographs 63: 1-27. , we would expect to find many yellow flowers, as the canopy filters most of the red and blue light; while on treetops, where the broad spectrum of the sun is found, we should expect no difference in abundance of flowers of different colorations, except for green flowers, which would not contrast well against the green dappled foliage. Surprisingly, increased cloud coverage in Australia was associated with low color diversity (Dalrymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ). Alternatively, in small clearings, where ambient light is shifted towards longer wavelengths (Endler 1993Endler JA. 1993. The color of light in forests and its implications. Ecological Monographs 63: 1-27. ), red flowers would benefit, while under a woodland shade, where natural light is more bluish (Endler 1993Endler JA. 1993. The color of light in forests and its implications. Ecological Monographs 63: 1-27. ), we would expect blue flowers to evolve. Nevertheless, in forests and grasslands of Germany (which vary in illumination and background), flowers seem to have similar colors according to the honeybee visual system (Binkenstein & Schaefer 2015Binkenstein J, Schaefer HM. 2015. Flower colors in temperate forest and grassland habitats: A comparative study. Arthropod-Plant Interactions 9: 289-299. ). Different altitudes also vary in ambient light and background. In Colorado (USA), ambient UV light increased with altitude and different altitudes had different backgrounds (foliage or bare), which impacted the conspicuity and preference for fly and bee pollinators (Finnell & Koski 2021Finnell LM, Koski MH. 2021. A test of Sensory Drive in plant-pollinator interactions: Heterogeneity in the signalling environment shapes pollinator preference for a floral visual signal. New Phytologist. doi:10.1111/nph.17631
https://doi.org/10.1111/nph.17631...
).

The importance of sensory drives is that it offers a distinct framework of how to integrate environmental heterogeneity and visual perception in the evolution of flower signals (Koski 2020Koski MH. 2020. The role of sensory drive in floral evolution. New Phytologist 227: 1012-1024. ). Signaling conditions are often overlooked when looking for patterns of color convergence in different habitats, as it is uncommon to find studies which control different background colors or light environments. The popularity of visual modeling will probably overcome this oversight in coming years. For more information on sensory drive in flower signals, we recommend the recent review published by Koski (2020)Koski MH. 2020. The role of sensory drive in floral evolution. New Phytologist 227: 1012-1024. .

Patterns of convergence

Evolutionary history

Flowers are dependent on their genetic make-up to determine their pigments and color possibilities (Chittka 1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ). Yet some cultivated flowers, like roses, can come in a wide variety of color, such as red, pink, yellow, orange, white, violet and even green (Eugster & Märki-Fischer 1991Eugster CH, Märki‐Fischer E. 1991. The chemistry of rose pigments. Angewandte Chemie 30: 654-672. ). Plants can also produce fruits of a different color than their flowers, which exemplify that plants may allocate different pigments to serve distinct functions (Chittka 1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ). Both examples show that flowers can rapidly evolve new colors given enough selective pressure (Chittka 1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ). Related plants can have similar colored flowers because of their ancestral state, if there is not enough pressure to diverge from it. Some plant families tend to have similar colors. Apiaceae flowers, for example, are human white (bee blue-green) and vary mostly in brightness (in this case measured as the distance from the center of the color hexagon) rather than hue (measured as the angle from the center of the hexagon, varying from 0° to 360°) (Chittka 1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ). The uncommonness of bee-white flowers has been associated with phylogenetic constraints (Chittka 1999Chittka L. 1999. Bees, white flowers, and the color hexagon - A reassessment? No, not yet. Comments on the contribution by Vorobyev et al. Naturwissenschaften 86: 595-597. ; Koski & Ashman 2016Koski MH, Ashman TL. 2016. Macroevolutionary patterns of ultraviolet floral pigmentation explained by geography and associated bioclimatic factors. The New Phytologist 211: 708-718. ). Other groups, however, have a tendency to preserve flower color (Chittka 1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ). In Solanaceae, biochemical pathways leading to red flowers by anthocyanin, or by double production of anthocyanin and carotenoids, seem to express phylogenetic signals (Ng & Smith 2016Ng J, Smith SD. 2016. Widespread flower color convergence in Solanaceae via alternate biochemical pathways. New Phytologist 209: 407-417. ).

Changes in flower color are common both between species and within species (polymorphism) (Roguz et al. 2020Roguz K, Gallagher MK, Senden E, et al. 2020. All the colors of the rainbow: Diversification of flower color and intraspecific color variation in the genus Iris. Frontiers in Plant Science 11: 569811. doi:3389/fpls.2020.569811
https://doi.org/3389/fpls.2020.569811...
). This could be because in certain clades few mutations lead to new colorations. In Antirrhinum majus (Plantaginaceae), for example, a single gene mutation may lead to color change in flowers (Dyer et al. 2007Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L. 2007. Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower color. Arthropod-Plant Interactions 1: 45-55. ). Likewise, in columbines (Aquilegia, Ranunculaceae), the loss of a single enzyme in the biopathway of some anthocyanins can cause blue to red transitions in flower color (Hodges & Derieg 2009Hodges SA, Derieg NJ. 2009. Adaptive radiations: from field to genomic studies. PNAS 1: 9947-9954. ). The type of mutation necessary to change flower color could explain the overrepresentation of some transitions in flower colorations (Sobel & Streisfeld 2013Sobel JM, Streisfeld MA. 2013. Flower color as a model system for studies of plant evo-devo. Frontiers in Plant Science 4: 1-17.). Blue to red (e.g. Ipomoea) and pigmented to white transitions, for instance, are more common than red to blue (e.g. Sinningia) or white to pigmented (Raucher 2008Raucher MD. 2008. Evolutionary Transitions in floral color. International Journal of Plant Sciences 169: 7-21.; Ma et al. 2017Ma Q, Zhang W, (Jenny) Xiang Q-Y. 2017. Evolution and developmental genetics of floral display-A review of progress. Journal of Systematics and Evolution 55: 487-515. ). Despite the biochemical pathways for the production of anthocyanin being well understood (Ma et al. 2017Ma Q, Zhang W, (Jenny) Xiang Q-Y. 2017. Evolution and developmental genetics of floral display-A review of progress. Journal of Systematics and Evolution 55: 487-515. ), studies with other pigment groups are still needed to understand the relationship between mutations and flower color.

Different clades have different mutation rates and higher mutation rates can lead to higher diversification rates (Hua & Bromham 2017Hua X, Bromham L. 2017. Darwinism for the genomic age: Connecting mutation to diversification. Frontiers in Genetics 8: 12. doi: 10.3389/fgene.2017.00012
https://doi.org/10.3389/fgene.2017.00012...
). Indeed, plants can accumulate mutations that will eventually lead to polymorphisms which are simply not selected against (Sapir et al. 2021Sapir Y, Gallagher MK, Senden E. 2021. What maintains flower colour variation within populations? Trends in Ecology & Evolution 36: 507-519.). Adaptative radiation can exemplify how closely related flowers can easily diverge in color. The iris, Iris lutescens (Iridaceae), has two color morphs, with different distributions across Spain and France, different processes seeming to be in play in the two regions (Wang et al. 2016Wang H, Talavera M, Min Y, Flaven E, Imbert E. 2016. Neutral processes contribute to patterns of spatial variation for flower color in the Mediterranean Iris lutescens (Iridaceae). Annals of Botany 117: 995-1007.). Spain has monomorphic populations of either yellow or purple flowers that have little to no gene flow between them, and genetic drift seems to be the factor determining the polymorphism. In France, however, where genes flow between these populations, most populations are polymorphic and composed of both colors. Similarly, in the milk thistle Silybum marianum (Asteraceae), founding effect and genetic drift seem to explain the variations of color morphs along the Mediterranean (Keasar et al. 2016Keasar T, Gerchman Y, Lev-Yadun S. 2016. A seven-year study of flower-color polymorphism in a Mediterranean annual plant. Basic and Applied Ecology 17: 741-750.). The importance of random and neutral factors on flower color polymorphism has only recently come into light, as most studies focus on balancing selection of flower color (Sapir et al. 2021Sapir Y, Gallagher MK, Senden E. 2021. What maintains flower colour variation within populations? Trends in Ecology & Evolution 36: 507-519.). Evolutionary history may also affect color because it allows for similar plants to withstand similar environmental factors, and hence to bloom close to each other (Kemp et al. 2019Kemp JE, Bergh NG, Soares M, Ellis AG. 2019. Dominant pollinators drive non-random community assembly and shared flower color patterns in daisy communities. Annals of Botany 123: 277-288. ). In Nepal, monocots are more present in lower elevations, and there is more color diversity at higher elevations (Shrestha et al. 2013Shrestha M, Dyer AG, Bhattarai P, Burd M. 2013. Flower color and phylogeny along an altitudinal gradient in the Himalayas of Nepal. Journal of Ecology 102: 126-135.).

It is difficult to define color as a variable for phylogenetic analyses, especially to avoid bias of human vision, so several studies approach evolutionary history from alternative methods. While some studies found phylogenetic signal in flower coloration (Ng & Smith 2016Ng J, Smith SD. 2016. Widespread flower color convergence in Solanaceae via alternate biochemical pathways. New Phytologist 209: 407-417. ; Reverté et al. 2016Reverté S, Retana J, Gómez JM, Bosch J. 2016. Pollinators show flower color preferences but flowers with similar colors do not attract similar pollinators. Annals of Botany 118: 249-257.; Shrestha et al. 2013Shrestha M, Dyer AG, Bhattarai P, Burd M. 2013. Flower color and phylogeny along an altitudinal gradient in the Himalayas of Nepal. Journal of Ecology 102: 126-135.), others did not (Smith et al. 2008Smith SDW, Ané C, Baum DA. 2008. The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution 62: 793-806.; Arnold et al. 2009Arnold SEJ, Savolainen V, Chittka L. 2009a. Flower colors along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod-Plant Interactions 3: 27-43. a; McEwen & Vamosi 2010McEwen JR, Vamosi JC. 2010. Floral color versus phylogeny in structuring subalpine flowering communities. Proceedings of the Royal Society B 277: 2957-2965. ; Weber et al. 2018Weber MG, Cacho NI, Phan MJQ, Disbrow C, Ramírez SR, Strauss SY. 2018. The evolution of floral signals in relation to range overlap in a clade of California Jewelflowers (Streptanthus s.l.). Evolution 72: 798-807. ). Inasmuch as phylogenetic effect varies across groups, it is important to include phylogeny as a possible cause for patterns of flower coloration. Compiling studies on phylogenetic signal would be a welcome measure toward understanding the evolution of flower coloration.

Pollinator pressure

The diversity of flower color is often attributed to pollination pressure and sexual selection, as flowers are the sexual organs of plants, and their traits can influence plant fitness (Schiestl & Johnson 2013Schiestl FP, Johnson SD. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology and Evolution 28: 307-315.). This could, however, be a reflection on the overrepresentation of pollination studies (18.8 %, Tab. 1) in flower coloration literature in comparison to antagonistic interactions (2 %, Tab. 1). In this section, we will address characteristics of pollinator’s behavior and visual systems that might lead flowers colors to converge.

Many pollinators display innate color preference when visiting flowers (Lunau & Maier 1995Lunau K, Maier EJ. 1995. Innate color preferences of flower visitors. Journal of Comparative Physiology A 177: 1-19. ; Gumbert 2000Gumbert A. 2000. Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning. Behavioral Ecology and Sociobiology 48: 36-43. ). Bees, for instance, have innate preference towards the violet-blue color range (Briscoe & Chittka 2001Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471-510. ), and pipevine swallowtail butterflies have innate preferences for yellow, blue and purple (Weiss 1997Weiss MR. 1997. Innate colour preferences and flexible colour learning in the pipevine swallowtail. Animal Behavior 53: 1043-1052. ). Innate preferences can be overcome by learning to associate rewards with colors (Gumbert 2000Gumbert A. 2000. Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning. Behavioral Ecology and Sociobiology 48: 36-43. ; Weiss & Papaj 2003Weiss MR, Papaj DR. 2003. Color learning in two behavioural contexts: How much can a butterfly keep in mind? Animal Behaviour 65: 425-434. ). In the pollination context, this is important because not all flowers produce equal rewards. Associative learning is important for pollinators, because it renders better foraging efficiency and fitness (Raine & Chittka 2008Raine NE, Chittka L. 2008. The correlation of learning speed and natural foraging success in bumble-bees. Proceedings of the Royal Society B 275: 803-808.). Some pollinators, however, can go back to relying on innate preferences when their preferred flowers are unavailable, even after learning (Gumbert 2000Gumbert A. 2000. Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning. Behavioral Ecology and Sociobiology 48: 36-43. ). Innate preference, then, support trait convergence, because by having flower coloration that matches pollinator preference, flowers can recruit pollinators more readily.

Pollinators also exhibit flower constancy, that is, the habit of a flower visitor effectively to restrict their visits to a few flower species or morphs (Chittka et al. 1999Chittka L, Thomson JD, Waser NM. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86: 361-377. ). Flower constancy is important for plants because it diminishes pollen wastage (Schaefer et al. 2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.). Having distinct coloration from neighboring plants facilitates this process (Schaefer et al. 2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.) and is one main argument for flower color divergence. Indeed, competition for pollinators was linked to flower color diversity in hummingbird-pollinated Iochrominae (Solanaceae) (Muchhala et al. 2014Muchhala N, Johnsen S, Smith SD. 2014. Competition for hummingbird pollination shapes flower color variation in Andean Solanaceae. Evolution 68: 2275-2286. ). This problem could be overcome by having other morphological traits that aid distinction, such as different shape. In the Erica genus (Ericaceae), flowers from the same community are more likely to be similar in color when they differ in other morphological features (Coetzee et al. 2021Coetzee A, Seymour CL, Spottiswoode CN. 2021. Facilitation and competition shape a geographical mosaic of flower colour polymorphisms. Functional Ecology 00:1-11. ).

The reproductive success of a plant is dependent on the kind of visitor it attracts (Schemske & Horvitz 1984Schemske DW, Horvitz CC. 1984. Variation among floral visitors in pollination ability: A precondition for mutualism specialization. Science 225: 519-521.). In Calathea ovandensis (Marantaceae), Hesperiidae butterflies account for 21 % of visits but for less than 1 % of seed set. Bombus medius (bumblebee) and Rhathymus sp. (bee), however, only had 5 % of visits, but were responsible for 22 % of seed set. Therefore, it is important to attract animals with the necessary behavior and morphology to pollinate properly. Some characteristics are overrepresented in flowers pollinated by certain functional groups (Fenster et al. 2004Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35: 375-403. ). Based on that, flowers are grouped by their morphological features, such as color, in pollination syndromes according to which pollinator it is supposed to attract (Willmer 2011Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.). These morphological characteristics would have converged due to pressure by pollinators that prefer certain characteristics. Color preferences are often used in pollination syndromes (Dellinger 2020Dellinger AS. 2020. Pollination syndromes in the 21st century: Where do we stand and where may we go? New Phytologist 228: 1193-1213. ). For example, red flowers are typically associated with bird pollination and blue with bee pollination (Willmer 2011Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.). Indeed, in Australia, bird-pollinated plants showed convergence for red-flowered plants (see the bee-avoidance hypothesis bellow) (Burd et al. 2014Burd M, Stayton T, Shrestha M, Dyer AG. 2014. Distinctive convergence in Australian floral colors seen through the eyes of Australian birds. Proceedings of the Royal Society B 281: 20132862. doi:10.1098/rspb.2013.2862
https://doi.org/10.1098/rspb.2013.2862...
).

Floral color, however, is not always the most reliable characteristic of pollination syndromes. In fact, a recent review found that color was the most uninformative trait studied in flower syndromes in the last decade (Dellinger 2020Dellinger AS. 2020. Pollination syndromes in the 21st century: Where do we stand and where may we go? New Phytologist 228: 1193-1213. ). Results vary with the location and clade studied. In snapdragons, Antirrhineae (Plantaginaceae), flower morphology, including flower color, had an overall positive predictive value of 65.95 % for pollinators and flower visitors (Guzmán et al. 2017Guzmán B, Gómez JM, Vargas P. 2017. Is floral morphology a good predictor of floral visitors to Antirrhineae (snapdragons and relatives)? Plant Biology 19: 515-524. ). Momose et al. (1998Momose K, Yumoto T, Nagamitsu T, et al. 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. American Journal of Botany 85: 1477-1501.) associated flowers of a lowland dipterocarp forest in Sarawak (Malaysia) to pollination syndromes, and found that pollination syndromes relate to certain flower characteristics, such as reward, shape, and flowering time, but not to color. In Erysimum (Brassicaceae), lilac flowers were related to a pollinator niche comprised of large long-tonged bees, but it seems that the development of lilac flowers pre-dates this pollinator preference, and is probably related to other environmental factors which eventually led to bee pollination (Gómez et al. 2015Gómez JM, Perfectti F, Lorite J. 2015. The role of pollinators in floral diversification in a clade of generalist flowers. Evolution 69: 863-878. ). Overall, it is possible that color predictability of pollinator-color interactions only plays a role in certain clades (Dellinger 2020Dellinger AS. 2020. Pollination syndromes in the 21st century: Where do we stand and where may we go? New Phytologist 228: 1193-1213. ). Interestingly, pollinators seem to prefer a certain flower color, but flower color does not determine pollinator assemblage (Reverté et al. 2016Reverté S, Retana J, Gómez JM, Bosch J. 2016. Pollinators show flower color preferences but flowers with similar colors do not attract similar pollinators. Annals of Botany 118: 249-257.). Caution is necessary when interpreting these works because human vision is often used to determine the categories of flower coloration. Perhaps the use of ecologically relevant visual systems would allow for less varied results.

Schaefer et al. (2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.) argue that the idea of pollination syndromes is outdated, because plants could have converged in flower coloration to exclude eavesdroppers just as easily as to attract pollinators. This notion fits well within the idea of private communication channels, that is, a communication system that involves a signal to which an eavesdropper is insensitive (Stevens 2013Stevens M. 2013. Sensory ecology, behavior & evolution. Oxford, Oxford University Press.), and underlies the bee-avoidance hypothesis which explain why bird-pollinated flowers often are red. Despite common belief, birds do not have innate color preferences (Lunau et al. 2011Lunau K, Papiorek S, Eltz T, Sazima M. 2011. Avoidance of achromatic colors by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214: 1607-1612. ). Instead, bees are generally insensitive to longer wavelengths (Peitsch et al. 1992Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based color vision. Journal of Comparative Physiology A 170: 23-40.), meaning that red flowers are hard for bees to detect. The red color serves to generate a private communication channel between red flowers and birds (Lunau et al. 2011Lunau K, Papiorek S, Eltz T, Sazima M. 2011. Avoidance of achromatic colors by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214: 1607-1612. ), excluding bee visitors that can be nectar robbers in hummingbird-pollinated species (Irwin & Brody 2000Irwin RE, Brody AK. 2000. Consequences of nectar robbing for realized male function in a hummingbird-pollinated plant. Ecology 81: 2637-2643.). Red flowers that are pollinated by bees usually have a secondary reflectance peak in the UV range, which makes them conspicuous to bees; red flowers pollinated by birds, however, reflect only longer wavelengths which birds can easily detect, but bees cannot (Lunau et al. 2011Lunau K, Papiorek S, Eltz T, Sazima M. 2011. Avoidance of achromatic colors by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214: 1607-1612. ; de Camargo et al. 2019de Camargo MGG, Lunau K, Batalha MA, Brings S, de Brito VLG, Morellato LPC. 2019. How flower color signals allure bees and hummingbirds: A community-level test of the bee avoidance hypothesis. New Phytologist 222: 1112-1122. ; Chen et al. 2020Chen Z, Niu Y, Liu C-Q, Sun H. 2020. Red flowers differ in shades between pollination systems and across continents. Annals of Botany 12: 837-848. ). Interestingly, yellow flowers seem to follow the same trend, where bird-pollinated flowers absorb UV and bee-pollinated flowers reflect UV at the periphery (Papiorek et al. 2016Papiorek S, Junker RR, Alves-dos-Santos I, et al. 2016. Bees, birds and yellow flowers: Pollinator-dependent convergent evolution of UV patterns. Plant Biology 18: 46-55.). Absence of UV-reflection in the center of yellow flowers could, however, also be seen as stamen mimicry (Lunau 2005Lunau K. 2005. Stamens and mimic stamens as components of floral colour patterns. Botanische Jahrbucher fur Systematik Pflanzengeschichte und Pflanzengeographie 127: 13-42. ). It is noteworthy that pollinators, such as butterflies and flies, which can also detect red flowers, are usually not included in studies evaluating the bee-avoidance hypothesis. Indeed, fly-pollinated flowers also seem to tend to reflect longer wavelengths and absorb shorter wavelengths (Shrestha et al. 2019Shrestha M, Burd M, Garcia JE, Dorin A, Dyer AG. 2019a. Color evolution within orchids depends on whether the pollinator is a bee or a fly. Plant Biology 21: 745-752.a). Another way to exclude unwanted visits is camouflage. Flowers of Eucomis autumnalis and Eucomis comosa (Asparagaceae) are visually cryptic by having a similar color to leaves, attracting pollinators solely by smell (Shuttleworth & Johnson 2009Shuttleworth A, Johnson SD. 2009. A key role for floral scent in a wasp-pollination system in Eucomis (Hyacinthaceae). Annals of Botany 103: 715-725.). Unfortunately, camouflage is a poorly studied topic in plants (Niu et al. 2018Niu Y, Sun H, Stevens M. 2018. Plant Camouflage: ecology, evolution, and implications. Trends in Ecology and Evolution 33: 608-618.). Previously, dull-colored bat pollinated flowers were considered as camouflaged from other visitors (Fleming et al. 2009Fleming TH, Geiselman C, Kress WJ. 2009. The evolution of bat pollination: a phylogenetic perspective. Annals of Botany 104: 1017-1043. ), but bats and other pollinators can use visual cues from these flowers (Domingos-Melo et al. 2021Domingos-Melo A, Brito VLG, Sérsic A, Cocucci AA, Lunau K, Machado IC. 2021. Shining bright in the dusk: How do bat-pollinated flowers reflect light? Ecology 102: e03416. doi: doi.org/10.1002/ecy.3416
https://doi.org/doi.org/10.1002/ecy.3416...
).

Pollinator pressure might also lead to convergence due to receiver bias in pollinators (Schaefer & Ruxton 2009Schaefer HM, Ruxton GD. 2009. Deception in plants: Mimicry or perceptual exploitation? Trends in Ecology and Evolution 24: 676-685.). This happens when animals apply selection pressure on flowers, imposed by traits that did not evolve via interactions with flowers (Schiestl 2017Schiestl FP. 2017. Innate Receiver Bias: Its Role in the Ecology and Evolution of Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics 48: 585-603.). Receiver bias can be innate preference for certain flower traits. Flower guides, stingless bee nest entrances, and insectivorous pitchers, for example, tend to have dark centers, radiating striped and peripheral dots which have been linked to finding mates or nesting ground (Biesmeijer et al. 2005Biesmeijer JC, Giurfa M, Koedam D, Potts SG, Joel DM, Dafni A. 2005. Convergent evolution: Floral guides, stingless bee nest entrances, and insectivorous pitchers. Naturwissenschaften 92: 444-450. ; Schiestl & Johnson 2013Schiestl FP, Johnson SD. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology and Evolution 28: 307-315.). Plants that do not offer any reward, but still manage to attract pollinators using pre-existing bias, are attracting pollinators via deception (Schiestl 2017Schiestl FP. 2017. Innate Receiver Bias: Its Role in the Ecology and Evolution of Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics 48: 585-603.). This deceit system can be the precursor of another kind of deceptive pollination, namely, mimetic flowers, because innate biases will lead flowers to converge without the need of a specific flower model (Schaefer & Ruxton 2009Schaefer HM, Ruxton GD. 2009. Deception in plants: Mimicry or perceptual exploitation? Trends in Ecology and Evolution 24: 676-685.; Schiestl 2017Schiestl FP. 2017. Innate Receiver Bias: Its Role in the Ecology and Evolution of Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics 48: 585-603.). Considering the visual system of most insects evolved before flowers (Chittka 1996Chittka L. 1996. Does bee color vision predate the evolution of flower color? Naturwissenschaften 83: 136-138. ; van der Kooi et al. 2021van der Kooi CJ, Stavenga DG, Arikawa K, Belušič G, Kelber A. 2021. Evolution of insect color vision: From spectral sensitivity to visual ecology. Annual Review of Entomology 66: 435-461.), and most flowers are only a fraction of possible colors (Chittka et al. 1994Chittka L, Shmida A, Troje N, Menzel R. 1994. Ultraviolet as a component of flower reflections, and the color perception of hymenoptera. Vision Research 34: 1489-1508. ), receiver bias could have had a major role shaping flower color to pollinator pre-flower preference.

Flower color change

Flower color is not static through time, something often forgotten when studying global patterns of flowering. Flower age can affect flower color, as many plants show a dramatic color change, different from senescence (Weiss 1995Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.). This phenomenon has been found in over 70 families of plants (Weiss 1995Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.). Byrsonima variabilis (Malpighiaceae), for instance, changes standard petal color during anthesis from yellow to orange and finally red, and bees preferentially visit flowers with yellow standard petals when foraging for pollen (de Melo et al. 2018de Melo BT, Mota T, Schlindwein C, Antonini Y, Oliveira R. 2018. Floral color change in Byrsonima variabilis (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees. Science of Nature 105: 46. doi:10.1007/s00114-018-1572-y
https://doi.org/10.1007/s00114-018-1572-...
). The retention of old flowers increases display size and, by doing so, increases attraction of pollinators (Ishii & Sakai 2001Ishii HS, Sakai S. 2001. Effects of display size and position on individual floral longevity in racemes of Narthecium asiaticum (Liliaceae). Functional Ecology 15: 396-405. ). Indeed, prolonged longevity of flowers may increase pollination even without color change (Teixido et al. 2019Teixido AL, Duarte MO, Ballego-Campos I, et al. 2019. One for all and all for one: Retention of color-unchanged old flowers increases pollinator attraction in a hermaphroditic plant. Plant Biology 21: 167-175. ). It seems, however, that the retention of old flowers without color change might come at a cost, because it leads to plant-level avoidance by pollinators with spatial memory (Makino & Ohashi 2017Makino TT, Ohashi K. 2017. Honest signals to maintain a long-lasting relationship: Floral color change prevents plant-level avoidance by experienced pollinators. Functional Ecology 31: 831-837.). Here we aim to explore how flowers not only converge on specific colors, but also on strategy of flower color change (Weiss 1995Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.).

Flower color change has been extensively associated with directing pollinators to rewarding flowers, inasmuch as flowers are unrewarding after color change (Weiss 1995Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.). Indeed, at close range, flower color change can direct pollinators to rewarding flowers (Sun et al. 2005Sun SG, Liao K, Xia J, Guo YH. 2005. Floral color change in Pedicularis monbeigiana (Orobanchaceae). Plant Systematics and Evolution 255: 77-85.) and is often considered an honest signal (Schaefer et al. 2004Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.; Makino & Ohashi 2017Makino TT, Ohashi K. 2017. Honest signals to maintain a long-lasting relationship: Floral color change prevents plant-level avoidance by experienced pollinators. Functional Ecology 31: 831-837.). Nevertheless, when considering long-distance attraction, it seems pollinators struggle to determine the proportion of rewarding to unrewarding flowers (Oberrath & Böhning-Gaese 1999Oberrath R, Böhning-Gaese K. 1999. Floral color change and the attraction of insect pollinators in lungwort (Pulmonaria collina). Oecologia 121: 383-391. ; Kudo et al. 2007Kudo G, Ishii HS, Hirabayashi Y, Ida TY. 2007. A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees. Oecologia 154: 119-128. doi:10.1007/s00442-007-0820-1
https://doi.org/10.1007/s00442-007-0820-...
). Insects have poor visual acuity, and typically only use color cues at short distances, relying on green receptor contrast for long distance detection (Giurfa et al. 1996Giurfa M, Vorobyev M, Kevan P, Menzel R. 1996. Detection of coloured stimuli by honeybees: Minimum visual angles and receptor specific contrasts. Journal of Comparative Physiology A 178: 699-709.; Vorobyev et al. 1997Vorobyev M, Gumbert A, Kunze J, Giurfa M, Menzel R. 1997. Flowers through insect eyes. Israel Journal of Plant Sciences 45: 93-101. ; de Ibarra et al. 2015de Ibarra NH, Langridge KV, Vorobyev M. 2015. More than colour attraction: Behavioural functions of flower patterns Current Opinion in Insect Science 12: 64-70.). For this reason, flower color change may attract pollinators at long distances via deception, by maintaining an increased display that includes unrewarding color-changed flowers that cannot be differentiated from rewarding flowers. Once pollinators approach, however, it provides an honest signal, regarding which flowers are rewarding (Brito et al. 2015Brito VLG, Weynans K, Sazima M, Lunau K. 2015. Trees as huge flowers and flowers as oversized floral guides: The role of floral color change and retention of old flowers in Tibouchina pulchra. Frontiers in Plant Science 6: 362. doi:10.3389/fpls.2015.00362
https://doi.org/10.3389/fpls.2015.00362...
). Since there might be a delay between flowers being emptied of reward and color change, flower color change might be better termed a “semi-honest” signal, that is, a signal that diminishes uncertainty, but is not completely reliable (Ruxton & Schaefer 2013Ruxton GD, Schaefer HM. 2013. Game theory, multi-modal signalling and the evolution of communication. Behavioral Ecology and Sociobiology 67: 1417-1423. ).

There are other benefits from the retention of old color-changed flowers, because even without increased attraction, floral color change can decrease the amount of geitonogamous pollination (when pollen is transferred from one flower to another of the same plant) (Ida & Kudo 2003Ida TY, Kudo G. 2003. Floral color change in weigela middendorffiana (caprifoliaceae): Reduction of geitonogamous pollination by bumble bees. Israel Journal of Plant Sciences 90: 1751-1757. ). Flower color change seems to be such an advantage that some wonder why it is not prevalent among angiosperms (Ruxton & Schaefer 2016Ruxton GD, Schaefer HM. 2016. Floral color change as a potential signal to pollinators. Current Opinion in Plant Biology 32: 96-100.). Flower color change is, altogether, more common than it gets credit for, and new reports of color-changing flowers are found often, even in the UV range (Ohashi et al. 2015Ohashi K, Makino TT, Arikawa K. 2015. Floral color change in the eyes of pollinators: Testing possible constraints and correlated evolution. Functional Ecology 29: 1144-1155. ). Flower color change has evolved many times (Weiss 1995Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.), and this outcome could be due to a simple mechanism. Pollinators have been shown to recognize old flowers, as is the case in Rosa virginiana (Rosaceae), where second day flowers are paler, and bees preferentially visit younger flowers (MacPhail et al. 2007MacPhail VJ, Kevan PG, Fuss C. 2007. Effect of flower age on honey bee behaviour when rewards are kept constant. Journal of Apicultural Research 46: 293-294. ). Pigments, especially anthocyanins, are altered by sunlight (Grotewold 2006Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57: 761-780.). Though color change may happen in any pigment, most color changes seem to be associated with variation in anthocyanins (Weiss 1995Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.; Lippi et al. 2011Lippi MM, Giuliani C, Gonnelli T, Bini LM. 2011. Floral color changes in Boswellia sacra Flueck. (Burseraceae): A dialogue between plant and pollinator. Flora 206: 821-826. ). In Viola cornuta (Violaceae) flowers, changes in color are due to anthocyanins; when flowers are grown in the dark, they do not show color change, as opposed to a white to purple change that occurs under light conditions (Farzad et al. 2002Farzad M, Griesbach R, Weiss MR. 2002. Floral color change in Viola cornuta L. (Violaceae): A model system to study regulation of anthocyanin production. Plant Science 162: 225-231. ). Thus, the first color changing in flowers would be brought upon by senescence. Natural selection would refine this natural change, inasmuch as flower color change benefits plants by attracting more pollinators (Ishii & Sakai 2001Ishii HS, Sakai S. 2001. Effects of display size and position on individual floral longevity in racemes of Narthecium asiaticum (Liliaceae). Functional Ecology 15: 396-405. ; Ida & Kudo 2010Ida TY, Kudo G. 2010. Modification of bumblebee behavior by floral color change and implications for pollen transfer in Weigela middendorffiana. Evolutionary Ecology 24: 671-684. ) and by diminishing geitonogamous pollination (Ida & Kudo 2003Ida TY, Kudo G. 2003. Floral color change in weigela middendorffiana (caprifoliaceae): Reduction of geitonogamous pollination by bumble bees. Israel Journal of Plant Sciences 90: 1751-1757. ; Sun et al. 2005Sun SG, Liao K, Xia J, Guo YH. 2005. Floral color change in Pedicularis monbeigiana (Orobanchaceae). Plant Systematics and Evolution 255: 77-85.); while it benefits pollinators by diminishing foraging time (Kudo et al. 2007Kudo G, Ishii HS, Hirabayashi Y, Ida TY. 2007. A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees. Oecologia 154: 119-128. doi:10.1007/s00442-007-0820-1
https://doi.org/10.1007/s00442-007-0820-...
). The first step into flower color change would be to retain older flowers (as flowers that fall from the plant do not go through color change), and such retention does not happen in multiple species. The cost of flower maintenance is, then, crucial to better understand this phenomenon.

There are other hypotheses that could explain flower color change. A pollinator may learn to visit plants that have honest signals regarding rewarding flowers, so a plant could evolve color change in response to that (Makino & Ohashi 2017Makino TT, Ohashi K. 2017. Honest signals to maintain a long-lasting relationship: Floral color change prevents plant-level avoidance by experienced pollinators. Functional Ecology 31: 831-837.; Ohashi et al. 2015Ohashi K, Makino TT, Arikawa K. 2015. Floral color change in the eyes of pollinators: Testing possible constraints and correlated evolution. Functional Ecology 29: 1144-1155. ). Another fascinating explanation is that flower color change is a step toward transitioning flowers from one pollinator to another, being ephemeral in evolutionary time (Ruxton & Schaefer 2016Ruxton GD, Schaefer HM. 2016. Floral color change as a potential signal to pollinators. Current Opinion in Plant Biology 32: 96-100.). In Combretum indicum (Combretaceae), white flowers are mostly visited by moths, while red ones are visited by butterflies (Yan et al. 2016Yan J, Wang G, Sui Y, Wang M, Zhang L. 2016. Pollinator responses to floral color change, nectar, and scent promote reproductive fitness in Quisqualis indica (Combretaceae). Scientific Reports 6: 24408. doi:10.1038/srep24408
https://doi.org/10.1038/srep24408...
). Of course, different explanations could apply to different groups presenting flower color change, as there is a predisposition for flower color to change in some families (Ohashi et al. 2015Ohashi K, Makino TT, Arikawa K. 2015. Floral color change in the eyes of pollinators: Testing possible constraints and correlated evolution. Functional Ecology 29: 1144-1155. ).

Flowering season and habitat

Another recurring theme in the literature is that plants with flowers of certain colors bloom at certain seasons (Willmer 2011Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.). Insects can change their color preference over time through learning (Gumbert 2000Gumbert A. 2000. Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning. Behavioral Ecology and Sociobiology 48: 36-43. ; Weiss & Papaj 2003Weiss MR, Papaj DR. 2003. Color learning in two behavioural contexts: How much can a butterfly keep in mind? Animal Behaviour 65: 425-434. ). Sharp & James (1979Sharp JL, James J. 1979. Color preference of Vespula squamosa. Environmental Entomology 8: 708-710.) found that yellowjackets were most attracted to traps painted buttercup yellow during spring and summer, and traps painted Saturn yellow during fall and winter. This move could be triggered by the blooming of abundant species. Aydin (2011Aydin G. 2011. Plant phenology-related shifts in color preferences of Epicometis (tropinota) hirta (coleoptera: scarabaeidae: cetoniinae) adults - key to effective population monitoring and suppression. Florida Entomologist 94: 832-838. ) found that the beetle Tropinota hirta (Scarabaeidae) alternated color preference during blooming of cherry trees, preferring light blue traps when flowers were in bloom and white traps before and after cherry blooming. Although blooming time is important for pollinator attraction, there are too few papers evaluating pollinator preference over seasons to be able to access how this affects flower communities.

The abundance of insects with color preference can also change throughout the year (Kevan 1983Kevan PG. 1983. Floral colors through the insect eye: What they are and what they mean. In: Jones E, Little J. (eds.) The handbook of experimental pollination biology. Scientific and Academic Editions. pp. 3-30.). In Australia, Epacris impressa (Ericaceae) has different color morphs, which vary across seasons. The white morph is found in spring and the red in winter. This pattern of occurrence seems to be related to abundance of pollinators, because birds are present in winter, when the red morph blooms, and white morphs occur in spring, when insects are more plentiful (Stace & Fripp 1977Stace HM, Fripp YJ. 1977. Raciation in Epacris impressa. II. Habitat differences and flowering times. Australian Journal of Botany 25: 315-323.). Similar patterns were also found in the Tibetan flower Gentiana leucomelaena (Gentianaceae), where white morphs are more abundant when ambient temperature is higher and there are more fly pollinators available, but blue morphs are more common when it is colder and bee pollinators prevail (Mu et al. 2010Mu J, Li G, Sun S. 2010. Petal color, flower temperature, and behavior in an alpine annual herb, Gentiana leucomelaena (Gentianaceae). Arctic, Antarctic, and Alpine Research 42: 219-226. ; Mu et al. 2017Mu J, Yang Y, Luo Y, Su R, Niklas KJ. 2017. Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb. Ecology and Evolution 7: 2947-2955. ).

Another hypothesis that could explain color differences due to ambient temperature is related to flower heat. Flowers of darker color will be warmer than light colored flowers, as they absorb more heat (Koski & Galloway 2021Koski MH, Galloway LF. 2021. Geographic variation in floral color and reflectance correlates with temperature and colonization history. Frontiers in Plant Science 11: 991. doi: 10.3389/fpls.2020.00991
https://doi.org/10.3389/fpls.2020.00991...
). Warmer flowers can bring advantages to plants under cold environments, because warmer flowers speed the development of floral organs (Whitney et al. 2011Whitney HM, Bennet KMV, Dorling M, et al. 2011. Why so many petals have conical epidermal cells? Annals of Botany 108: 609-616. ; Koski & Galloway 2021Koski MH, Galloway LF. 2021. Geographic variation in floral color and reflectance correlates with temperature and colonization history. Frontiers in Plant Science 11: 991. doi: 10.3389/fpls.2020.00991
https://doi.org/10.3389/fpls.2020.00991...
), and in warm environments lighter colors dissipate heat (Sullivan & Koski 2021Sullivan CN, Koski MH. 2021. The effects of climate change on floral anthocyanin polymorphisms. Proceedings of the Royal Society B 28: 20202693. doi:10.1098/rspb.2020.2693
https://doi.org/10.1098/rspb.2020.2693...
). Different color morphs also affect anther temperature (Mu et al. 2017Mu J, Yang Y, Luo Y, Su R, Niklas KJ. 2017. Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb. Ecology and Evolution 7: 2947-2955. ). Pollen is sensitive to temperature variations, so when flowers are too warm or too cold, there is loss of pollen viability (Mu et al. 2017Mu J, Yang Y, Luo Y, Su R, Niklas KJ. 2017. Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb. Ecology and Evolution 7: 2947-2955. ). In Campanulastrum americanum (Campanulaceae) temperature explains flower color better than pollinator assemblage (Koski & Galloway 2021Koski MH, Galloway LF. 2021. Geographic variation in floral color and reflectance correlates with temperature and colonization history. Frontiers in Plant Science 11: 991. doi: 10.3389/fpls.2020.00991
https://doi.org/10.3389/fpls.2020.00991...
).

Additionally, some pollinators, such as bees, can associate color difference with warmer flowers and preferentially forage on warmer artificial feeders (Dyer et al. 2006Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L. 2006. Bees associate warmth with floral color. Nature 442: 525. doi:10.1038/442525a
https://doi.org/10.1038/442525a...
). This makes for a pollination system in which heat is offered as a reward (Whitney et al. 2011Whitney HM, Bennet KMV, Dorling M, et al. 2011. Why so many petals have conical epidermal cells? Annals of Botany 108: 609-616. ). In three species of iris (Iridaceae), I. atrofusca (dark purple to brown), I. atropurpurea (dark purple to brown), and I. hermona (dark spotted inner petter and blue outer petal), pollinators do not get any nectar or pollen reward; instead, flowers warm up quicker than ambient temperature in the early morning, so that male bees, who sleep inside flowers, will start foraging earlier the next day (Sapir et al. 2006Sapir Y, Shmida A, Ne’eman G. 2006. Morning floral heat as a reward to the pollinators of the Oncocyclus irises. Oecologia 147: 53-59.). Ambient temperature could be acting as a selective pressure for flowers to converge to darker morphs in colder environments, and to lighter morphs in warmer environments. The literature on flower temperature is, however, biased towards the heating effect of flower color, with most studies being conducted on alpine or artic species (van der Kooi 2019van der Kooi CJ. 2019. The thermal ecology of flowers. Annals of Botany 124: 343-353. ).

Another influence of phenology on flower color ensues from synchronous flowering, that is, overlap between flowering species of a community (Wolowski et al. 2017Wolowski M, Carvalheiro LG, Freitas L. 2017. Influence of plant-pollinator interactions on the assembly of plant and hummingbird communities. Journal of Ecology 105: 332-344. ). Flowering together with other members of the same community can lead to convergence of colors because of joined attraction to pollinators (Wolowski et al. 2017Wolowski M, Carvalheiro LG, Freitas L. 2017. Influence of plant-pollinator interactions on the assembly of plant and hummingbird communities. Journal of Ecology 105: 332-344. ; Bergamo et al. 2020Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346. ). This particularly aids rare flowers that might not be numerous enough to attract pollinators alone (Bergamo et al. 2020Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346. ). There is some evidence of a convergence of flower color according to season. Initially spring flowers were thought to be predominantly white, based on a study done by Motten (1986Motten AF. 1986. Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecological Monographs 56: 21-42.) in North Carolina, USA. A posterior study showed that, instead, the corolla color of spring flowers in temperate deciduous forests are lighter than non-spring flowers, but not necessarily white (Hensel & Sargent 2012Hensel LE, Sargent RD. 2012. A phylogenetic analysis of trait convergence in the spring flora. Botany 90:557-564.). In the Brazilian Savanna, yellow flowers were abundant year around, but white flowers peaked in the dry season, and pink flowers in the wet season (Martins et al. 2021Martins AE, Camargo MGG, Morellato LPC. 2021. Flowering phenology and the influence of seasonality in flower conspicuousness for bees. Frontiers in Plant Science 11: 594538. doi: 10.3389/fpls.2020.594538
https://doi.org/10.3389/fpls.2020.594538...
). Indeed, in Itatiaia National Park (Brazil), community level fitness increased with synchronous flowering and color similarities, using visual systems of bees, flies and birds (Bergamo et al. 2020Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346. ). In Germany, however, flower color was studied across a year period, and there was no relationship between floral color and blooming time when considering the bee visual system; but there was a difference when considering human vision, which exemplifies the importance of using an ecologically relevant visual model to study flower coloration (Arnold et al. 2009Arnold SEL, Le Comber SC, Chittka L. 2009b. Flower color phenology in European grassland and woodland habitats, through the eyes of pollinators. Israel Journal of Plant Sciences 57: 211-230. b). Further research, emphasizing pollinator perspective and accessing different populations, is essential to reach a better understanding of the effects of seasonality on flower coloration.

Similar to flowering season, different environments exert different selective pressures for plant communities, so it is important to take locality under consideration when analyzing flower color patterns. Abiotic factors, such as temperature (discussed in the previous section), rainfall, and ambient light, can vary between environments. Warren & Mackenzie (2001Warren J, Mackenzie S. 2001. Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytologist 151:237-241.) found that in polymorphic flowers, none-white morphs performed better under drought conditions and white morphs performed better on well-watered conditions. Koski & Ashman (2016Koski MH, Ashman TL. 2016. Macroevolutionary patterns of ultraviolet floral pigmentation explained by geography and associated bioclimatic factors. The New Phytologist 211: 708-718. ) found that habitats with high UV-B irradiance were more likely to have UV-absorbing flowers. Abiotic conditions are, however understudied compared to biotic pressures on flower color (Darlymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ).

Biotic interactions may also affect flower color either to defend from antagonists or to better attract pollinators. Despite lack of studies relating antagonistic interactions and flower color, Boaventura et al. (2021Boaventura MG, Villamil N, Teixido AL, et al. 2021. Revisiting florivory: An integrative review and global patterns of a neglected interaction. doi: 10.1111/nph.17670
https://doi.org/10.1111/nph.17670...
) found that florivory is twice as high on tropical plants. This could suggest a tendency for less conspicuous flowers in the tropics. Indeed, a comparison of flower coloration between different latitudes in Australia showed that colors are more saturated, contrasting and diverse farther from the tropics (Dalrymple et al. 2015Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2015. Birds, butterflies and flowers in the tropics are not more colourful than those at higher latitudes. Global Ecology and Biogeography 24: 1424-1432. ).

Locality can influence pollinators in three ways. First, pollinators can have differential color preferences between habitats. Bumblebees usually have a UV-violet preference, but some populations have an additional red preference (Raine et al. 2006Raine NE, Ings TC, Dornhaus A, Saleh N, Chittka L. 2006. Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Advances in the Study of Behavior 36: 305-354.). Hence, plants can have local adaptations depending on pollinator’s preference. The mimetic orchid Disa ferruginea (Orchidaceae) is pollinated by a single species of butterfly. This orchid has two color morphs occurring in different mountains in South Africa (Newman et al. 2012Newman E, Anderson B, Johnson SD. 2012. Flower color adaptation in a mimetic orchid. Proceedings of the Royal Society B 279: 2309-2313. ). The red morph occurs when there are red rewarding flowers around, and butterflies show preference for red flowers, and the orange morph occurs when there are orange rewarding flowers and butterflies show orange preference (Newman et al. 2012Newman E, Anderson B, Johnson SD. 2012. Flower color adaptation in a mimetic orchid. Proceedings of the Royal Society B 279: 2309-2313. ).

Second, the abundance of different kinds of pollinators varies across habitats. Ellis et al. (2021Ellis AG, Anderson B, Kemp JE. 2021. Geographic mosaics of fly pollinators with divergent color preferences drive landscape-scale structuring of flower color in daisy communities. Frontiers in Plant Science 12: 617761. doi:10.3389/fpls.2021.617761
https://doi.org/10.3389/fpls.2021.617761...
) found that pollinator density predicted the distribution of white and orange daisies, with white daisies flowering where the dominant fly species had an innate preference for white flowers and orange daisies flowering where the dominant fly species had an innate preference for orange. Flower coloration in Australia (Dyer et al. 2012Dyer AG, Boyd-Gerny S, Mcloughlin S, Rosa MGP, Simonov V, Wong BBM. 2012. Parallel evolution of angiosperm color signals: Common evolutionary pressures linked to hymenopteran vision. Proceedings of the Royal Society B 279: 3606-3615. ) and Israel (Chittka & Menzel 1992Chittka L, Menzel R. 1992. The evolutionary adaptation of flower colors and the insect pollinators’ color vision. Journal of Comparative Physiology A 171: 171-181. ) seems to be shaped by Hymenoptera vision, while the abundance of red flowers in the tropics is often attributed to hummingbird pollination (Willmer 2011Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.). Red flowers from the New World, where birds are important pollinators, are more conspicuous to birds than red flowers from the Old World (Chen et al. 2020Chen Z, Niu Y, Liu C-Q, Sun H. 2020. Red flowers differ in shades between pollination systems and across continents. Annals of Botany 12: 837-848. ). Blue-purple flowers in the Arctic seem to be related to species richness of bumblebees showing a coevolution between flower color and pollinator species (Eidesen et al. 2017Eidesen PB, Little L, Müller E, Dickinson KJM, Lord JM. 2017. Plant-pollinator interactions affect colonization efficiency: Abundance of blue-purple flowers is correlated with species richness of bumblebees in the arctic. Biological Journal of the Linnean Society 121: 150-162. ). Likewise, New Zealand flora is mostly comprised of white flowers well suited for bee detection (Bischoff et al. 2013Bischoff M, Lord JM, Robertson AW, Dyer AG. 2013. Hymenopteran pollinators as agents of selection on flower color in the New Zealand mountains: Salient chromatic signals enhance flower discrimination. New Zealand Journal of Botany 51: 181-193. ). In Macquarie Island (Australia), where there are no birds and bee pollinators, flowers are predominantly cream-green and white colored, a circumstance that could be due to fly pollination, either by allowing migrants with these colors to persist or by flowers converging to these colors due to pollinator pressure (Shrestha et al. 2016Shrestha M, Lunau K, Dorin A, et al. 2016. Floral colors in a world without birds and bees: the plants of Macquarie Island. Plant Biology 18: 842-850.).

Convergence of flower coloration within communities can increase misidentification from pollinators, and with that, pollen loss between similar species (Coetzee et al. 2021Coetzee A, Seymour CL, Spottiswoode CN. 2021. Facilitation and competition shape a geographical mosaic of flower colour polymorphisms. Functional Ecology 00:1-11. ). The effect of color convergence depends on community structure. Competition would result in loss of fitness for the whole community (Bergamo et al. 2020Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346. ), but another possibility is that color similarities can cause a gain of fitness in communities through facilitation (Bergamo et al. 2020Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346. ). Under the facilitation scenario, flowers blooming together with the same coloration would attract more pollinators, creating a rewarding mimicry ring (Jamie 2017Jamie GA. 2017. Signals cues and the nature of mimicry. Proceedings of the Royal Society B 284: 20162080. doi:10.1098/rspb.2016.2080
https://doi.org/10.1098/rspb.2016.2080...
; Coetzee et al. 2021Coetzee A, Seymour CL, Spottiswoode CN. 2021. Facilitation and competition shape a geographical mosaic of flower colour polymorphisms. Functional Ecology 00:1-11. ). Turnera sidoides (Turneracea) occurs in two varieties in different locations, color closely resembling other abundant Malvacea species of the flowering region (Benitez-Vieyra et al. 2007Benitez-Vieyra S, de Ibarra NH, Wertlen AM, Cocucci AA. 2007. How to look like a mallow: Evidence of floral mimicry between Turneraceae and Malvaceae. Proceedings of the Royal Society B 274: 2239-2248. ). Additionally, reproductive success of one of the T. sidoides phenotypes increased when the model Malvacea species was more abundant (Benitez-Vieyra et al. 2007Benitez-Vieyra S, de Ibarra NH, Wertlen AM, Cocucci AA. 2007. How to look like a mallow: Evidence of floral mimicry between Turneraceae and Malvaceae. Proceedings of the Royal Society B 274: 2239-2248. ). Facilitation leads to flower color convergence, as shown in some communities. In South African Erica (Ericaceae) communities, birds vary in preference between sites. Visitation of less preferred Erica flower species increased when they were similar in color to preferred species by local birds (Coetzee et al. 2021Coetzee A, Seymour CL, Spottiswoode CN. 2021. Facilitation and competition shape a geographical mosaic of flower colour polymorphisms. Functional Ecology 00:1-11. ). Community flower abundancy was related to lower trait (including color) diversity in Brazil (Bergamo et al. 2020Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346. ). In Australia, flower communities with higher diversity tended to converge to less contrasting colors (Dalrymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ).

Higher altitude gradients are an interesting study system because they vary in biotic and abiotic factors such as ambient light, with higher altitudes having higher UV (Gray et al. 2018Gray M, Stansberry MJ, Lynn JS, Williams CF, White TE, Whitney KD. 2018. Consistent shifts in pollinator-relevant floral coloration along Rocky Mountain elevation gradients. Journal of ecology 106: 1910-1924.); and in pollinator assemblage (Shrestha et al. 2013Shrestha M, Dyer AG, Bhattarai P, Burd M. 2013. Flower color and phylogeny along an altitudinal gradient in the Himalayas of Nepal. Journal of Ecology 102: 126-135.). At first, a study in Norway (Arnold et al. 2009Arnold SEJ, Savolainen V, Chittka L. 2009a. Flower colors along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod-Plant Interactions 3: 27-43. a), with altitudes varying from 700-1600 m above sea level (a.s.l.), found no effect of altitude on flower color. The same data was re-evaluated latter and found within community convergence of flower colors in higher elevations (Bergamo et al. 2018Bergamo PJ, Telles FJ, Arnold SEJ, de Brito VLG. 2018. Flower colour within communities shifts from overdispersed to clustered along an alpine altitudinal gradient. Oecologia 188: 223-235. ). By contrast, in Nepal (900-4100 m a.s.l.), flowers found in higher altitudes show more diversity of colors than in lower ones (Shrestha et al. 2013Shrestha M, Dyer AG, Bhattarai P, Burd M. 2013. Flower color and phylogeny along an altitudinal gradient in the Himalayas of Nepal. Journal of Ecology 102: 126-135.). In Colorado (2,700-4,000 m a.s.l.), there was a decrease of short wavelength reflection and bee-blue species, along with an increase in saturation with higher elevations (Gray et al. 2018Gray M, Stansberry MJ, Lynn JS, Williams CF, White TE, Whitney KD. 2018. Consistent shifts in pollinator-relevant floral coloration along Rocky Mountain elevation gradients. Journal of ecology 106: 1910-1924.). The same study found a hump-shaped pattern for longer wavelengths and green receptor contrast throughout elevation gradients. In Japan and New Zealand (sites varying from 1500-1630 m to 2200-2850 m a.s.l.), there was an increase of the likelihood of bee-blue or UV-blue flowers occurring in higher altitudes. Finally, in Taiwan (sites varying from 0-900 m to 2800-3300 m a.s.l.), lower altitudes had more diversity in flower color than higher altitudes (Tai et al. 2020Tai K, Shrestha M, Dyer AG, Yang E, Wang C. 2020. Floral color diversity: How are signals shaped by elevational gradient on the tropical-subtropical mountainous island of Taiwan? Frontiers in Plant Science 11: 582784. ). Although metrics of diversity and altitudes varied between studies, overall four out of six studies found that flowers in higher altitudes were less diverse in color than in lower altitudes. Though many studies relate altitude patterns to pollination, it is possible that abiotic factors, though understudied, also play a crucial role (Dalrymple et al. 2020Dalrymple RL, Kemp DJ, Flores-Moreno H, et al. 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985. ). The studies mentioned are still not enough to identify a clear altitudinal pattern, and changes in color diversity could be due to other factors.

Global patterns

We have looked so far at mechanisms that might lead flowers to converge, and in this section, we will look at studies done around the world to see whether these mechanisms lead to an overabundance of certain colors categories (refer to section II.b for a discussion on limitations of using color categories) in flower communities around the world. We will first address studies using human vision, and then using bee vision.

A survey of the Plant Trait Database (www.try-db.org; Kattge et al. 2019Kattge J, Bönisch G, Díaz S, et al. 2019. TRY plant trait database - enhanced coverage and open access. Global Change Biology 26: 110-188.), conducted by Dyer et al. (2021Dyer AG, Jentsch A, Burd M, et al. 2021. Fragmentary blue: Resolving the rarity paradox in flower colors. Frontiers in Plant Science 11: 618203. doi: 10.3389/fpls.2020.618203
https://doi.org/10.3389/fpls.2020.618203...
), found that the majority of flower colors recorded were white and yellow (24 % and 20 % respectively). When considering only animal-pollinated species, most of the flowers remained white and yellow (35 % and 22 % respectively). Interestingly, when only considering abiotic pollinated plants, green (41 %) was the most abundant color, followed by white (20 %) and brown (20 %). This aligns with other studies in the Brazilian sandbank and seasonally dry forest (Machado & Lopes 2004Machado IC, Lopes AV. 2004. Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Annals of Botany 94: 365-376.), mountainous landscapes in central Europe (Dyer et al. 2021Dyer AG, Jentsch A, Burd M, et al. 2021. Fragmentary blue: Resolving the rarity paradox in flower colors. Frontiers in Plant Science 11: 618203. doi: 10.3389/fpls.2020.618203
https://doi.org/10.3389/fpls.2020.618203...
), and Taiwan (Tai et al. 2020Tai K, Shrestha M, Dyer AG, Yang E, Wang C. 2020. Floral color diversity: How are signals shaped by elevational gradient on the tropical-subtropical mountainous island of Taiwan? Frontiers in Plant Science 11: 582784. ). Other studies describe a different pattern. In the Brazilian savanna, the main flower color was white, followed by pink, and then yellow, but color category abundancy changed over seasons (Martins et al. 2021Martins AE, Camargo MGG, Morellato LPC. 2021. Flowering phenology and the influence of seasonality in flower conspicuousness for bees. Frontiers in Plant Science 11: 594538. doi: 10.3389/fpls.2020.594538
https://doi.org/10.3389/fpls.2020.594538...
). In British grasslands, yellow was the most common color followed by pink and white (Warren & Billington 2005Warren J, Billington T. 2005. Flower colour phenology in British mesotrophic grassland communities. Grass and Forage Science 60: 332-336.). In Macquarie Island (Australia), frequently blooming flowers are predominantly pale cream to dull green (Shrestha et al. 2016Shrestha M, Lunau K, Dorin A, et al. 2016. Floral colors in a world without birds and bees: the plants of Macquarie Island. Plant Biology 18: 842-850.), a category which is missing from other studies, where these flowers could likely be considered either yellow, green or white. Hence, even studies that did not find a white and yellow prevalence found a white or yellow prevalence in flower categories. When using human vision to categorize, then, flowers seem to converge towards white and yellow across habitats, and pink flowers are also common. This pattern must be considered with caution, because many places in the world remain unsampled.

White flowers are typically blue-green in a bee color space and yellow flowers are typically UV-green (Tai et al. 2020Tai K, Shrestha M, Dyer AG, Yang E, Wang C. 2020. Floral color diversity: How are signals shaped by elevational gradient on the tropical-subtropical mountainous island of Taiwan? Frontiers in Plant Science 11: 582784. ). Actually, studies using the flower hexagon have shown an overwhelming majority of bee blue-green flowers and a scarcity of purely UV reflecting flowers Chittka (1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ). Prevalence of blue-green flowers has been found in various environments such as the Rocky Mountains (Gray et al. 2018Gray M, Stansberry MJ, Lynn JS, Williams CF, White TE, Whitney KD. 2018. Consistent shifts in pollinator-relevant floral coloration along Rocky Mountain elevation gradients. Journal of ecology 106: 1910-1924.), Brazilian Savanna (Martins et al. 2021Martins AE, Camargo MGG, Morellato LPC. 2021. Flowering phenology and the influence of seasonality in flower conspicuousness for bees. Frontiers in Plant Science 11: 594538. doi: 10.3389/fpls.2020.594538
https://doi.org/10.3389/fpls.2020.594538...
), Japan and New Zealand (Ishii et al. 2019Ishii HS, Kubota MX, Tsujimoto SG, Kudo G. 2019. Association between community assemblage of flower colours and pollinator fauna: a comparison between Japanese and New Zealand alpine plant communities. Annals of Botany 123: 533-541.); Taiwan (Tai et al. 2020Tai K, Shrestha M, Dyer AG, Yang E, Wang C. 2020. Floral color diversity: How are signals shaped by elevational gradient on the tropical-subtropical mountainous island of Taiwan? Frontiers in Plant Science 11: 582784. ); Macquarie Island (Shrestha et al. 2016Shrestha M, Lunau K, Dorin A, et al. 2016. Floral colors in a world without birds and bees: the plants of Macquarie Island. Plant Biology 18: 842-850.); Australia, Nepal and Israel (Shrestha et al. 2019bShrestha M, Dyer AG, Garcia JE, Burd M. 2019b. Floral color structure in two Australian herbaceous communities: It depends on who is looking. Annals of Botany 124: 221-232.). The second most abundant color varies among studies. This prevalence of blue-green color could be due to bee’s innate preference for blue-reflecting flowers, coupled with the easily detectability of green-reflecting flowers by green-contrast (Dyer et al. 2021Dyer AG, Jentsch A, Burd M, et al. 2021. Fragmentary blue: Resolving the rarity paradox in flower colors. Frontiers in Plant Science 11: 618203. doi: 10.3389/fpls.2020.618203
https://doi.org/10.3389/fpls.2020.618203...
).

When looking for patterns of convergence other than using color categories, results widely differ between studies. Chittka (1997Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127. ) has shown that the color distribution of flowers in a German grassland was found not to differ from chance, but in the Brazilian rainforest, flowers seemed convergent towards bee-blue. Gumbert et al. (1999Gumbert A, Kunze J, Chittka L. 1999. Floral color diversity in plant communities, bee color space and a null model. Proceedings of the Royal Society B 266: 1711-1716. ) analyzed five different habitats within Germany for trends in flower color. When considering common flowers only, they did not find any color to prevail; but when rare flowers were included, results varied across communities studied, with two showing divergent distribution, another showing convergent distribution and two finding random distribution (Gumbert et al. 1999Gumbert A, Kunze J, Chittka L. 1999. Floral color diversity in plant communities, bee color space and a null model. Proceedings of the Royal Society B 266: 1711-1716. ). Subalpine communities in Canada show evidence for divergent evolution of floral color (McEwen & Vamosi 2010McEwen JR, Vamosi JC. 2010. Floral color versus phylogeny in structuring subalpine flowering communities. Proceedings of the Royal Society B 277: 2957-2965. ). Daisy communities in South Africa showed evidence for convergent evolution in flower coloration (Kemp et al. 2019Kemp JE, Bergh NG, Soares M, Ellis AG. 2019. Dominant pollinators drive non-random community assembly and shared flower color patterns in daisy communities. Annals of Botany 123: 277-288. ). Shrestha et al. (2019Shrestha M, Dyer AG, Garcia JE, Burd M. 2019b. Floral color structure in two Australian herbaceous communities: It depends on who is looking. Annals of Botany 124: 221-232.b) analyzed flower communities in the perspective of different species of bees in the state of Victoria (Australia) and found that flower color structure varied according to the visual system used, some showing convergence, others divergence, but most showing a random distribution of flower coloration. These results highlight the importance of using the visual system of local pollinators or antagonists for analyzing patterns.

Using color categories, most flowers worldwide seem to follow a pattern of white and yellow flowers according to human vision and blue-green flowers according to bee vision. It is also important to note that there is publication bias towards studies that find differences between habitats which could be influencing this pattern. Patterns of convergence independent of flower categories depend on the habitat, and can vary relative to the visual system used to analyze these patterns. Even though most species of bees have similar visual systems (Peitsch et al. 1992Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based color vision. Journal of Comparative Physiology A 170: 23-40.), Shrestha et al. (2019Shrestha M, Dyer AG, Garcia JE, Burd M. 2019b. Floral color structure in two Australian herbaceous communities: It depends on who is looking. Annals of Botany 124: 221-232.b) showed that demonstrating color divergence or convergence of the same set of flowers is possible when utilizing different bee species as models. We encourage future work to take this matter into consideration, preferentially adopting species which naturally occur in the studied environment, better to understand biogeographic patterning of flower color. Here we only addressed studies using human and bee perspectives, partly because studies using other pollinators are relatively scarce and also because the bee-hexagon model can provide clear color categories (Chittka 1992Chittka L. 1992. The colour hexagon: A chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. Journal of Comparative Physiology 170: 533-543. ) and such models are not available for most pollinators. Greater appreciation of other visual systems is important so that similar analyses can be conducted using perspectives of other pollinators and herbivores.

Summary and prospects

Research on flower coloration has increased in the past decades, but there are still many topics to be studied. So far, inquiries into this topic have focused on two areas: ecology and evolution, and biochemistry of pigments. Most ecological research has been focused on pollinator pressures, specifically on bee pollination. Biochemical research has focused mainly on anthocyanin biosynthesis.

The biochemistry of flower coloration is determined by the synergy of pigments, pH and cellular structure, and is influenced by environment. Flower pigments are selected via a balance between pollinator attraction, defense against herbivores and resistance to environmental factors. Regarding mechanisms of flower coloration, the impact of iridescence, fluorescence and polarization regarding communication with pollinators and antagonists still remains to be explored.

The study of biochemical pathways which lead to flower coloration, particularly betalains and carotenoids, and what genes are associated with them would help determine how frequently new colors evolve within different clades. New colorations can be fixed by selective pressure or lack thereof, and the effect of random and neutral processes on coloration is still in its infancy and has much space to grow. It is important to consider phylogenetic history when interpreting flower coloration data. A global analysis or metanalyses of phylogenetic signal of flower color is still lacking. Quantifying coloration on a global level can be difficult because coloration varies according to the receiver, and there are few species of which there is enough information of their visual systems to make robust analyses. Using purely physical data to analyze coloration often does not translate into realistic models. Since most pollinators see UV light, it can be costly to purchase equipment proper to study flower color, especially where government investment in science is lacking, so collaboration among research groups is recommended to help overcome the impeding costs of this kind of research. A good example is the Flower Reflectance Database (www.reflectance.co.uk) that provides reflectance data on many different flowers in an accessible way (Arnold et al. 2010Arnold SEJ, Faruq S, Savolainen V, McOwan PW, Chittka L. 2010. FReD: The Floral Reflectance Database - A web portal for analyses of flower colour. PLoS ONE 5: e14287. doi:10.1371/journal.pone.0014287
https://doi.org/10.1371/journal.pone.001...
). The good news is that methods for analyzing coloration using animal perspective are becoming more refined and widespread.

Biochemical studies of flower pigments can also help to understand how flower color change evolved. In particular, the degradation of anthocyanins by sunlight could be a key precursor of flower color change. Likewise, studying the cost of maintaining color changed flowers would help explain why flower color change is not more common. Finding a model that only presents color-changed flowers under certain environmental conditions would greatly assist in this matter.

There are many pressures in each habitat that will make for flower color patterning. Most studies on biotic factors are about pollination; among pollinators and regarding flower color, bees are the most and beetles are the least studied. An interesting abiotic factor to consider would be the impact of temperature on blooming of polymorphic flowers. This is particularly intriguing because, aside from providing heat for pollinators as a reward, overheating of flowers could damage pollen and impact male fitness of flowers. Climate change makes it pressing to better understand how color impacts temperature of flowers and how temperature affects color in flowers. Ambient light and background contrast in flower coloration are promising topics, especially coupled with the sensory drive hypothesis. An interesting way to study this topic would be to compare flower colors between the canopy and understory of forests, where light variation (blue sky and forest shade) and background variations (green leaves in the canopy and leaf litter in the understory) occur. Another promising model system would be to analyze patterns of flower coloration on deciduous environments, comparing flower colors of forests which lose their leaves in winter against those which lose leaves in summer. This model could also assist to understand the trade-off between conspicuity and resistance to extreme temperature.

Overall patterns of flower coloration across different habitats remain to be studied in many biomes and using pollinators other than bees as a visual model. Current studies show a prevalence of white and yellow flowers according to human vision and blue-green flowers according to bee vision. A coordinated studied (standardizing environmental variables such as biome, altitude, latitude), with replicable methodology around the world is still lacking and would add to our comprehension of the evolution of flower color. Studying how pollinators preference can change across seasons could also aid understanding the global pattern of flower coloration. Use of eavesdropper perspective on flower coloration is rare and could foster interesting findings in plant biology. Herbivores and other antagonists can also employ flower coloration to identify food sources. Several interesting questions can come from bringing herbivores to the spotlight of flower color evolution. How does the presence of flowers influence egg-laying in herbivore insects (such as Lepidoptera)? Are blooming plants more parasitized (e.g. have more galls) than non-blooming plants? Are plants with flowers of certain color more damaged by herbivores (or florivores) from a specific group (ie. grasshoppers prefer to eat plants with blue flowers)?

Acknowledgments

This study was financed in part by the Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior - Brasil CAPES (Finance Codes 001 and 043/2012). A M.Sc. Scholarships was granted to M.F.E., and a Researcher Scholarship was granted to D. M. A. P., all by the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico - Brasil CNPq. We also thank L. M. Versieux and F. M. Gawryszewski for their valuable insights, and G. W. Erickson, E. Erickson, R. Erickson, D. J. A. Silva, and S. C. Schirmer for discussions and corrections.

References

  • Arikawa K. 2017. The eyes and vision of butterflies. The Journal of Physiology 595: 5457-5464.
  • Armbruster WS. 2002. Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-color evolution in two genera. Journal of Evolutionary Biology 15: 468-486.
  • Arnold SEJ, Chittka L. 2012. Illumination preference, illumination constancy and color discrimination by bumblebees in an environment with patchy light. Journal of Experimental Biology 215: 2173-2180.
  • Arnold SEJ, Faruq S, Savolainen V, McOwan PW, Chittka L. 2010. FReD: The Floral Reflectance Database - A web portal for analyses of flower colour. PLoS ONE 5: e14287. doi:10.1371/journal.pone.0014287
    » https://doi.org/10.1371/journal.pone.0014287
  • Arnold SEJ, Savolainen V, Chittka L. 2009a. Flower colors along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod-Plant Interactions 3: 27-43.
  • Arnold SEL, Le Comber SC, Chittka L. 2009b. Flower color phenology in European grassland and woodland habitats, through the eyes of pollinators. Israel Journal of Plant Sciences 57: 211-230.
  • Aydin G. 2011. Plant phenology-related shifts in color preferences of Epicometis (tropinota) hirta (coleoptera: scarabaeidae: cetoniinae) adults - key to effective population monitoring and suppression. Florida Entomologist 94: 832-838.
  • Benard J, Stach S, Giufa M. 2006. Categorization of visual stimuli in the honeybee Apis mellifera Animal Cognition 9: 257-270.
  • Benitez-Vieyra S, de Ibarra NH, Wertlen AM, Cocucci AA. 2007. How to look like a mallow: Evidence of floral mimicry between Turneraceae and Malvaceae. Proceedings of the Royal Society B 274: 2239-2248.
  • Bergamo PJ, Streher NS, Wolowski M, Sazima M. 2020. Pollinator-mediated facilitation is associated with floral abundance, trait similarity and enhanced community-level fitness. Journal of Ecology 108: 1334-1346.
  • Bergamo PJ, Telles FJ, Arnold SEJ, de Brito VLG. 2018. Flower colour within communities shifts from overdispersed to clustered along an alpine altitudinal gradient. Oecologia 188: 223-235.
  • Biesmeijer JC, Giurfa M, Koedam D, Potts SG, Joel DM, Dafni A. 2005. Convergent evolution: Floral guides, stingless bee nest entrances, and insectivorous pitchers. Naturwissenschaften 92: 444-450.
  • Binkenstein J, Schaefer HM. 2015. Flower colors in temperate forest and grassland habitats: A comparative study. Arthropod-Plant Interactions 9: 289-299.
  • Bischoff M, Lord JM, Robertson AW, Dyer AG. 2013. Hymenopteran pollinators as agents of selection on flower color in the New Zealand mountains: Salient chromatic signals enhance flower discrimination. New Zealand Journal of Botany 51: 181-193.
  • Boaventura MG, Villamil N, Teixido AL, et al 2021. Revisiting florivory: An integrative review and global patterns of a neglected interaction. doi: 10.1111/nph.17670
    » https://doi.org/10.1111/nph.17670
  • Bowmaker JK. 1981. Visual pigments and color vision in man and monkeys. Journal of the Royal Society of Medicine 74: 348-356.
  • Briscoe AD, Chittka L. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471-510.
  • Brito VLG, Weynans K, Sazima M, Lunau K. 2015. Trees as huge flowers and flowers as oversized floral guides: The role of floral color change and retention of old flowers in Tibouchina pulchra Frontiers in Plant Science 6: 362. doi:10.3389/fpls.2015.00362
    » https://doi.org/10.3389/fpls.2015.00362
  • Bukovac Z, Shrestha M, Garcia JE, Burd M, Dorin A, Dyer AG. 2017. Why background color matters to bees and flowers. Journal of Comparative Physiology A 203: 369-380.
  • Burd M, Stayton T, Shrestha M, Dyer AG. 2014. Distinctive convergence in Australian floral colors seen through the eyes of Australian birds. Proceedings of the Royal Society B 281: 20132862. doi:10.1098/rspb.2013.2862
    » https://doi.org/10.1098/rspb.2013.2862
  • Burger J, Edwards GE. 1996. Photosynthetic efficiency, and photodamage by UV and visible radiation, in red versus green leaf coleus varieties. Plant and Cell Physiology 37: 395-399.
  • Chalker-Scott L. 1999. Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70: 1-9.
  • Chen Z, Niu Y, Liu C-Q, Sun H. 2020. Red flowers differ in shades between pollination systems and across continents. Annals of Botany 12: 837-848.
  • Chittka L, Faruq S, Skorupski P, Werner A. 2014. Color constancy in insects. Journal of Comparative Physiology A 200: 435-448.
  • Chittka L, Menzel R. 1992. The evolutionary adaptation of flower colors and the insect pollinators’ color vision. Journal of Comparative Physiology A 171: 171-181.
  • Chittka L, Shmida A, Troje N, Menzel R. 1994. Ultraviolet as a component of flower reflections, and the color perception of hymenoptera. Vision Research 34: 1489-1508.
  • Chittka L, Thomson JD, Waser NM. 1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86: 361-377.
  • Chittka L. 1992. The colour hexagon: A chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. Journal of Comparative Physiology 170: 533-543.
  • Chittka L. 1996. Does bee color vision predate the evolution of flower color? Naturwissenschaften 83: 136-138.
  • Chittka L. 1997. Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded-why? Israel Journal of Plant Sciences 45: 115-127.
  • Chittka L. 1999. Bees, white flowers, and the color hexagon - A reassessment? No, not yet. Comments on the contribution by Vorobyev et al Naturwissenschaften 86: 595-597.
  • Coetzee A, Seymour CL, Spottiswoode CN. 2021. Facilitation and competition shape a geographical mosaic of flower colour polymorphisms. Functional Ecology 00:1-11.
  • Cuthill IC, Allen WL, Arbuckle K, et al 2017. The biology of color. Science 357: eaan0221. doi:10.1126/science.aan0221
    » https://doi.org/10.1126/science.aan0221
  • Dalrymple RL, Kemp DJ, Flores-Moreno H, et al 2015. Birds, butterflies and flowers in the tropics are not more colourful than those at higher latitudes. Global Ecology and Biogeography 24: 1424-1432.
  • Dalrymple RL, Kemp DJ, Flores-Moreno H, et al 2020. Macroecological patterns in flower colour are shaped by both biotic and abiotic factors. New Phytologist 228: 1972-1985.
  • de Camargo MGG, Lunau K, Batalha MA, Brings S, de Brito VLG, Morellato LPC. 2019. How flower color signals allure bees and hummingbirds: A community-level test of the bee avoidance hypothesis. New Phytologist 222: 1112-1122.
  • de Ibarra NH, Langridge KV, Vorobyev M. 2015. More than colour attraction: Behavioural functions of flower patterns Current Opinion in Insect Science 12: 64-70.
  • de Melo BT, Mota T, Schlindwein C, Antonini Y, Oliveira R. 2018. Floral color change in Byrsonima variabilis (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees. Science of Nature 105: 46. doi:10.1007/s00114-018-1572-y
    » https://doi.org/10.1007/s00114-018-1572-y
  • Dellinger AS. 2020. Pollination syndromes in the 21st century: Where do we stand and where may we go? New Phytologist 228: 1193-1213.
  • Domingos-Melo A, Brito VLG, Sérsic A, Cocucci AA, Lunau K, Machado IC. 2021. Shining bright in the dusk: How do bat-pollinated flowers reflect light? Ecology 102: e03416. doi: doi.org/10.1002/ecy.3416
    » https://doi.org/doi.org/10.1002/ecy.3416
  • Dyer AG, Boyd-Gerny S, Mcloughlin S, Rosa MGP, Simonov V, Wong BBM. 2012. Parallel evolution of angiosperm color signals: Common evolutionary pressures linked to hymenopteran vision. Proceedings of the Royal Society B 279: 3606-3615.
  • Dyer AG, Jentsch A, Burd M, et al 2021. Fragmentary blue: Resolving the rarity paradox in flower colors. Frontiers in Plant Science 11: 618203. doi: 10.3389/fpls.2020.618203
    » https://doi.org/10.3389/fpls.2020.618203
  • Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L. 2006. Bees associate warmth with floral color. Nature 442: 525. doi:10.1038/442525a
    » https://doi.org/10.1038/442525a
  • Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L. 2007. Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower color. Arthropod-Plant Interactions 1: 45-55.
  • Dyer AG. 1998. The color of flowers in spectrally variable illumination and insect pollinator vision. Journal of Comparative Physiology A 183: 203-212.
  • Dyer AG. 2012. The mysterious cognitive abilities of bees: Why models of visual processing need to consider experience and individual differences in animal performance. Journal of Experimental Biology 215: 387-95.
  • Eidesen PB, Little L, Müller E, Dickinson KJM, Lord JM. 2017. Plant-pollinator interactions affect colonization efficiency: Abundance of blue-purple flowers is correlated with species richness of bumblebees in the arctic. Biological Journal of the Linnean Society 121: 150-162.
  • Ellis AG, Anderson B, Kemp JE. 2021. Geographic mosaics of fly pollinators with divergent color preferences drive landscape-scale structuring of flower color in daisy communities. Frontiers in Plant Science 12: 617761. doi:10.3389/fpls.2021.617761
    » https://doi.org/10.3389/fpls.2021.617761
  • Endler JA. 1992. Signals, signal conditions, and the direction of evolution. American Naturalist 139: 125-153.
  • Endler JA. 1993. The color of light in forests and its implications. Ecological Monographs 63: 1-27.
  • Eugster CH, Märki‐Fischer E. 1991. The chemistry of rose pigments. Angewandte Chemie 30: 654-672.
  • Farzad M, Griesbach R, Weiss MR. 2002. Floral color change in Viola cornuta L. (Violaceae): A model system to study regulation of anthocyanin production. Plant Science 162: 225-231.
  • Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35: 375-403.
  • Finnell LM, Koski MH. 2021. A test of Sensory Drive in plant-pollinator interactions: Heterogeneity in the signalling environment shapes pollinator preference for a floral visual signal. New Phytologist. doi:10.1111/nph.17631
    » https://doi.org/10.1111/nph.17631
  • Fleming TH, Geiselman C, Kress WJ. 2009. The evolution of bat pollination: a phylogenetic perspective. Annals of Botany 104: 1017-1043.
  • Forrest J, Thomson JD. 2009. Background complexity affects color preference in bumblebees. Naturwissenschaften 96: 921-925.
  • Foster DH. 2011. Color constancy. Vision Reserach 51: 674-700.
  • Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Saito N, Iida S. 2000. Color-enhancing protein in blue petals. Nature 407: 581-582.
  • Garcia JE, Hung YS, Greentree AD, Rosa MGP, Endler JA, Dyer AG. 2017. Improved color constancy in honey bees enabled by parallel visual projections from dorsal ocelli. PNAS 114: 7713-7718.
  • Garcia JE, Phillips RD, Peter CI, Dyer AG. 2020. Changing how biologists view flowers-color as a perception not a trait. Frontiers in Plant Science 11: 1775. doi:10.3389/fpls.2020.601700
    » https://doi.org/10.3389/fpls.2020.601700
  • Gawryszewski FM. 2018. Color vision models: Some simulations, a general n-dimensional model, and the colorvision R package. International Journal of Business Innovation and Research 8: 8159-8170.
  • Giurfa M, Vorobyev M, Kevan P, Menzel R. 1996. Detection of coloured stimuli by honeybees: Minimum visual angles and receptor specific contrasts. Journal of Comparative Physiology A 178: 699-709.
  • Glover BJ, Martin C. 1998. The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus Heredity 80: 778-784.
  • Gómez JM, Perfectti F, Lorite J. 2015. The role of pollinators in floral diversification in a clade of generalist flowers. Evolution 69: 863-878.
  • Gould KS. 2004. Nature’s Swiss army knife: The diverse protective roles of anthocyanins in leaves. Journal of Biomedicine and Biotechnology 2004: 314-320.
  • Gray M, Stansberry MJ, Lynn JS, Williams CF, White TE, Whitney KD. 2018. Consistent shifts in pollinator-relevant floral coloration along Rocky Mountain elevation gradients. Journal of ecology 106: 1910-1924.
  • Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57: 761-780.
  • Gumbert A, Kunze J, Chittka L. 1999. Floral color diversity in plant communities, bee color space and a null model. Proceedings of the Royal Society B 266: 1711-1716.
  • Gumbert A. 2000. Color choices by bumble bees (Bombus terrestris): Innate preferences and generalization after learning. Behavioral Ecology and Sociobiology 48: 36-43.
  • Guzmán B, Gómez JM, Vargas P. 2017. Is floral morphology a good predictor of floral visitors to Antirrhineae (snapdragons and relatives)? Plant Biology 19: 515-524.
  • Hensel LE, Sargent RD. 2012. A phylogenetic analysis of trait convergence in the spring flora. Botany 90:557-564.
  • Herrera G, Zagal JC, Diaz M, et al 2008. Spectral sensitivities of photoreceptors and their role in color discrimination in the green-backed firecrown hummingbird (Sephanoides sephaniodes). Journal of Comparative Physiology A 194: 785. doi:10.1007/s00359-008-0349-8
    » https://doi.org/10.1007/s00359-008-0349-8
  • Hodges SA, Derieg NJ. 2009. Adaptive radiations: from field to genomic studies. PNAS 1: 9947-9954.
  • Hua X, Bromham L. 2017. Darwinism for the genomic age: Connecting mutation to diversification. Frontiers in Genetics 8: 12. doi: 10.3389/fgene.2017.00012
    » https://doi.org/10.3389/fgene.2017.00012
  • Ida TY, Kudo G. 2003. Floral color change in weigela middendorffiana (caprifoliaceae): Reduction of geitonogamous pollination by bumble bees. Israel Journal of Plant Sciences 90: 1751-1757.
  • Ida TY, Kudo G. 2010. Modification of bumblebee behavior by floral color change and implications for pollen transfer in Weigela middendorffiana Evolutionary Ecology 24: 671-684.
  • Irwin RE, Brody AK. 2000. Consequences of nectar robbing for realized male function in a hummingbird-pollinated plant. Ecology 81: 2637-2643.
  • Irwin RE, Strauss SY, Storz S, Emerson A, Guibert G. 2003. The role of herbivores in the maintenance of a flower color polymorphism in wild radish. Ecology 84: 1733-1743.
  • Ishii HS, Kubota MX, Tsujimoto SG, Kudo G. 2019. Association between community assemblage of flower colours and pollinator fauna: a comparison between Japanese and New Zealand alpine plant communities. Annals of Botany 123: 533-541.
  • Ishii HS, Sakai S. 2001. Effects of display size and position on individual floral longevity in racemes of Narthecium asiaticum (Liliaceae). Functional Ecology 15: 396-405.
  • Jamie GA. 2017. Signals cues and the nature of mimicry. Proceedings of the Royal Society B 284: 20162080. doi:10.1098/rspb.2016.2080
    » https://doi.org/10.1098/rspb.2016.2080
  • Johnson ET, Berhow MA, Dowd PF. 2008. Colored and white sectors from star-patterned petunia flowers display differential resistance to corn earworm and cabbage looper larvae. Journal of Chemical Ecology 34: 757-765.
  • Kattge J, Bönisch G, Díaz S, et al 2019. TRY plant trait database - enhanced coverage and open access. Global Change Biology 26: 110-188.
  • Keasar T, Gerchman Y, Lev-Yadun S. 2016. A seven-year study of flower-color polymorphism in a Mediterranean annual plant. Basic and Applied Ecology 17: 741-750.
  • Kelber A, Osorio D. 2010. From spectral information to animal colour vision: Experiments and concepts. Proceedings of the royal society 277: 1617-1625.
  • Kelley LA, Kelley JL. 2014. Animal visual illusion and confusion: The importance of a perceptual perspective. Behavioral Ecology 25: 450-463.
  • Kemp DJ, Herberstein ME, Fleishman LJ, et al 2015. An integrative framework for the appraisal of coloration in nature. American Naturalist 185: 705-724.
  • Kemp JE, Bergh NG, Soares M, Ellis AG. 2019. Dominant pollinators drive non-random community assembly and shared flower color patterns in daisy communities. Annals of Botany 123: 277-288.
  • Kevan P, Giurfa M, Chittka L. 1996. Why are there so many and so few white flowers? Trends in Plant Science 1: 280-284.
  • Kevan PG. 1983. Floral colors through the insect eye: What they are and what they mean. In: Jones E, Little J. (eds.) The handbook of experimental pollination biology. Scientific and Academic Editions. pp. 3-30.
  • Kootstra A. 1994. Protection from UV-B-induced DNA damage by flavonoids. Plant Molecular Biology 26: 771-774.
  • Koski MH, Ashman TL. 2015. Floral pigmentation patterns provide an example of Gloger's rule in plants. Nature Plants 1: 14007. doi:10.1038/nplants.2014.7
    » https://doi.org/10.1038/nplants.2014.7
  • Koski MH, Ashman TL. 2016. Macroevolutionary patterns of ultraviolet floral pigmentation explained by geography and associated bioclimatic factors. The New Phytologist 211: 708-718.
  • Koski MH, Galloway LF. 2021. Geographic variation in floral color and reflectance correlates with temperature and colonization history. Frontiers in Plant Science 11: 991. doi: 10.3389/fpls.2020.00991
    » https://doi.org/10.3389/fpls.2020.00991
  • Koski MH. 2020. The role of sensory drive in floral evolution. New Phytologist 227: 1012-1024.
  • Kries K, Barros MAS, Duytschaever G, et al 2018. Color vision variation in leaf-nosed bats (Phyllostomidae): Links to cave roosting and dietary specialization. Molecular Ecology 27: 3627-3640.
  • Kudo G, Ishii HS, Hirabayashi Y, Ida TY. 2007. A test of the effect of floral color change on pollination effectiveness using artificial inflorescences visited by bumblebees. Oecologia 154: 119-128. doi:10.1007/s00442-007-0820-1
    » https://doi.org/10.1007/s00442-007-0820-1
  • Lev-Yadun S, Gould KS. 2007. What do red and yellow autumn leaves signal? The Botanical Review 73: 279-289.
  • Lev-Yadun S, Ne’eman G, Keasar T. 2018. Differences in flower colors between spiny and non-spiny Asteraceae species: A possible case of aposematism? Flora 239: 98-103.
  • Lev-Yadun S. 2011. Fearful symmetry in aposematic plants. Plant Signaling and Behavior 6:1739-1740.
  • Lippi MM, Giuliani C, Gonnelli T, Bini LM. 2011. Floral color changes in Boswellia sacra Flueck. (Burseraceae): A dialogue between plant and pollinator. Flora 206: 821-826.
  • Lotto RB, Chittka L. 2005. Seeing the light: Illumination as a contextual cue to color choice behavior in bumblebees. PNAS 102: 3852-3856.
  • Lunau K, Maier EJ. 1995. Innate color preferences of flower visitors. Journal of Comparative Physiology A 177: 1-19.
  • Lunau K, Papiorek S, Eltz T, Sazima M. 2011. Avoidance of achromatic colors by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214: 1607-1612.
  • Lunau K. 2005. Stamens and mimic stamens as components of floral colour patterns. Botanische Jahrbucher fur Systematik Pflanzengeschichte und Pflanzengeographie 127: 13-42.
  • Lunau K. 2014. Visual ecology of flies with particular reference to color vision and color preferences. Journal of Comparative Physiology A 200: 497-512.
  • Ma Q, Zhang W, (Jenny) Xiang Q-Y. 2017. Evolution and developmental genetics of floral display-A review of progress. Journal of Systematics and Evolution 55: 487-515.
  • Machado IC, Lopes AV. 2004. Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Annals of Botany 94: 365-376.
  • MacPhail VJ, Kevan PG, Fuss C. 2007. Effect of flower age on honey bee behaviour when rewards are kept constant. Journal of Apicultural Research 46: 293-294.
  • Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD. 2013. pavo: An R Package for the analysis, visualization and organization of spectral data. Methods in Ecology and Evolution 4:609-613.
  • Maia R, Gruson H, Endler JA, White TE. 2019. pavo2: New tools for the spectral and spatial analysis of colour in r. Methods in Ecology and Evolution 10: 1097-1107.
  • Makino TT, Ohashi K. 2017. Honest signals to maintain a long-lasting relationship: Floral color change prevents plant-level avoidance by experienced pollinators. Functional Ecology 31: 831-837.
  • Martins AE, Camargo MGG, Morellato LPC. 2021. Flowering phenology and the influence of seasonality in flower conspicuousness for bees. Frontiers in Plant Science 11: 594538. doi: 10.3389/fpls.2020.594538
    » https://doi.org/10.3389/fpls.2020.594538
  • McEwen JR, Vamosi JC. 2010. Floral color versus phylogeny in structuring subalpine flowering communities. Proceedings of the Royal Society B 277: 2957-2965.
  • Momose K, Yumoto T, Nagamitsu T, et al 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. American Journal of Botany 85: 1477-1501.
  • Mori M, Yoshida K, Ishigaki Y, et al 2005. UV-B protective effect of a polyacylated anthocyanin, HBA, in flower petals of the blue morning glory, Ipomoea tricolor cv. Heavenly Blue. Bioorganic and Medicinal Chemistry 13: 2015-2020.
  • Motten AF. 1986. Pollination ecology of the spring wildflower community of a temperate deciduous forest. Ecological Monographs 56: 21-42.
  • Mu J, Li G, Sun S. 2010. Petal color, flower temperature, and behavior in an alpine annual herb, Gentiana leucomelaena (Gentianaceae). Arctic, Antarctic, and Alpine Research 42: 219-226.
  • Mu J, Yang Y, Luo Y, Su R, Niklas KJ. 2017. Pollinator preference and pollen viability mediated by flower color synergistically determine seed set in an Alpine annual herb. Ecology and Evolution 7: 2947-2955.
  • Muchhala N, Johnsen S, Smith SD. 2014. Competition for hummingbird pollination shapes flower color variation in Andean Solanaceae. Evolution 68: 2275-2286.
  • Müller B, Gloann M, Peichl L, Knop GC, Hagemann C, Ammermüller J. 2009. Bat eyes have ultraviolet-sensitive cone photoreceptors. PLoS ONE 7: e6390. doi:10.1371/journal.pone.0006390
    » https://doi.org/10.1371/journal.pone.0006390
  • Newman E, Anderson B, Johnson SD. 2012. Flower color adaptation in a mimetic orchid. Proceedings of the Royal Society B 279: 2309-2313.
  • Ng J, Smith SD. 2016. Widespread flower color convergence in Solanaceae via alternate biochemical pathways. New Phytologist 209: 407-417.
  • Niu Y, Sun H, Stevens M. 2018. Plant Camouflage: ecology, evolution, and implications. Trends in Ecology and Evolution 33: 608-618.
  • Oberrath R, Böhning-Gaese K. 1999. Floral color change and the attraction of insect pollinators in lungwort (Pulmonaria collina). Oecologia 121: 383-391.
  • Ohashi K, Makino TT, Arikawa K. 2015. Floral color change in the eyes of pollinators: Testing possible constraints and correlated evolution. Functional Ecology 29: 1144-1155.
  • Ollerton J, Winfree R, Tarrant S. 2011. How many flowering plants are pollinated by animals? Oikos 120: 321-326.
  • Olsson P, Lind O, Kelber A. 2018. Chromatic and achromatic vision: Parameter choice and limitations for reliable model predictions. Behavioral Ecology 29: 273-282.
  • Osorio D, Vorobyev M. 1996. Colour Vision as an Adaptation to Frugivory in Primates. Proceeding of the Royal Society B 263: 593-599.
  • Papiorek S, Junker RR, Alves-dos-Santos I, et al 2016. Bees, birds and yellow flowers: Pollinator-dependent convergent evolution of UV patterns. Plant Biology 18: 46-55.
  • Papiorek S, Rohde K, Lunau K. 2013. Bees’ subtle color preferences: How bees respond to small changes in pigment concentration. Naturwissenschaften 100: 633-643.
  • Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based color vision. Journal of Comparative Physiology A 170: 23-40.
  • Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I. 2007. Flavonoid oxidation in plants: From biochemical properties to physiological functions. Trends in Plant Science 12: 29-36.
  • Raine NE, Chittka L. 2008. The correlation of learning speed and natural foraging success in bumble-bees. Proceedings of the Royal Society B 275: 803-808.
  • Raine NE, Ings TC, Dornhaus A, Saleh N, Chittka L. 2006. Adaptation, genetic drift, pleiotropy, and history in the evolution of bee foraging behavior. Advances in the Study of Behavior 36: 305-354.
  • Raucher MD. 2008. Evolutionary Transitions in floral color. International Journal of Plant Sciences 169: 7-21.
  • Renoult JP, Kelber A, Schaefer HM. 2017. Color spaces in ecology and evolutionary biology. Biological Reviews 92: 292-315.
  • Reverté S, Retana J, Gómez JM, Bosch J. 2016. Pollinators show flower color preferences but flowers with similar colors do not attract similar pollinators. Annals of Botany 118: 249-257.
  • Roguz K, Gallagher MK, Senden E, et al 2020. All the colors of the rainbow: Diversification of flower color and intraspecific color variation in the genus Iris Frontiers in Plant Science 11: 569811. doi:3389/fpls.2020.569811
    » https://doi.org/3389/fpls.2020.569811
  • Ruxton GD, Schaefer HM. 2013. Game theory, multi-modal signalling and the evolution of communication. Behavioral Ecology and Sociobiology 67: 1417-1423.
  • Ruxton GD, Schaefer HM. 2016. Floral color change as a potential signal to pollinators. Current Opinion in Plant Biology 32: 96-100.
  • Sapir Y, Gallagher MK, Senden E. 2021. What maintains flower colour variation within populations? Trends in Ecology & Evolution 36: 507-519.
  • Sapir Y, Shmida A, Ne’eman G. 2006. Morning floral heat as a reward to the pollinators of the Oncocyclus irises. Oecologia 147: 53-59.
  • Schaefer HM, Rolshausen G. 2006. Plants on red alert: Do insects pay attention? BioEssays 28: 65-71.
  • Schaefer HM, Ruxton GD. 2009. Deception in plants: Mimicry or perceptual exploitation? Trends in Ecology and Evolution 24: 676-685.
  • Schaefer HM, Schaefer V, Levey DJ. 2004. How plant-animal interactions signal new insights in communication. Trends in Ecology and Evolution 19: 577-584.
  • Schemske DW, Horvitz CC. 1984. Variation among floral visitors in pollination ability: A precondition for mutualism specialization. Science 225: 519-521.
  • Schiestl FP, Johnson SD. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology and Evolution 28: 307-315.
  • Schiestl FP. 2017. Innate Receiver Bias: Its Role in the Ecology and Evolution of Plant-Animal Interactions. Annual Review of Ecology, Evolution, and Systematics 48: 585-603.
  • Servedio MR, Doorn GSV, Kopp M, Frame AM, Nosil P. 2011. Magic traits in speciation: ‘magic’ but not rare? Trends in Ecology and Evolution 26: 389-397.
  • Sharp JL, James J. 1979. Color preference of Vespula squamosa Environmental Entomology 8: 708-710.
  • Shrestha M, Burd M, Garcia JE, Dorin A, Dyer AG. 2019a. Color evolution within orchids depends on whether the pollinator is a bee or a fly. Plant Biology 21: 745-752.
  • Shrestha M, Dyer AG, Bhattarai P, Burd M. 2013. Flower color and phylogeny along an altitudinal gradient in the Himalayas of Nepal. Journal of Ecology 102: 126-135.
  • Shrestha M, Dyer AG, Garcia JE, Burd M. 2019b. Floral color structure in two Australian herbaceous communities: It depends on who is looking. Annals of Botany 124: 221-232.
  • Shrestha M, Lunau K, Dorin A, et al 2016. Floral colors in a world without birds and bees: the plants of Macquarie Island. Plant Biology 18: 842-850.
  • Shuttleworth A, Johnson SD. 2009. A key role for floral scent in a wasp-pollination system in Eucomis (Hyacinthaceae). Annals of Botany 103: 715-725.
  • Smith SDW, Ané C, Baum DA. 2008. The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution 62: 793-806.
  • Sobel JM, Streisfeld MA. 2013. Flower color as a model system for studies of plant evo-devo. Frontiers in Plant Science 4: 1-17.
  • Stace HM, Fripp YJ. 1977. Raciation in Epacris impressa II. Habitat differences and flowering times. Australian Journal of Botany 25: 315-323.
  • Stanton ML. 1987. Reproductive biology of petal color variants in wild populations of Raphanus sativus I. Pollinator response to color morphs. American Journal of Botany 74:178-187.
  • Stavenga DG, Leertouwer HL, Dudek B, van der Kooi CJ. 2021. Coloration of flowers by flavonoids and consequences of pH dependent absorption. Frontiers in Plant Science 11: 600124. doi: 10.3389/fpls.2020.600124
    » https://doi.org/10.3389/fpls.2020.600124
  • Stevens M, Stoddard MC, Higham JP. 2009. Studying primate color: Towards visual system-dependent methods. International Journal of Primatology 30: 893-917.
  • Stevens M. 2013. Sensory ecology, behavior & evolution. Oxford, Oxford University Press.
  • Stöckl AL, Kelber A. 2019. Fuelling on the wing: Sensory ecology of hawkmoth foraging. Journal of Comparative Physiology A 205: 399-413.
  • Stournaras K, Schaefer HM. 2017. Does flower and fruit conspicuousness affect plant fitness? Contrast, color coupling and the interplay of pollination and seed dispersal in two Vaccinium species. Evolutionary Ecology 31: 229-247.
  • Sullivan CN, Koski MH. 2021. The effects of climate change on floral anthocyanin polymorphisms. Proceedings of the Royal Society B 28: 20202693. doi:10.1098/rspb.2020.2693
    » https://doi.org/10.1098/rspb.2020.2693
  • Sun SG, Liao K, Xia J, Guo YH. 2005. Floral color change in Pedicularis monbeigiana (Orobanchaceae). Plant Systematics and Evolution 255: 77-85.
  • Tai K, Shrestha M, Dyer AG, Yang E, Wang C. 2020. Floral color diversity: How are signals shaped by elevational gradient on the tropical-subtropical mountainous island of Taiwan? Frontiers in Plant Science 11: 582784.
  • Teixido AL, Duarte MO, Ballego-Campos I, et al 2019. One for all and all for one: Retention of color-unchanged old flowers increases pollinator attraction in a hermaphroditic plant. Plant Biology 21: 167-175.
  • van den Berg CP, Troscianko J, Endler JA, Marshall NJ, Cheney KL. 2020. Quantitative Colour Pattern Analysis (QCPA): A comprehensive framework for the analysis of colour patterns in nature. Methods in Ecology and Evolution 11: 316-332.
  • van der Kooi CJ, Dyer AG, Kevan PG, Lunau K. 2019. Functional significance of the optical properties of flowers for visual signalling. Annals of Botany 123: 263-276.
  • van der Kooi CJ, Elzenga JTM, Staal M, Stavenga DG 2016. How to color a flower: On the optical principles of flower coloration. Proceedings of the Royal Society B 283: 20160429. doi:10.1098/rspb.2016.0429
    » https://doi.org/10.1098/rspb.2016.0429
  • van der Kooi CJ, Stavenga DG, Arikawa K, Belušič G, Kelber A. 2021. Evolution of insect color vision: From spectral sensitivity to visual ecology. Annual Review of Entomology 66: 435-461.
  • van der Kooi CJ, Wilts BD, Leertouwer HL, Staal M, Elzenga JTM, Stavenga DG. 2014. Iridescent flowers? Contribution of surface structures to optical signaling. New Phytologist 203: 667-673.
  • van der Kooi CJ. 2019. The thermal ecology of flowers. Annals of Botany 124: 343-353.
  • van Eck NJ, Waltman L. 2010. Software Survey: VOSviewer, a Computer Program for Bibliometric Mapping. Scientometrics: 84: 523-38.
  • Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R. 2001. Colour thresholds and receptor noise: Behaviour and physiology compared. Vision Research 41: 639-653.
  • Vorobyev M, Gumbert A, Kunze J, Giurfa M, Menzel R. 1997. Flowers through insect eyes. Israel Journal of Plant Sciences 45: 93-101.
  • Vorobyev M, Osorio D, Bennett AT, Marshall NJ, Cuthill IC. 1998. Tetrachromacy, oil droplets and bird plumage colours. Journal of Comparative Physiology A 183: 621-633.
  • Wang H, Talavera M, Min Y, Flaven E, Imbert E. 2016. Neutral processes contribute to patterns of spatial variation for flower color in the Mediterranean Iris lutescens (Iridaceae). Annals of Botany 117: 995-1007.
  • Warren J, Billington T. 2005. Flower colour phenology in British mesotrophic grassland communities. Grass and Forage Science 60: 332-336.
  • Warren J, Mackenzie S. 2001. Why are all colour combinations not equally represented as flower-colour polymorphisms? New Phytologist 151:237-241.
  • Waser NM. 1986. Flower constancy: Definition, cause, and measurement. The American Naturalist 127: 593-603.
  • Weber MG, Cacho NI, Phan MJQ, Disbrow C, Ramírez SR, Strauss SY. 2018. The evolution of floral signals in relation to range overlap in a clade of California Jewelflowers (Streptanthus s.l.). Evolution 72: 798-807.
  • Weiss MR, Papaj DR. 2003. Color learning in two behavioural contexts: How much can a butterfly keep in mind? Animal Behaviour 65: 425-434.
  • Weiss MR. 1995. Floral Color Change: A Widespread Functional Convergence. American Journal of Botany 82: 167-185.
  • Weiss MR. 1997. Innate colour preferences and flexible colour learning in the pipevine swallowtail. Animal Behavior 53: 1043-1052.
  • Whitney HM, Bennet KMV, Dorling M, et al 2011. Why so many petals have conical epidermal cells? Annals of Botany 108: 609-616.
  • Willmer P. 2011. Pollination and Floral Ecology. New Jersey, Princeton University Press.
  • Wolowski M, Carvalheiro LG, Freitas L. 2017. Influence of plant-pollinator interactions on the assembly of plant and hummingbird communities. Journal of Ecology 105: 332-344.
  • Yan J, Wang G, Sui Y, Wang M, Zhang L. 2016. Pollinator responses to floral color change, nectar, and scent promote reproductive fitness in Quisqualis indica (Combretaceae). Scientific Reports 6: 24408. doi:10.1038/srep24408
    » https://doi.org/10.1038/srep24408
  • Yoshida K, Toyama-Kato Y, Kameda K, Kondo T. 2003. Sepal color variation of Hydrangea macrophylla and vacuolar pH measured with a proton-selective microelectrode. Plant and Cell physiology 44: 262-268.

Publication Dates

  • Publication in this collection
    28 Oct 2022
  • Date of issue
    2022

History

  • Received
    01 Oct 2021
  • Accepted
    15 July 2022
Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br