Why Are So Many Bird Flowers Red?

Are bird-pollinated flowers red because bees - which might rob the flower of its nectar - cannot easily detect them, or might it be because of more subtle evolutionary trade-offs?

M ost bird-pollinated fl owers are both red and rich in nectar. The traditional explanation for this association is that, since red is inconspicuous to bees, it evolved to prevent bees from depleting the nectar of bird-pollinated fl owers without effecting pollination. But bees can see, and they actually visit red fl owers. So why are most bird-pollinated fl owers red? To help answer this question, we need to consider how the outcomes of foraging decisions are affected by the community in which individuals live, and by the foraging options of other individuals.

The Mystery
Plants face a trade-off between attracting pollinators and remaining hidden from fl ower parasites (such as nectar robbers and seed predators). Consequently, there is often strong selection pressure for highly specifi c communication channels that can advertise the presence of their fl owers to effective pollinators but not to other individuals. Many aspects of pollinator syndromes are best understood in these terms (Proctor et al. 1996). For example, fl owers that are pollinated by birds-bird fl owers-produce nectar at much higher rates than those pollinated by bees (Stiles 1981). If a bee is attracted to such a fl ower, it might sometimes remove nectar and pollen without providing an outcrossing service (i.e., bringing pollen from a different plant of the same species) to the fl ower. Therefore, bird-pollinated fl owers should advertise their presence to birds, but not to bees. Following this line of reasoning, Peter Raven (1972) suggested more than thirty years ago that bird-pollinated fl owers were predominantly red because 'red is the only color of the spectrum that is at once inconspicuous to most insects and also an excellent "signal" of a high caloric reward for birds'. Raven's interpretation of inconspicuousness was soon transformed into invisibility; it was assumed that bees did not visit red fl owers because they couldn't detect them (Proctor et al. 1996;Vogel 1996).
However, this interpretation no longer holds. Chittka and Waser (1997) have shown that red fl owers are not actually invisible to bees. Indeed, typical bird fl owers with no UV refl ectance, such as the scarlet gilia (Ipomopsis aggregata) and the scarlet monkeyfl ower (Mimulus cardinalis) (Figure 1), are routinely visited and exploited by different bee species (reviewed by Chittka and Waser 1997). Moreover, when bees are extremely abundant, they can drive birds away from red fl owers. Echium wildpretii, an endemic of the Canary Islands, presents an entomophylous ('insect-loving') and an ornithophyllous ('bird-loving') subspecies ( Figure 2) that differ in fl ower colour: E. wildpretii trichosiphon, endemic to La Palma Island, has entomophylous, pink fl owers, whereas E. wildpretii wildpretii, endemic to Tenerife Island, has ornithophyllous, red fl owers, pollinated by generalist native birds and insects. E. wildpretii wildpretii is pollinated predominantly by birds early in the season until introduced honeybees (Apis mellifera, which have increased enormously in number because of apiculture) deplete the nectar and displace nectar-feeding birds (Valido et al. 2002).
So if red fl owers are not invisible to bees, why are most bird-pollinated fl owers red? Perhaps birds are particularly apt at detecting red objects (Chittka and Waser 1997)? Again, this is not strictly true. Although all birds detect red objects and some birds do have their greatest spectral sensitivity and fi nest hue discrimination towards the long-wavelength (red) end of the spectrum (Stiles 1981), they can also respond to ultraviolet light, and there is no evidence that, for example, hummingbirds have greater spectral sensitivity or greater spectral discrimination ability in the red part of the spectrum (Goldsmith and Goldsmith 1979). Feeding experiments, where hummingbirds are given nectar in artifi cial fl owers of different colours, show no inherited colour preferences; hummingbirds have temporary preferences that can be modifi ed by conditioning (Proctor et al. 1996). So are there other clues as to how this mystery might be solved?

The Visual System of Bees
One clue might come from the visual system of bees. Humans perceive light with a wavelength above approximately 600 nm as red (Buser and Imbert 1968). Most bees have three types of colour receptors, with sensitivity peaks at 340, 430, and 540 nm (Chittka 1996), although a very few bee species have sensitivity peaks at substantially longer wavelengths. For the majority, however, provided that the light source is suffi ciently intense, red light (up to 650 nm) will stimulate the 540 nm receptor of bees (Chittka and Waser 1997). Bees will therefore perceive red objects. To discriminate red fl owers from their green background, bees must rely essentially on the difference between the intensity of the signal that fl ower and foliage generate on the bees' 'green' (540 nm) receptor (Giurfa et al. 1996). Therefore, depending on the relative intensity of the green and red sources, bees may or may not be able to discriminate between red fl owers and green foliage (Chittka and Waser 1997).
Because of the structure of their visual system, bees trained to feed at artifi cial red fl owers take longer to fi nd their goals than bees trained to feed at other-coloured fl owers (Spaethe et al. 2001). In a real environment, where red fl owers would be more camoufl aged against the different shades and intensities of the green foliage, the ability of bees to discriminate red fl owers should be further reduced.

Colour Vision and Niche Partition
The fact that bees require more time to fi nd red fl owers than other-coloured fl owers, together with some results from optimal-foraging theory, outlined here, could unlock the mystery and explain the association between red coloration and bird pollination in fl owers.
When different animals, either from the same or different species, are forced to share some resources, any degree of specialization tends to result in habitat selection (Rosenzweig 1981). In 1992, Possingham, developed a 'habitat selection' model that showed how two nectar-feeding pollinator species, which differed in their foraging effi ciency, would forage on two types of fl owers. Although an abstract model, we can use it to illustrate how birds might interact with bees at differentcoloured fl owers.
Consider a community that includes bees and birds, and red and blue fl owers. Let us assume that the fl owers differ only in their colour, that there are only two patches of fl owers (one of blue, the other of red fl owers), and that the density of fl owers is the same in both patches. (For a general analysis, with the same qualitative results, see Possingham 1992.) The question is: how many birds and bees should forage at the red and blue patches so that their intake of nectar is DOI: 10.1371/journal.pbio.0020350.g001 maximised? The expected intake rate is the average amount of nectar obtained per fl ower (or standing crop) divided by the time it takes to fi nd and exploit a fl ower. If the fl owers are the same distance apart and birds can detect red and blue fl owers equally well, then travel time is independent of fl ower colour. Under these circumstances, an ecological equilibrium, with birds exploiting red and blue fl owers equally, would indicate that the amount of nectar available from both fl ower colours was identical.
Now add a few bees to this community of birds, suffi ciently few that their intake of nectar is negligible. We know that the standing crop is the same at red and blue fl owers. However, we also know that bees require more time to fi nd red fl owers than blue ones (Spaethe et al. 2001), so their intake rate of nectar will be higher at blue fl owers, and they will all go to the blue patch.
If we continue to add bees one at a time to this community, then sooner or later, the number of bees will no longer be suffi ciently low for us to ignore their depleting effect on the nectar available. What will happen at that point? Will bees now start visiting red fl owers? Not yet. For a bee to visit the red patch, the difference in standing crop between red and blue fl owers would have to be large enough to compensate for the difference in detection time. Before that happens, some birds will shift to the red patch. Indeed, since birds require the same time to detect red or blue fl owers, some birds will move from the blue to the red patch as soon as bees start to noticeably reduce the nectar available from the blue fl owers.
What Possingham's model predicts, therefore, is that when the number of bees is large enough, all birds will forage at the red patch. Only when the difference in standing crop between red and blue fl owers is so large that it compensates for the reduced detectability of red fl owers, will bees start visiting the red patch.
To conclude, there will be an association between red fl owers and birds. Birds will exploit red fl owers, and bees blue fl owers. In addition, depending on the relative abundance of bees and birds (and of red and blue fl owers), either birds or bees, but never both simultaneously, can also exploit the other fl ower type (Figure 3). Possingham's model (1992) helps to explain the ecological association between fl ower colour and pollinator type, provided that both fl ower colours and pollinator types are present-but why did the red colouration of these fl owers evolve in the fi rst place? We believe that the model can also help explain the evolution of red coloration in bird-pollinated fl owers.

Niche Partition and the Evolution of Red Flowers
To understand the evolutionary process, consider a community where bees and birds are present, and where two fl ower species coexist. One fl ower type, the generalist fl ower, is blue and is effi ciently pollinated by bees and birds alike. The blue Rocky Mountain penstemon, Penstemon strictus, provides a good example (Castellanos et al. 2003). The other fl ower type, or bird fl ower, is yellow and is effi ciently pollinated by birds, but not by bees-the red beardlip penstemon P. barbatus provides an example of this type (Castellanos et al. 2003). If bee visits were costly for the ancestral bird fl owers, they would experience a selective pressure to become red. Bees could impose several costs on the ancestral bird fl owers; for example, the number of hummingbird visits may depend on the amount of nectar available in the fl owers.
Throughout evolutionary history, there will be variability and heritability in fl ower colour (as documented for Mimulus by Bradshaw et al. 1995). Since both bees and birds easily detect and effi ciently pollinate generalist blue fl owers, there is no particular reason to expect that their colour will evolve in one direction or another. Things are otherwise for bird fl owers, which are more effi ciently pollinated by birds. For simplicity, consider that, at any given time, this bird fl ower comes in only two shades of colour, one of them with a slightly longer wavelength (an orange morph). On an ecological timescale, yellow fl owers will be visited mainly by bees and orange fl owers mainly by birds. Orange fl owers, being more effi ciently pollinated by birds, will therefore have higher fi tness than yellow fl owers, and given enough time, there will be selection for bird fl owers to become orange. In the absence of other costs, mutant fl owers with higher wavelengths (i.e., becoming redder) can invade a population of yellow fl owers so long as bird fl owers continue to be visited by bees (unpublished data). So bird fl owers will continue to shift their colour until bees are completely excluded from the bird fl owers or until further shifts deteriorate detectability by birds.
This explanation for the evolution of red coloration in bird-pollinated fl owers differs from the one proposed by Raven (1972) in a key respect. In our view, the main point is not that bees fl y over red fl owers without seeing them; it is not even that they are unable to exploit red fl owers effi ciently in absolute terms. It is rather a question of relative effi ciency that makes bees avoid red fl owers when birds are depleting their nectar; it would work just as well if birds were colourblind and perceived red fl owers as badly as fl owers of other colours. Of course, Possingham's model (1992) is not incompatible with birds being more effi cient than bees at exploiting red fl owers, and the results would be strengthened if, as has been suggested (Raven 1972;Chittka and Waser 1997), birds are better at detecting red fl owers than blue ones.

Toward a Solution
Comparable problems can be found in other plant-pollinator systems. For example, when several species of bumblebees coexist, resource DOI: 10.1371/journal.pbio.0020350.g002 partitioning normally doesn't follow colour, but is dependent on different parameters: the corolla length of the plant and the proboscis length of the bee. Proboscis length affects the effi ciency with which fl owers of different depth are exploited (Inouye 1980); bumblebees with long proboscises preferentially exploit fl owers with deep corollas, while bumblebees with short proboscises exploit shallow fl owers (Heinrich 1976). But a bumblebee with a long proboscis can also exploit shallow fl owers, and, to some extent, a bumblebee with a short proboscis can exploit deep fl owers, if corollas are not too deep (although they will still leave some nectar behind). Indeed, when one bumblebee type is experimentally removed, the other one is seen to exploit both deep and shallow fl owers (Inouye 1978). The same, we believe, should happen with fl ower colour: the experimental removal of birds should lead to the systematic exploitation of red fl owers by bees, at least when corolla tube morphology does not prevent bees from accessing the nectar.
In fact, there is even no need to perform experimental bird removals, because plants provide us with a ready-made design: bees visit fl owers searching for both nectar and pollen, while most birds exploit only the nectar. Hence, bees should readily collect pollen at red bird fl owers. There are numerous examples of this, although in most cases they are indirectly documented. For example, solitary bees and syrphid and muscoid fl ies visit the red, hummingbirdpollinated fl owers of Ipomopsis aggregata to collect pollen when hummingbirds visits are frequent, while bumblebee (Bombus appositus) visits to collect nectar are only common when hummingbird visits are rare (Mayfi eld et al. 2001). Outside the native range of bird-pollinated plants, the same phenomenon can be observed: in Spanish gardens, the honeybee collects pollen from Aloe arborescens plants. Bees cannot access the nectar, concealed at the bottom of the corolla tube. This is opportunistically collected by birds such as the Sardinian warbler Sylvia melanocephala (unpublished data).
Another comparison of interest concerns beetle-pollinated fl owers, which in the Mediterranean region have open, bowl shapes and red coloration (Dafni et al. 1990). Amphicoma beetles are more effi cient pollinators of these fl owers than commonly occurring bees (Dafni et al. 1990), so the red coloration of these fl owers might help to keep other visitors (possibly bees and fl ies) at bay. Indeed, other bowl-shaped fl owers of different colours (such as yellow, white, and purple, e.g., in the genera Cistus and Helianthemum) are commonly visited by pollen-collecting bees and bumblebees. A particularly interesting test case is provided by the corn poppy Papaver rhoeas; in the eastern Mediterranean region, it is pollinated by beetles and does not refl ect in the UV (Dafni et al. 1990), while in central and western Europe it refl ects in the UV (Daumer 1958) and is pollinated by bees.
Although refi nements of Possingham's model, such as developing a prey-model version, or introducing stochasticity or several foraging constraints, might help us determine the extent to which we should expect resource partitioning along the colour dimension to take place, it is, in our view, far more pressing to determine the extent and conditions under which bees exploit red fl owers (i.e., through comparisons of pollen vs. nectar exploitation, bird exclusion experiments, etc.), the detection time of red fl owers against a natural background, and the effect of fl ower colour and size on fl ight mode in the fi eld. Only then will we be able to fully unravel the factors that solve this fascinating mystery.