Why Autumn leaves are red

It's autumn now in New England (or as the Americans call it, fall), and the leaves are turning beautiful shades of yellow and red. While cycling down a leafy avenue in Boston, I was struck by how perfectly the autumn foliage complemented the stately brownstone town houses—checking the property prices, an apartment in each of them in Boston's Back Bay area is typically priced upwards of $1.5 million, so I quickly abandoned my dream of moving into the neighborhood.

But what use, biologically speaking, is it for trees to produce such beautiful colors before they shed their leaves? Many plant physiologists will say that it is simply an effect of chlorophyll resorption by the plant. Chlorophyll is metabolically expensive, so plants will want to save on further investment by resorbing it before shedding their leaves. Yellow to orange colored carotenoid secondary pigments, normally present in leaves alongside chlorophyll, will be unmasked when chlorophyll is gone, exposing their yellow colors. That explains yellow leaves in fall, but what about red leaves? It turns out that red leaves get their color from anthocyanins, and these are produced and shunted into the leaves before they are shed, so they are not usually present. Hence there must be some explanation for why the plants make this additional investment.

Autumn leaves (Wikimedia).

One hypothesis, originally proposed by William Hamilton (of kin selection fame) and Sam Brown, but also independently by Marco Archetti, is that the red coloration acts as an 'honest signal' to aphids. Aphids are major herbivorous pests and can inflict potentially significant damage to a plant's health and hence reproductive fitness. Plants with red autumn leaves (not all temperate trees turn red, contrary to what we in the tropics think) tend to be correlated with high phenolic content. Phenolics are secondary metabolites that are commonly used by plants to deter herbivores. Therefore, red colors are a signal to deter aphids from settling and laying eggs on the trees before winter (eggs that would hatch come springtime), but this signal is no empty threat but also carries the force of anti-herbivory defenses behind it. This idea of honest signals originally came from economics, where a whole field of signaling theory has been built up.

Recently, however, this nice adaptationist story has come under criticism. You may have seen this review in PLoS Biology by Chitka and Doring that essentially says aphids (and insects in general) can't see red, so how could they perceive this signal? Insects with three color receptors (trichromatic) have maximal sensitivities at ultraviolet, blue-violet, and yellow. Aphids are trichromatic, and have pretty much the same maximal sensitivities. This is unlike human photoreceptors, which are maximally sensitive at blue, green, and red. So humans are able to see red, but unable to see ultraviolet like insects do. Does this deal a fatal blow to the 'too good to be true' story of Hamilton, Brown, and Archetti?

On Tuesday I had the privilege of attending a talk by Archetti himself. He's presently come to Harvard from Oxford, and was invited to present his work to the Cambridge Entomological Club at its monthly meeting. It turns out that he is acquainted with Chitka and Doring and soon after their review came out in PLoS, he went to see Doring with the argument that aphids actually can see red. His theoretical argument is that spectral sensitivities reflect sensitivities to monochromatic light (i.e. light at a single wavelength). So a monochromatic beam at say far red will be indistinguishable from another beam at near red or yellow to an insect. But the pigments in leaves do not have monochromatic reflectances - they reflect light across a band of wavelengths. If one plots out reflectance against wavelength for leaf pigments, they resemble step functions, instead of being narrow single-color bands. Overlaying the reflectance data for green leaves and red leaves against the sensitivity spectra of insect eyes, it shows that it is possible for them to distinguish between say green, yellow, and red.

That shows at least that it is possible for insects to distinguish between red and other colors despite not having a dedicated red photoreceptor. But do they actually do so in nature? Archetti then did a very simple experiment, painting petri dishes in various hues and setting them out in a field experimental station in England. He found that insects preferred to land in yellow dishes most of all (an unusual affinity that field entomologists have long known as a trick for luring insects into traps more effectively), followed by green, then least of all red. So they are able to distinguish between these colors, a trend that is supported even when corrected for the different brightnesses of these colors.

Archetti also examined the relative distribution of hues in autumn foliage in different regions, in the wild and in cultivation. It turns out that New England has the highest proportion of red/yellow foliage in autumn (ca. 70%), compared to an average for all temperate zones of about 15% though the reason for this disparity is unclear. Furthermore, within a single species in different regions, there is often variation in what proportion of the local population turns red, showing that it is a variable trait subject to selection. To support his hypothesis, he examined the relative proportion of red against green autumn foliage in wild versus cultivated fruit trees. Cultivated fruit trees show a smaller proportion of red leaves compared to their wild counterparts, suggesting that the selective pressures on the leaf color trait has changed upon domestication.

The evidence he has mustered is mostly indirect. We still do not know what is the direct influence of aphid herbivory upon temperate trees. But at least he has shown that the theory, that red autumn coloration could be a warning signal to aphids or other herbivores, is still a plausible one. More work obviously has to be done to tease apart the various interactions that are going on. In the tropics, one related question is the bright coloration of young and immature foliage. What function does this coloration serve? Perhaps a similar process might be going on, and it would be interesting to see how immature foliage coloration in tropical plants correlates with secondary metabolite content (anti-herbivory agents) and actual rates of herbivory.