Autumn tree colours as a handicap signal

Abstract

Many species of deciduous trees display striking colour changes in autumn. Here, we present a functional hypothesis: bright autumn coloration serves as an honest signal of defensive commitment against autumn colonizing insect pests. According to this hypothesis, individuals within a signalling species show variation in the expression of autumn coloration, with defensively committed trees producing a more intense display. Insects are expected to be averse to the brightest tree individuals and, hence, preferentially colonize the least defensive hosts. We predicted that tree species su¡ering greater insect damage would, on average, invest more in autumn-colour signalling than less troubled species. Here, we show that autumn coloration is stronger in species facing a high diversity of damaging specialist aphids. Aphids are likely to be an important group of signal receivers because they are choosy, damaging and use colour cues in host selection. In the light of further aspects of insect and tree biology, these results support the notion that bright autumn colours are expensive handicap signals revealing the defensive commitment of individual trees to autumn colonizing insect pests.

Visual ecology of aphids—a critical review on the role of colours in host finding

“…Because insect and human colour vision are so fundamentally different, any classification of colours that is based on human colour vision (e.g., Hamilton and Brown 2001;Archetti and Leather 2005;Dominy et al 2002) could potentially be misleading when discussing possible effects of colours on insects or any other animals.…”

“…Even if, in a given tree species, reflectance from red autumn leaves was consistently lower (or higher) than from green leaves, noise from small-scale illumination variability would severely diminish the indicator value of 'red'. Hamilton andBrown (2001, p. 1492) predicted that 'specialist aphids of red autumnal trees will have red-sensitive vision and show increasing aversion to increasing red coloration'. However, so far there is no evidence for red receptors in aphids (see previous sections).…”

“…Additional interest in the role of colours in host selection of aphids was recently created by the debate on autumn leaf colouration as a potential signal or cue to aphids (e.g., Sinkkonen 2006), initiated by a paper from Hamilton and Brown (2001); for a review see Manetas (2006). However, in this debate, the perspective of colour perception by the aphids appears to have been largely neglected.…”

The shared and separate roles of aposematic (warning) coloration and the co-evolution hypothesis in defending autumn leaves

“…9 Originally, the co-evolutionary hypothesis addressed both red and yellow autumn leaves. [6][7][8] However, with the later understanding that yellow leaves usually attract rather than repel aphids, [9][10][11][12][13] the co-evolutionary hypothesis was later restricted to red leaves when aphids are concerned. 9 In addition to other various potential anti-herbivory roles, 14,15 red autumn leaf coloration has several potential physiological functions, such as protection from photoinhibition and photo oxidation, and other physiological functions have been proposed but not agreed upon.…”

“…The first was the recognition that anthocyanins are synthesized de novo in red autumn leaves, 1,2 and the second was the formulation of the anti-herbivory co-evolutionary hypothesis. [6][7][8] The updated version of the co-evolutionary hypothesis 9 posits that red autumn coloration signals to all types of insects (including aphids) that migrate to the trees in autumn about their chemical defense, lower nutritional quality or imminent leaf fall, or any other characteristic that would induce a lower fitness in the insects. In addition, yellow leaves signals the same to all herbivores except aphids.…”