What do red and yellow autumn leaves signal?

Botanical Review, The, Oct-Dec, 2007 by Simcha Lev-Yadun, Kevin S. Gould

Abstract
Introduction
Previous Hypotheses for the Signaling Function of Red and Yellow
   Autumn Leaves
Autumn Leaves and the Nature of Signals
We Propose That Autumn Leaves Signal That They Are About to Be Shed
The Risk of Herbivore Attacks and the Strength of Defense
Autumn Leaf Colors Undermine Herbivorous Insect Camouflage
Size of Color Patch and Efficiency of Insect Camouflage
Red and Yellow Autumn Leaves Are
Leaf Color Variability
Conclusions
Acknowledgments
Literature Cited

Introduction

Bright red and yellow autumn leaves are a widespread phenomenon, particularly in temperate regions (Hoch et al., 2001). For many decades, most people believed that these colors simply appeared after the degradation of chlorophyll that masked these pigments, and that they served no function. Recently, however, it has been shown that in many plants, anthocyanins are not simply unmasked but rather synthesized de novo by leaves in mid-senescence (Lee et al., 2003). Thus, the question of the possible physiological and ecological benefits of this coloration has attracted considerable scientific attention. There is very good evidence for physiological benefits of autumn leaf coloration, such as an enhanced recovery of foliar nitrogen owing to the protection by anthocyanins from photoinhibition and photo-oxidation (Yamasaki, 1997; Chalker-Scott, 1999; Matile, 2000; Feild et al., 2001; Gould et al., 2002a; Lee & Gould, 2002a; Hoch et al., 2001, 2003; Close & Beadle, 2003; Schaefer & Wilkinson, 2004; Gould, 2004; Ougham et al., 2005). These physiological advantages notwithstanding, certain hypotheses regarding nonphysiological functions of autumn leaf coloration also merit consideration. Gould et al. (2002b), Lev-Yadun et al. (2002, 2004), Lev-Yadun (2006), and Schaefer and Wilkinson (2004) have already argued that the nonphotosynthetic plant pigments have the potential to serve more than one function concurrently. Thus, various hypotheses concerning coloration of leaves and other plant parts need not contrast with or exclude any other functional explanation of specific types of plant coloration, and those traits such as coloration that might have more than one type of benefit may be selected for by several agents. Consistent with Grubb's (1992) view that defense systems are not simple, and with Diamond's (2005) view that single-factor explanations can fail when complex environmental issues are being discussed, we consider that the evolution of autumn leaf coloration reflects an adaptation both to physiological pressures and to other organisms. Such synergistic gains may cause evolution of the red leaf color trait to be quicker and more frequent.

Previous Hypotheses for the Signaling Function of Red and Yellow Autumn Leaves

One of the earliest proposals that autumn leaves function as a signal to animals held that the pigments serve as a fruit flag for frugivores (Stiles, 1982; Willson & Hoppes, 1986; Facelli, 1993). Several additional roles of this coloration in defense against insect herbivory have been proposed. The first proposed, that the colors of autumn leaves signal that the trees are well defended, representing a case of Zahavi's handicap principle operating in plants (Archetti, 2000, 2007a, 2007b; Hamilton & Brown, 2001; Hagen et al., 2003, 2004; Archetti & Brown, 2004; Archetti & Leather, 2005; Brown, 2005), is an idea that some accept only partly or not at all (Holopainen & Peltonen, 2002; Wilkinson et al., 2002; White, 2003; Schaefer & Wilkinson, 2004; Ougham et al., 2005; Sinkkonen, 2006a, 2006b; Schaefer & Rolshausen, 2006, 2007; Chitka & Doring, 2007; Rolshausen & Schaefer, 2007; Schaefer & Gould, 2007). The handicap principle (Zahavi, 1975) states that signaling is costly and therefore reliable. It has been proposed that those features that constitute the handicap evolved as a measure of the quality of the signaler (Zahavi, 1975, 1977, 1987; Grafen, 1990; Zahavi & Zahavi, 1997). Organisms that operate under the handicap principle send honest (and usually, but not always, costly) signals (Lachmann et al., 2001), which the receiver can evaluate in the process of deciding whether or not to respond. Archetti (2000) specifically rejected the possibility that autumn leaf coloration is aposematic, and other studies that favor the signaling hypothesis (Hamilton & Brown, 2001; Hagen et al., 2003, 2004; Archetti & Brown, 2004; Archetti & Leather, 2005) do not discuss aposematism. Lee and Gould (2002b), Lee (2002), Gould (2004), and Sherratt et al. (2005) interpreted the hypothesis of handicap-related coloration as described by Archetti (2000) and Hamilton and Brown (2001) as a case of aposematism, notwithstanding the different view of the authors. As for the objections, Holopainen and Peltonen (2002) proposed that leaves that had just turned yellow would be good indicators to aphids that nitrogen in the form of amino acids was available in these leaves. Wilkinson et al. (2002) proposed that rather than signaling aphids about their defensive qualities, especially since yellow leaves attract aphids, the yellow coloration serves as a sunscreen, and that red colors both warm leaves and function as antioxidants. Ougham et al. (2005) stressed that the physiological role of autumn leaf coloration is both important and well documented. They argued that the signal is not costly, yet plants often show within-canopy variation in leaf color; thus, studies of individual leaves, rather than of canopies as a whole, might provide a better understanding of the possible role in defense. Since honest signals are not always costly (Lachmann et al., 2001), there is no need for them to be so in the case of bright autumn leaves.