The Botanical Review 73(4): 279–289 What Do Red and Yellow Autumn Leaves Signal? Simcha Lev-Yadun Department of Biology Faculty of Science and Science Education University of Haifa - Oranim Tivon 36006, Israel and Kevin S. Gould Department of Botany University of Otago, Dunedin, New Zealand Abstract . 279 Introduction . 280 Previous Hypotheses for the Signaling Function of Red and Yellow Autumn Leaves . 280 Autumn Leaves and the Nature of Signals . 282 We Propose That Autumn Leaves Signal That They Are About to Be Shed . 282 The Risk of Herbivore Attacks and the Strength of Defense . 282 Autumn Leaf Colors Undermine Herbivorous Insect Camouflage . 283 Size of Color Patch and Efficiency of Insect Camouflage . 284 Red and Yellow Autumn Leaves Are Aposematic . 284 Leaf Color Variability . 285 Conclusions . 285 Acknowledgments . 286 Literature Cited . 286 Abstract The widespread phenomenon of red and yellow autumn leaves has recently attracted considerable scientific attention. The fact that this phenomenon is so prominent in the cooler, temperate regions and less common in warmer climates is a good indication of a climate-specific effect. In addition to the putative multifarious physiological benefits, such as protection from photoinhibition and photo-oxidation, several plant/animal inter- action functions for such coloration have been proposed. These include (1) that the bright leaf colors may signal frugivores about ripe fruits (fruit flags) to enhance seed dispersal; (2) that they signal aphids that the trees are well defended (a case of Zahavi’s handicap principle operating in plants); (3) that the coloration undermines herbivore in- sect camouflage; (4) that they function according to the “defense indication hypothesis,” which states that red leaves are chemically defended because anthocyanins correlate with various defensive compounds; or (5) that because sexual reproduction advances the Copies of this issue [73(4)] may be purchased from the NYBG Press, The New York Botanical Garden, Bronx, NY 10458-5125, U.S.A. Please in- quire as to prices. Issued 28 December 2007 © 2007 The New York Botanical Garden 280 THE BOTANICAL REVIEW onset of leaf senescence, the pigments might indicate to sucking herbivores that the leaves have low amounts of resources. Although the authors of hypotheses 3, 4, and 5 did not say that bright autumn leaves are aposematic, since such leaves are chemically defended, unpalatable, or both, we suggest that they are indeed aposematic. We propose that in addition to the above-mentioned hypotheses, autumn colors signal to herbivorous insects about another defensive plant property: the reliable, honest, and critical informa- tion that the leaves are about to be shed and may thus cause their mortality. We empha- size that all types of defensive and physiological functions of autumn leaves may oper- ate simultaneously. 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 synthe- sized 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 bene- fits of autumn leaf coloration, such as an enhanced recovery of foliar nitrogen owing to the protection by anthocyanins from photoinhibition and photo-oxidation (Ya- masaki, 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; Schae- fer & Wilkinson, 2004; Gould, 2004; Ougham et al., 2005). These physiological ad- vantages 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 al- ready 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 envi- ronmental issues are being discussed, we consider that the evolution of autumn leaf coloration reflects an adaptation both to physiological pressures and to other organ- isms. 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 sig- nal that the trees are well defended, representing a case of Zahavi’s handicap principle WHAT DO RED AND YELLOW AUTUMN LEAVES SIGNAL? 281 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; Sinkko- nen, 2006a, 2006b; Schaefer & Rolshausen, 2006, 2007; Chitka & Döring, 2007; Rol- shausen & 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 sig- naler (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 decid- ing whether or not to respond. Archetti (2000) specifically rejected the possibility that autumn leaf coloration is aposematic, and other studies that favor the signaling hypothe- sis (Hamilton & Brown, 2001; Hagen et al., 2003, 2004; Archetti & Brown, 2004; Ar- chetti & 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 ob- jections, Holopainen and Peltonen (2002) proposed that leaves that had just turned yel- low 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 func- tion 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 understand- ing of the possible role in defense. Since honest signals are not always costly (Lach- mann et al., 2001), there is no need for them to be so in the case of bright autumn leaves. Schaefer and Rolshausen (2006) proposed an upgraded and combined new hypothe- sis for defensive plant coloration, focusing on anthocyanins. Elaborating on a previous idea by Fineblum and Rausher (1997) concerning the common biochemical pathways for flower color and defensive molecules, Schaefer and Rolshausen (2006) formulated the “defense indication hypothesis.” This hypothesis predicts that fewer herbivorous in- sects (and we propose any sensitive herbivore) will feed on plants that have strong an- thocyanin coloration because it correlates with the strength of a chemical defense. The biochemical basis for this correlation is that anthocyanins and a number of defense chemicals such as tannins stem from the same biosynthetic pathways. A new defensive hypothesis about the function of autumn leaf colors has recently been proposed following the observation that in mountain birch, leaves turn yellow ear- lier if the trees produce an abundance of female catkins (Sinkkonen, 2006a, 2006b). Sinkkonen proposed that leaf coloration might signal to sucking herbivores that the leaves hold low amounts of resources. Although not explicitly stated as such, signaling about low-quality food yet again implies aposematism. This new hypothesis warrants further study. However, since young and even mature nonflowering individuals also ex- press the autumn coloration, the role of reproduction in the evolution of this coloration