Signaling defenses with color: a meta-analysis of leaf color variation, palatability, and herbivore damage

Introduction

A complex interplay of leaf functional traits such as size (Zhu et al., 2024), specific leaf area (Poorter et al., 2004; Kozlov et al., 2015), shape (Ferris, 2019; Higuchi & Kawakita, 2019), nutrient stoichiometry (Njovu et al., 2019; Schön et al., 2023), and mechanical and chemical defenses (Hanley et al., 2007; Caldwell et al., 2016; Agrawal et al., 2021) determines how herbivores find and use resources. Leaf palatability, therefore, reflects a syndrome of coordinated leaf traits that ultimately shape plant resistance and/or tolerance to insect herbivory, which in turn is countered by insect adaptation, driving the coevolutionary dynamics between insects and host plants (Ehrlich & Raven, 1964; Archetti et al., 2009; Agrawal & Zhang, 2021). Despite overwhelming evidence of the effects of plant interspecific trait variability on herbivory (see Wetzel et al., 2023; Liu et al., 2024; Zvereva et al., 2024), considerably little attention has been paid to intraspecific leaf color variability that occurs between plant populations or within individual plants. The intraspecific diversity in leaf size, shape, morphology, and color is typically suggested as the product of selective pressures optimizing trait combinations to cope with abiotic conditions that drive strategies of resource use, acquisition, and conservation (Campitelli et al., 2008; Hughes et al., 2022). However, leaf functional traits also influence how plants interact with insect herbivores, but which leaf traits influence variation in herbivory and how these variations arise and are selected have been a long-lasting debate in plant–herbivore interactions (Harper, 1977; Carmona et al., 2011; Muiruri et al., 2019).

While the role of color has been extensively studied in animals, particularly in the contexts of color vision, aposematism, and sexual selection (see Wiens & Emberts, 2024), a comprehensive understanding from the plant perspective is emerging more recently (but see Landi et al., 2015; Renoult et al., 2017). Research has predominantly focused on flower and fruit color, a key trait mediating interactions with pollinators, frugivores, and seed dispersers. However, the significance of leaf color and its implications for understanding plant–herbivore interactions and plant defense mechanisms remain largely underexplored. Leaf color variability is commonly observed in phylogenetically unrelated species and across biogeographic regions (e.g. Lee & Collins, 2001; Lee, 2002; Gong et al., 2020; Hughes & Lev-Yadun, 2023), with nonphotosynthetic pigments arguably playing dual roles in plant physiology and defense (Archetti et al., 2009). The diverse range of leaf color polymorphisms not only likely reflects a complex interplay between environmental factors and physiological processes associated with photoprotection and photoinhibition (Gould et al., 2002; Karageorgou et al., 2008; Archetti et al., 2009; Menzies et al., 2016) but also other sources of stress such as heavy metals (Landi, 2015), temperature (Renner & Zohner, 2019), and nutrient deficiency (Liang & He, 2018). Still, leaf polymorphism may also indicate the end product of evolutionary pressures driven by leaf herbivores (Archetti, 2009; Cooney et al., 2012; Menzies et al., 2016; Lev-Yadun, 2023). Although valuable insights about the ecological role of leaf coloration have been accrued over the past 20 yr (Archetti, 2000; Hamilton & Brown, 2001; Lev-Yadun, 2006, 2014, 2016, 2022; Lev-Yadun & Gould, 2007, 2009; Archetti et al., 2009), our understanding of its significance in mediating plant–herbivore interactions has been mostly focused on autumn leaves. The lack of synthetic views on how leaf color influences herbivory prevents us from generating insights into the adaptive strategies employed by plants to deter or tolerate herbivory under different environmental conditions.

Ontogenetic and seasonal leaf color change is usually coordinated with leaf traits shown to affect herbivory, in which the contribution of mechanical features (Caldwell et al., 2016) and chemical compounds in shaping herbivore selective feeding and ovipositing sites is widely recognized (Moore et al., 2014; Richards et al., 2015; Wetzel & Whitehead, 2020; Muller & Junker, 2022). Variation in color of leaves, petioles, and stems (Lev-Yadun et al., 2004; Lev-Yadun, 2016) can occur during ontogeny, under varying physiological conditions and seasonality in both temperate and tropical regions (Kursar & Coley, 1992; Archetti, 2009; Queenborough et al., 2013). For example, leaf color is linked to plant defenses against herbivores, representing a covariate of trait syndromes associated with the accumulation of secondary compounds (see Cooney et al., 2012) and mechanical defenses (e.g. toughness and trichome density; Poorter et al., 2004; Hughes et al., 2022). These traits often co-vary during leaf ontogeny, as seen in nongreen leaves during young, early developmental stages, which later transition to harder, green, and more herbivore-prone leaves (Chen & Huang, 2013; Ochoa-López et al., 2015; Dayrell et al., 2018).

Several hypotheses have been proposed to explain the relationship between leaf color variability and herbivory incidence and intensity (e.g. Givnish, 1990), as summarized in Fig. 1. The coevolutionary or signaling hypothesis (Archetti, 2000; Hamilton & Brown, 2001; Archetti & Brown, 2004) suggests that nongreen leaves represent honest warning signs of low leaf palatability due to higher concentration and diversity of defensive compounds such as secondary metabolites so that lower herbivory of such leaves would benefit both herbivores and plants. The camouflage hypothesis (Stone, 1979; Karageorgou & Manetas, 2006; Niu et al., 2017, 2018) suggests that nongreen leaves might not be perceived by insects and would therefore escape herbivory. The camouflage hypothesis pertains specifically to red leaves and animals that do not perceive red wavelengths, such as most mammals and many insects (Döring et al., 2009; Hughes et al., 2021; Van Der Kooi et al., 2021). The anti-camouflage hypothesis (or the undermining insect camouflage; Lev-Yadun et al., 2004) proposes that nongreen leaves (especially young red leaves) would enhance the conspicuousness of insect herbivores, making them more apparent and more vulnerable to visually oriented predators, resulting in low herbivory levels. The unpalatability hypothesis (Coley & Aide, 1989; Archetti, 2009) suggests that low herbivory in nongreen leaves or plants with nongreen leaves is due to the presence of nongreen pigments that act as herbivore deterrents, benefiting plants by a direct gustatory effect (Schoonhoven, 1969; Van Loon, 1990). Finally, the net-damage hypothesis (Kursar & Coley, 1992), initially proposed for tropical plants with delayed greening, poses that nongreen leaves are both less nutritive and visually attractive to herbivores, which may function to delay herbivory until the leaves are better mechanically protected. While temperate plants also produce nongreen young leaves, the adaptive significance of this trait may differ from tropical delayed greening, as it often co-occurs with abiotic stress or variegation (e.g. Gould et al., 2002; Hughes & Lev-Yadun, 2023). Although these five hypotheses differ mechanistically, they are functionally similar in that all lead to lower levels of herbivory, due to either bottom-up control via leaf quality or to top-down control via predators or parasites (Fig. 1).

Fig. 1

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Conceptual models and predictions of the effects of leaf color on herbivory based on classical hypotheses aiming to explain intra- and interspecific variation in plant traits, including leaf defense and leaf quality, and insect traits associated with fitness. The response variables commonly evoked by authors to explain differences in herbivory levels in nongreen leaves are listed on the left. Arrows indicate either an increase (pointed up) or a decrease (pointed down) of such variables in nongreen, colored leaves.

Although hypotheses addressing the role of leaf color as an important driver of plant–herbivore interactions have been discussed and exposed to criticism (e.g. Lev-Yadun, 2006) over the past 25 yr (see Archetti, 2000, 2009; Lev-Yadun, 2003, 2016, 2022; Hughes & Lev-Yadun, 2023), a quantitative synthesis incorporating the predictions of the main hypotheses accounting for leaf color variability and its effects on herbivory is still lacking. Here, we aimed to integrate the current hypotheses relating the adaptive value of leaf color with a deep and comprehensive examination of how leaf color influences herbivory patterns. To this end, we conducted a meta-analysis that incorporates the effects of plant phylogeny and biogeographic region to provide a quantitative assessment of the effects of color on (1) plant traits associated with leaf defense and leaf palatability or nutritional quality, (2) traits associated with the fitness of insect herbivores, and (3) interactions between herbivorous insects and plants via leaf consumption. We tested the following predictions: (1) Nongreen leaves will show lower herbivory than green leaves, with stronger effects in tropical species where delayed greening is a common anti-herbivore strategy; (2) Nongreen leaves will exhibit higher defense traits, with stronger effects in tropical plants due to stronger selection pressure from herbivores on young leaves; (3) Nongreen leaves will have lower nutritional quality, with temperate plants showing stronger reductions due to the prevalence of stress- or senescence-related pigments (e.g. anthocyanins in aging leaves); and (4) Herbivore fitness will be lower on nongreen leaves across regions, reflecting their dual role as defended (tropics) or low-quality (temperate) resources.