The goal of both apparency theory and the RAH has been to provide a theoretical framework that adequately explains the interspecific variation in plant defensive strategies. The RAH relates the evolution of defences to interspecific differences in inherent growth rate, whereas apparency theory assumes that defences are related to a species’ predictability to herbivores. Although the theories have different assumptions regarding the reasons leading to defence differences, some of the predictions are similar. For example, both theories agree that long-lived, slow-growing species (apparent species) should invest more in defences than short-lived, fast-growing species (unapparent species). However, a fundamental difference between the theories is their contrasting predictions for the amount of herbivory. The RAH predicts that fast-growing species should suffer greater herbivore damage, while apparency theory predicts similar losses for apparent and unapparent species. In the discussion that follows, we examine results for defence and herbivory, as these apply to both theories. We also examine two predictions that apply only to the RAH, that resources affect growth and that growth affects leaf lifetimes.
Prediction 2: growth rate effects on leaf lifetime
As predicted, slow-growing species have leaves with significantly longer leaf lifetimes than fast-growing species. Long-lived leaves minimize nutrient losses (Aerts 1995) and constitute an essential adaptation of slow-growing species to habitats with low-resource availability (Grime 1977). The relationship between growth rate and leaf life span was the foundation for suggesting that qualitative defences, because of a higher maintenance cost, would be favoured in leaves with short life spans, and quantitative defences, with high initial costs but low maintenance costs, would be favoured in leaves with long life spans (Coley 1987).
Prediction 3: growth rate effects on defences
Both theories predicted greater investment in defence for slow-growing species, but for different reasons. The RAH predicts that for slow-growing species the opportunity cost of defence will be low and the negative impact of herbivory high. Therefore, slow growers should exhibit higher investments in constitutive defences (Coley 1987). Apparency theory predicted that apparent plants would need effective defences against both specialists and generalists. The results from our meta-analysis found that, when considering only the studies that compared defence investment across species in the same habitat, there was a significant negative effect of growth rate on overall defence investment. This result was also maintained when considering chemical and mechanical defences independently (Fig. 3). Moreover, this pattern appears robust, as the direction of the growth effect on defences was the same when comparing different latitudes and ontogenetic stages.
Although defences were universally higher in slow growers, our meta-analysis showed that defence differences between fast and slow growers were significantly greater in tropical ecosystems. Possible explanations for this pattern might lie in the fact that, in the tropics, there is a higher absolute investment in defences (Coley & Aide 1991), a higher variance in defensive compounds (Gauld & Gaston 1994), and a greater range of plant growth rates (Van Zandt 2007). Greater amounts and ranges could facilitate detection of differences. Similarly, there was a negative effect of growth on overall defences for all ontogenetic stages, but the magnitude of this effect was significantly higher for seedlings. The reason for this is unclear, however, again, it may be easier to detect differences in defences if seedlings invest more than other age classes because of the potentially devastating effects of herbivory (Barton & Koricheva 2010; but see Boege & Marquis 2005).
However, when analysing the studies comparing two or more different species from different sites, we did not find a significant effect of growth rate on overall defences. This was consistent whether habitats differed with respect to nutrients or light. We interpret this as resulting from a combination of phenotypic responses of plants to short-term changes in resources with selection for different defence strategies in different habitats. Thus, these results can be better explained by integrating both the RAH and the carbon-nutrient balance hypothesis (CNB; Bryant, Chapin & Klein 1983; Dyer & Coley 2002; Stamp 2003). The CNB hypothesis suggests that when resources are in excess of what can be used for growth, they will be invested in defences. Accordingly, under high light where carbon is in excess relative to nutrients, this theory predicts higher amounts of carbon-based defences, whereas the RAH predicts lower defences for species adapted to this low-resource condition. Because of these counterbalancing influences, we would expect no significant effect of plant growth on defences, and this is what we found in our meta-analysis for studies comparing species from sites with different levels of light. In another study, Baldwin & Schultz (1988) also found no significant differences in phenol investment when comparing species of the genus Piper from gaps and understorey. For mechanical defences, the CNB theory does not have a prediction, while the RAH predicts lower mechanical defences for species adapted to high-light levels. Again, our results were consistent with this, as leaves of slow-growing species were significantly tougher.
In contrast to the defence comparisons across light gradients, which were consistent with the combined effects of RAH and CNB theories, results from habitats with different nutrient levels were confusing. Under high nutrient levels, both the CNB hypothesis and the RAH predict lower carbon-based defences, however, we found a non-significant opposite trend. Another meta-analysis (Koricheva 1998) also found a weak but negative effect of fertilization on carbon-based defences. Although Herms & Mattson (1992) proposed a model that integrates genetic and phenotypic plasticity, the predictions are nonlinear and complex, making it difficult or impossible to capture secondary metabolic responses to variation in resource availability (Stamp 2003). Thus, when comparisons are made within a site, there is a clear negative relationship between plant growth and defence following the RAH, however, when confounding effects of environmental plasticity are included (Figs 4 and 5), particularly those associated with nutrient gradients, it is obvious that our understanding is incomplete.
The RAH also predicts higher inducible defences in fast-growing species. This is because the opportunity cost of defence is higher for fast growers, and because fast growers may more often occur under conditions that favour induction, such as predictable, but periodic herbivore attack (Karban 2011). Although we did not analyse this prediction, supporting evidence has been found. In a literature review of 68 studies, Nykanen & Koricheva (2004) found that the production of phenolics and protein-precipitation capacity of tannins increased in fast-growing species after herbivore damage more than in slow-growing species. Van Zandt (2007) found a similar result in an experimental study with nine species of temperate herbaceous plants.
Plant defences: unanswered questions
A pattern first identified by Feeny was that unapparent plants invested in qualitative defences and apparent plants in quantitative defences. Although this observation has been fairly well supported, the reasons why are still unclear. A quantitative review of defensive classes in different plant guilds corroborated this idea by finding that fast-growing plants (apparent plants) are most often defended with quantitative, dose-dependent defences and slow-growing plants (unapparent plants) with qualitative defences (T. Massad & L. Dyer, pers. comm.). Feeny suggested it was because quantitative defences worked against all herbivores, while qualitative defences worked only against generalists and non-adapted specialists. However, the fact that the herbivores attacking apparent and unapparent plants are a similar mix of specialists and generalists (Futuyma & Gould 1979), and that quantitative and qualitative defences do not have different effects on generalists vs. specialists herbivores (Smilanich 2008; Carmona, Lajeunesse & Johnson 2011; T. Massad & L. Dyer, pers. comm.) brings this explanation into question. Another criticism of apparency theory, though one that we do not view as a fatal attack, is that the primary function of tannins may not be to bind proteins and reduce digestion (Bernays 1981). Instead, more recent evidence shows that oxidation of hydrolysable tannins forms reactive oxygen species, which can overwhelm the antioxidant defences of herbivorous insects and damage midgut tissues (Martin, Martin & Bernays 1987; Appel 1993; Summers & Felton 1994; Salminen & Karonen, 2011). Nonetheless, this could be considered a quantitative defence as higher concentrations of hydrolysable tannins will lead to greater levels of oxidative stress.
The RAH proposed that leaf lifetime, which is related to plant growth rates, is the key factor directing selection for the type of defence. They argued that qualitative defences, in addition to being present in low concentrations, are low molecular weight molecules with high turnover or maintenance rates. In contrast, quantitative defences such as condensed tannins, would require a considerable initial investment since they are present at high concentrations, but because they do not turnover, there would be no subsequent maintenance costs. Thus, for species with short-leaf lifetimes, it would be more cost effective to invest in qualitative compounds, whereas for long-lived leaves, the cumulative cost would be lower for quantitative compounds. However, this argument rests on differences in turnover rates for qualitative and quantitative compounds, an assumption that also has been challenged (Mihaliak, Gershenzon & Croteau 1991; Baldwin & Ohnmeiss 1994; van Dam et al. 1995; Salminen & Karonen 2011). Thus, the underlying factors favouring compounds along the quantitative/qualitative continuum remain to be determined.
Prediction 4: Growth rate effects on herbivory
One of the key differences between the RAH and apparency theory is related to the predicted herbivore damage. Apparency theory (Feeny 1976; Rhoades & Cates 1976) predicts similar rates of damage. Unapparent plants escape from specialists and have secondary metabolites that are effective against generalists, whereas, apparent plants have metabolites that are effective against both specialists and generalists. In contrast, RAH predicts that fast-growing species will support higher levels of herbivory than slow-growing species because they are less defended. Our results support the last prediction, since we found a negative and significant effect size of growth rate on herbivory when analysing studies comparing species with different growth rates within the same habitat. Thus, unapparent plant species (fast-growing species according to the RAH) did not escape from herbivory, but had significantly higher levels than apparent species (slow-growing species according to the RAH). Therefore, variation in growth rate among species explains better the differences in herbivory than variation in apparency. We found similar trends in the meta-analyses for studies comparing herbivory and growth rate between species growing in sites with different level of resources. This comparison not only takes into account differences in growth rates, but also differences between sites in overall herbivore pressure. A negative effect size of growth suggested that fast-growing species from resource-rich habitats suffered higher herbivory than slow-growing species from resource-poor habitats. However, the greater variance and absence of significance is consistent with herbivore pressure varying among habitats.
In addition to high herbivory on unapparent, fast-growing species, there is no evidence that they are attacked more by specialists than ephemeral species (Futuyma & Gould 1979; Cates 1980; Basset 1992), a key element of apparency theory posited to drive selection for different defence strategies. The host-finding abilities of insect herbivores are sufficiently good that escape from discovery does not appear to occur, except perhaps for extremely ephemeral species or tissues. Thus the patterns of defence first described by Feeny may not be adequately explained by a plant’s apparency, as this does not lead to differential attack by specialist vs. generalist herbivores.