This researched aimed to evaluate the LES paradigm at the level of intraspecific trait variation, and its potential to explain insect herbivore resistance. Our results demonstrate that the paradigm can indeed be useful for explaining intraspecific variation in plant strategies. Fast-growing, resource-acquisitive aspen had higher specific leaf area, higher foliar nitrogen concentrations, and lower foliar salicinoid concentrations, resulting in low herbivore resistance, when compared with more resource-conservative strategies. No strong insect preference-performance linkage was found, and aspen traits affected the two indicators of herbivore resistance somewhat differently. Larvae preferred to feed on aspen with low salicinoid concentrations and fast growth. Larvae also performed well on aspen with low salicinoid concentrations, but performance was primarily associated with nitrogen and specific leaf area. In summary, leaf economics traits were useful indicators of plant resistance strategies.
Observed trait patterns within P. tremuloides align with those found among species worldwide. Intraspecific LES patterns have been demonstrated in a variety of species (e.g., common reed: Hu et al. 2015; coffee: Martin et al. 2017). Yet, recent comparisons of the LES across diverse ecological and taxonomic scales reveal that trait correlations can be scale-dependent. For example, in their meta-analysis of 2,031 species, Anderegg et al. (2018) found that, though directions remain consistent, magnitudes of trait correlations with LMA (i.e., ) and nitrogen vary among taxonomic scales. Other research also shows that conformation with LES patterns can depend upon spatial scales (Messier et al. 2017). We could not evaluate spatial dependence but trait patterns driven by genetics are unlikely spatially structured in Wisconsin aspen due to lack of population structure (Cole 2005; Barker et al. 2019b).
This work also reveals that incorporation of defense traits can benefit assessments of the LES at the intraspecific level. Recent research shows that plant defense is correlated with traditional LES traits within and among species. For example, Helianthus defense is correlated with interspecific LES strategy (Mason and Donovan 2015). Similarly, across species of spiny plants, physical defenses are associated with leaf productivity, whereas chemical defenses are not (Armani et al. 2020). Both chemical and physical defense traits are correlated with LES traits within Asclepias syriaca, but not among different Asclepias species (Agrawal 2020). In short, a growing body of literature suggests that the utility of incorporating herbivore defense into the LES paradigm is species- or context-specific. A major limitation of a defense-integrated LES paradigm is the sheer diversity of defense types, which makes comparisons across species challenging. Even so, because herbivores are ubiquitous and formative components of plant communities, incorporation of herbivore defense traits will likely enhance the value and function of LES models.
Our results show that not only are defense traits associated with leaf economics strategies, but so too are defense outcomes. While it is clear that intraspecific plant strategies result in tradeoffs between growth and defense traits in many systems (Endara and Coley 2011; Züst and Agrawal 2017), to our knowledge, none of the recent evaluations of plant defense and the LES include measures of resistance outcomes. Covarying effects of plant traits on herbivore fitness are well known (e. g., Simpson and Raubenheimer 2001) and defense traits are particularly well-studied (e.g., Gong and Zhang 2014). This work further establishes how those traits are integrated across a spectrum of intraspecific functional strategies and the consequences thereof for trophic interactions.
Intraspecific covariation in defense and conventional LES traits has important ecological and evolutionary consequences in aspen and other Populus species. Foliar nitrogen and salicinoids govern the preference, performance, distribution, and abundance of herbivorous insects, as well as their rates of defoliation (Donaldson and Lindroth 2007; Falk et al. 2018). They also influence the structure of herbivorous insect communities (Bangert et al. 2006; Barker et al. 2018, 2019a) and dynamics of multi-trophic interactions (Bailey et al. 2006). More recently, work with experimental aspen stands documented that intraspecific competition alters the consequences of genotypic growth-defense tradeoffs, leading to divergent genetic architecture of aspen populations (Cope et al. 2021).
The relationship between host plant selection and performance of insect herbivores remains equivocal. The most comprehensive meta-analysis of preference-performance relationships to date found that survival, but not weight or development time, are associated with host preference (21 comparable plant-insect systems; Gripenberg et al. 2010). For gypsy moths and numerous other insects, however, preference and performance appear unrelated (e.g., Valladares and Lawton 1991; Underwood 1994; Fritz et al. 2000).
Gypsy moth larvae engage in host plant selection by dispersing from unsuitable hosts (Capinera and Barbosa 1976; Lance and Barbosa 1981). These decisions appear to be made primarily in response to chemical defenses; Solari et al. (2002) found that gypsy moth larvae respond strongly to deterrent stimuli (i.e., nicotine) but not to classical nutrition stimuli. Our work reaffirms these findings. Gypsy moths selected hosts according to salicinoid concentrations and largely ignored performance-associated nutrients (i.e., nitrogen).
In conclusion, our work reveals that the leaf economics spectrum can be useful for describing patterns of association among plant functional traits, - including herbivore resistance traits - at the intraspecific level. In trembling aspen, genotypes of resource acquisitive plants had high specific leaf area, high nitrogen concentrations, and low salicinoid concentrations compared with resource conservative genotypes. This trait combination elicited higher herbivore preference, and performance, relative to insects on resource conservative plants. Patterns of phenotypic relationships identified in this research suggest that growth-associated traits render individuals more susceptible to herbivore attack.