Tolerance and phenological avoidance of herbivory in tarweed species

Abstract

Avoidance and tolerance of herbivory are important components of plant interactions with herbivores. Their relationship to each other and to plant defense is important in understanding how plants maximize fitness in the face of herbivore pressure. Various tarweed species have populations comprised of both early-season and late-season flowering individuals. Late-season flowering individuals employ a recently described indirect defense against herbivores in which the accumulation of dead insects on their sticky surfaces attracts predatory insects that eat herbivores. In two tarweed species (Hemizonia congesta and Madia elegans), we observed that key herbivores rarely interact with early-season individuals in the field, and early-season individuals did not invest in dense glandular trichomes that cause indirect defense. We conducted field and greenhouse bud-removal experiments to assess tolerance of M. elegans to herbivore damage. We found that lateseason individuals were more tolerant of simulated herbivory than early-season individuals in both the field and the greenhouse. Late-season individuals that were forced into an earlier phenology with a 24-h light cue lost their tolerance to simulated herbivory. One possible mechanism linking phenological avoidance of herbivores with decreased tolerance is that early-season individuals invested less in below-ground biomass than late-season individuals, which may accumulate belowground resources for regrowth at the expense of early flowering.

Macroevolutionary constraints to tolerance: trade‐offs with drought tolerance and phenology, but not resistance

“…While this logic is impeccable in theory, in practice, the majority of studies that look for tolerance-resistance relationships look for them within species, and typically find no relationship, or even positive ones (Tiffin and Rausher 1999, Leimu and Koricheva 2006, N uñez-Farf an et al 2007, Stevens et al 2007, Carmona and Fornoni 2013. A positive relationship between resistance and tolerance might be expected for several reasons, for example: because resource acquisition processes change the ability to invest in both tolerance and resistance, because costs of tolerance and resistance are mediated by factors other than internal resource allocation, and because plants that experience high herbivore pressure may benefit from both strategies (Stowe et al 2000, Fornoni et al 2004, N uñez-Farf an et al 2007, Krimmel and Pearse 2016. Moreover, within-species variation may not be great enough to test a hypothesis developed for differences in tolerance and resistance across species, for which the range in trait values is much greater.…”

“…Phenology-related traits have shown a close association to plant tolerance within species in several systems (Weinig et al 2003, Ehrl en and M€ unzbergov a 2009, Lehndal and Agren 2015, Krimmel and Pearse 2016, though the theories about the relationship between plant phenology and tolerance have not been as clearly formalized as those relating tolerance to resources or resistance. A common prediction is that species that flower later relative to rosette formation or investment in vegetative growth have greater tolerance in herbaceous species.…”

“…Tolerance may be constrained by early phenology because plants that flower and senesce early do not have time to accumulate resources allowing compensation for damage, whereas late-flowering plants may have such time. In favor of this hypothesis, late-flowering, herbivore tolerant genotypes of annual Madia elegans lost their herbivore tolerance when forced into an earlier phenology by an artificial bolting cue (Krimmel and Pearse 2016), and later-flowering herbaceous annuals that receive early damage may have time to rebuild resources for tolerance (Trumble et al 1993). Second, early phenologies may cause relaxed selection for tolerance because plants that reproduce and senesce early may be more likely to escape herbivores altogether (Bishop andSchemske 1998, Krimmel andPearse 2016).…”

Cumulative herbivory outpaces compensation for early floral damage on a monocarpic perennial thistle

“…Although C. canescens plants had the potential to tolerate loss of the large, early apical flower head investment, such tolerance was insufficient on average to override the fitness costs imposed by cumulative floral herbivory. The relative advantage of high early investment, that escapes herbivores, compared to that of releasing additional investment to other flowers, likely varies extensively in time and space (i.e., Brody and Irwin 2012;Klimešová et al 2014;Krimmel and Pearse 2016). For instance, Adhikari and Russell (2014) found a greater proportion of flowering heads developed in response to apical damage in another native thistle (Cirsium altissimum), but the fecundity of axillary flower heads was insufficient to provide compensatory seed production.…”

“…Effective compensation depends upon multiple interactions; response capacity, and the range of damage at which tolerance works, varies with ecological context. Plant resource condition, herbivore dynamics, phenological overlap with shared hosts and pollinators or competing predators, and timing of damage can influence the degree of plant tolerance (Kolb et al 2007;Wise and Abrahamson 2007;von Euler et al 2014;Lehndal and Ågren 2015;Krimmel and Pearse 2016;Stieha et al 2016;Kafle et al 2017). Co-occurring stressors may further interact with cumulative herbivory pressure to inhibit successful tolerance (Lay et al 2011;Nguyen et al 2016).…”