Phytoecia rufiventris
Introduction
Plants attacked by insect herbivores defend themselves to minimize fitness loss by the attack . While the herbivore attack is blocked by resistance traits (e.g., Plant secondary metabolites , protease inhibitors , and herbivore-induced plant volatiles ), the damage is restored by tolerance traits . Tolerance allows plants to grow and reproduce under herbivore attack. Specifically, insect attacks induce an increase in photosynthetic rate and compensatory growth which overcome the loss of tissue by herbivory. Especially, damage to the apical meristem releases the apical dominance and induces branching which leads to increased production of the reproductive organ . Attacked plants also reallocate resources from damaged organs to less vulnerable organs and boost proliferation to restore damage . The tolerance responses of plants that are often sufficient to recover from damage may even overcompensate for the performance of undamaged plants .
Although tolerance response is generally accepted as adaptive, the degree to which the damage is restored varies. The mode of attack , nutritional state , abiotic factors , and neighbors in the same community affect the extent of damage compensation in the attacked plant. Thus, the adaptive value of tolerance response may differ depending on context. It is important to understand both the cost and benefit of one trait to evaluate the fitness value of the trait. While there are several mechanisms studied that exert costs on tolerating plants (e.g., increased herbivory ), what factors hinder tolerating plants from restoring fitness is less studied compared to the apparent benefit of tolerance response.
The difference in fitness between damaged and undamaged plants is a typical measure of tolerance. While it is the most precise way to measure fitness following the definition-contribution to the gene pool of the next generation-, the direct measurements of fitness are often replaced by parameters such as plant damage , plant growth , and the number of flowers and seeds . Notably, the extent to which tolerance restores fitness depends on the fitness components used to measure the tolerance. For instance, male and female fitness is differentially restored after herbivore attack while fruit and seed production display different outcomes of tolerance . Moreover, reproductive tolerance can show a trade-off with vegetative tolerance . The inconsistency of multiple parameters restricts our understanding of the adaptive value of tolerance responses. Though measuring the value of tolerance at the offspring growth would be important to evaluate the adaptive value of tolerance, growth and reproduction of offspring produced by tolerating and undamaged plants have not been intensively investigated.
A straightforward but less-investigated feature of tolerance response is the time taken for the response. Delay of phenology is common in attacked and tolerating plants . Phenological shifts, such as delays in germination, growth, and flowering, can be costly, as the life history strategies of plants aim for sophisticated temporal regulation of phase transition, which is critical for maintaining niches over generations . Although phenological shifts can be adaptive in the context of avoiding herbivory , suboptimal regulation of the phase transition may result in a dramatic loss of plant fitness . While phase transitions are controlled by external and internal cues in some plants (e.g., seed dormancy break by karrikin and vernalization-induced flowering ), other plants, including many ruderal species, show less controlled phase transitions . Spontaneous phase transitions in such species (e.g.,Erigeron annuus and rapid-cycling accessions of Arabidopsis thaliana ) can cause variations in the recruitment timing in newly disturbed areas. This variation often plays an important role in the competition . Thus, the impact of the tolerance response on plant fitness must encounter the effect of altered phenology on offspring production.
Here, we tested the hypothesis that the delayed phenology in offspring of tolerating plants is costly using a biennial herb E. annuus L. (Asteraceae) and its stem-boring herbivore Phytoecia rufiventrisGautier (Cerambycidae; Lamiinae). Phytoecia rufiventris females girdle the stem of E. annuus before endophytic oviposition. Girdling kills the upper part of the stem, including the shoot apical meristem, and induces axillary bud emergence. We first examined whether the tolerance response of E. annuus fully compensates for the loss of shoot apical meristem by the attack of girdling beetle. Then we measured the competition-mediated cost of delayed phenology in the offspring of tolerated plants. Finally, the context-dependency of the phenology-associated cost was investigated by excluding competition and herbivory to collectively show that the ecological consequence of tolerance response largely depends on the offspring’s competition.
Materials and methods