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