Discussion
In comparison to the broad evidence supporting the benefits of tolerance
responses of plants under attack, what factors hinder fitness
compensation by tolerance response are unclear. Measuring fitness using
appropriate parameters is crucial for assessing the adaptive value of a
trait in an ecologically relevant manner . Traits or phenomena can
affect plant fitness at various stages of the plant life cycle .
Although plant growth sufficiently represents fitness in some cases, the
production and/or germination of seeds is considered proxies closer to
actual fitness. In this study, we showed that
restoring the number of flowers
did not fully compensate for the fitness loss caused by girdling beetle
attacks, under intraspecific competition in offspring generation.
Plants under herbivore attack actively increase their photosynthetic
performance to compensate for damage . E. annuus also showed
increased chlorophyll content, which could represent enhanced
photosynthetic performance after girdling by P. rufiventris .
Moreover, insect attacks enhance branching, which results in increased
reproductive organ production . Although girdling behavior caused a
serious loss in flower number due to the loss of shoot apical meristem
in the short term, increased axillary branch emergence in girdledE. annuus restored the number of flowers within 7 weeks of
girdling. At the end of the flowering season, girdled E. annuusproduced not significantly different numbers or sizes of flowers
compared to those in non-girdled E. annuus .
Our attention was drawn to the 2 weeks of delay in flower production in
girdled E. annuus plants. Plant-insect interactions often result
in phenological shifts in plants, and the scale of the shift varies from
hours to months in the context of defense. The phenological shift is
trans-generationally transmitted to make a ‘mismatch’ with herbivory .
However, the delay in flower production in girdled E. annuus ,
which is likely to persist through seed germination due to lack of seed
dormancy, caused a dramatic cost in the intraspecific competition of
offspring rather than benefits from the mismatch. The DG plants, which
were referred to be produced by girdled E. annuus plants, showed
smaller biomass and produced fewer flowers than did the EG plants, which
were referred to be produced by non-girdled E. annuus plants.
The consequences of competition between DG and EG plants were similar in
the greenhouse and field experiments. Our field competition experiment
was designed to test whether the competition-associated cost of delay in
germination is also exhibited in the field, which has different
conditions from those of greenhouse experiments . For instance, rosettes
tolerate cold stress during winter and transition into a reproductive
form in consecutive springs using accumulated resources . Consistent
with the greenhouse results, DG plants produced smaller rosettes, lower
biomass, and fewer flowers than EG plants in the field. Moreover,
herbivore damage was more severe in DG plants than in EG plants during
the rosette stage. As plant ontogeny significantly affects the degree of
defense and the early stages are particularly vulnerable to herbivory ,
it can be suspected that the growth defect by the intraspecific
competition caused weaker defense in DG plants, and even worsened the
inferiority of DG plants over EG plants in the subsequent spring.
Notably, the growth and reproductive trends of the EG and DG plants were
opposite in the two different field experiments performed with and
without biotic interactions. Excluding intraspecific competition and
herbivory led to similar rosette sizes in EG and DG plants. Furthermore,
DG plants produced more branches and, thereby, more flowers than EG
plants in the following year. The observed data may have resulted from
artifacts originated from discrepancies between plant developmental
stages and environmental conditions. The mismatch between resource
demand determined by plant ontogeny and resource availability in the
environment could cause fitness costs . Moreover, the ontogeny of plants
significantly affects the recruitment of plants at the community level .
While the exact mechanism underlying the low fitness of EG plants are
elusive, our field assay without competition may not fully reflect the
relevant phenology of E. annuus and thereby resulted in fitness
defect in EG plants. Nevertheless, when EG and DG plants were planted
closely and exposed to natural herbivory, as in the field, those
potential defects were diminished and EG plants were superior to DG
plants with respect to growth and development, as discussed previously.
These imply that the biotic interaction might have a more major impact
on the fitness of E. annuus compared to abiotic conditions.
Ruderal species, including E. annuus , adopt an opportunistic
strategy of occupying an empty niche caused by disturbance .
Disturbances occur in various ways in ecosystems, and their timing is
unpredictable. Therefore, the long seed dispersal period of pioneer
species might be adapted to increase the chance of invading disturbed
populations , and the girdling-induced delay in flower production might
increase the cost of losing access to the disturbed population.
Plant-herbivore interaction exerts selection on both organisms and the
effects are transmitted over a long period . Although our study was
conducted under the assumption that tolerance-associated delay in flower
production affects intraspecific competition and herbivory in the
subsequent generation, evolutionary changes in plants and herbivore
rooting for such phenomena needs to be studied in the future. Moreover,
interspecific competition which was not considered in the current study
but might strongly affect the fitness of tolerating plants, deserves
further investigation.
Our data emphasize that the restoration of floral production in plants
under herbivory does not fully compensate for fitness in the context of
tolerance responses. However, the current results do not reflect all
aspects of plant fitness. Although girdled E. annuus plants
started to produce flowers 2 weeks later than non-girdled plants, flower
and seed production continued for more than 8 weeks. The wide range of
seed dispersal periods may diminish the initial gap in germination time
between seeds produced by girdled and non-girdled plants.
In this study, we describe an overlooked fitness cost that occurs during
tolerance responses to insect attacks. Although the tolerance response
enabled attacked plants to restore the number of flowers, the
restoration caused 2 weeks of delay in the germination of offspring.
Delayed germination was found to cause critical defects in offspring
under intraspecific competition. In other words, the fitness loss of
being attacked by girdling behavior is inflicted on the offspring
produced by girdled plants, even with a tolerance response. We conclude
that reproductive tolerance which is considered to result in similar
fitness between damaged and undamaged plants, actually may not fully
compensate for the fitness depending on competition and herbivory.
Furthermore, we suggest future research on plant defense, especially
those involving phenological shifts, to take into account the effect of
the shift in offspring to more accurately measure the adaptive value of
plant defense traits.