10.5061/DRYAD.X3FFBG7DZ
Sercu, Bram
0000-0003-4037-1677
Ghent University
Moeneclaey, Iris
Ghent University
Bonte, Dries
Ghent University
Baeten, Lander
Ghent University
Data from: Induced phenological avoidance: a neglected defense mechanism
against seed predation in plants
Dryad
dataset
2019
Plant development and life‐history traits
Plant‐herbivore interactions
timing
Research Foundation - Flanders
https://ror.org/03qtxy027
W0.003.16N
2019-11-28T00:00:00Z
2019-11-28T00:00:00Z
en
https://doi.org/10.1111/1365-2745.13325
282003 bytes
2
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
1. Flowering phenology is an important life history trait affecting
plant reproductive performance and is influenced by various abiotic and
biotic factors. Pre-dispersal seed predation and pollination are expected
to impose counteracting selection pressure on flowering phenology, with
pre-dispersal seed predation expected to favor off-peak flowering and
pollination to favor synchronous flowering. 2. Here we studied the
effect of pre-dispersal seed predation by the beetle Byturus ochraceus, a
specialist seed herbivore, on the flowering phenology of Geum urbanum.
This forest understorey plant species is self-pollinating, so that the
influence of seed predation can be studied independent from pollination.
We measured in detail the timing and predation rate of individual flowers
during two consecutive years in more than 60 individuals. We tested the
hypotheses that pre-dispersal seed predation exerts selection for
within-season compensatory flowering as well as for induced phenological
avoidance in the following season. 3. We found no indication for
compensatory flowering within a growing season, but plants that
experienced predation shifted their flowers to the end of the flowering
season the subsequent year. This induced phenological avoidance points to
a plastic response to pre-dispersal seed predation that may be adaptive.
Importantly, the delay in flower production came at a cost, since flowers
later in the season had a reduced seed output, presumably because of
increasing light limitation following forest canopy closure. 4.
Synthesis: Herbivory by specialist enemies can cause serious fitness
decline in hosts. We here show that induced shifts in phenology can form
an important defense strategy against pre-dispersal seed predation. The
induced mismatches between herbivore and host phenology are anticipated to
be adaptive when herbivory is predictable across successive flowering
periods.
Study site and species The research was conducted in the Aelmoeseneie
forest, located south of Ghent (Gontrode, Belgium). This ca. 30 ha
forested area entails a mix of ancient and post-agricultural forest and
has been managed as high forest since 1950 (Vanhellemont &
Verheyen, 2011). The soil consists of sand and sandy loam with alluvial
ash forest on the more humid parts and acidophilous beech forest on the
drier sandy parts. Within the forest, we selected ten groups of Geum
urbanum plants in different locations spread over the forest. A group of
individuals located close to each other, within a radius of 15 m, was
considered a ‘plot’. In 2015, 59 plants were marked for detailed
monitoring (N = 10 plots, 4-6 plants per plot). In 2016, the set of
monitored plants was expanded with another 50 plants to obtain a larger
sample size (N=12 plots, 4 – 15 plants per plot). In 2017 only the plants
from 2016 were monitored. Differences in abiotic conditions, i.e. canopy
openness, canopy phenology and chemical soil conditions were measured and
controlled for but none of these variables were correlated with flowering
phenology, reproductive output or presence of seed predators and could
therefore be ignored in this study (unpublished data). Plants were
monitored once a week in 2015 from May until October. Timing of flower
emergence was recorded as the day of the year and all open unmarked
flowers were marked with a unique tag to enable identification of
individual flowers. Total number of flowers per plant could be derived
from these data at the end of the season. Based on the data of 2015,
flowers were monitored on fewer occasions in 2016 (July 4, 12, 20, 27,
August 12 and September 7; day of year 186, 194, 202, 209, 225, 251) and
2017 (July 13, September 19, October 18; day of year 194, 262, 291). We
observed two flowering peaks per season during the three consecutive years
of observations and during a preliminary study in 2014: high number of
flowers in June (around day of year 150) and in August (around day of year
225) and a period with fewer flowers in between (around day of year 194)
(SI 1 in the Supplementary Information). This period of fewer flowers
coincides with the end of predator infection. Because of the bimodality of
the flowering phenology of G. urbanum, off-peak flowering cannot be
straightforwardly quantified. We therefore defined off-peak flowering
relative to the activity period of the seed predators, that is, flowering
away from the peak in seed predator activity. During the first flowering
peak, most flowers emerged, and seed predation took place. We hence
calculated, for each plant, the proportion of flowers that appeared in the
second flowering peak relative to the total number of flowers produced on
each plant as a measure of ‘off-peak’ flowering. In 2015 and 2016, flowers
were collected throughout the season when seeds were ripe, that is, for
each plant we collected flowers on different occasions. In 2015, few
flowers contained beetle larvae, which means that seed herbivory was still
ongoing. In 2016, flowers were collected slightly later in order to ensure
that seed herbivory was completed and no larvae were found in the flowers
anymore. No seeds were collected in 2017. Only flowering phenology data
were collected to test for lagged effects of seed predation on flowering
phenology. The seeds from all flowers were checked for herbivory by
Byturus ochraceus. The number of seeds and seed mass was determined
separately for predated and unpredated seeds for each flower. From these
data, we calculated the mean mass per seed for unpredated seeds. We used
seed mass as a proxy for reproductive output instead of the number of
seeds, since many flowers contained small seeds that were weakly
developed. Moreover, we found a strong correlation between seed mass and
germination probability (unpublished results). As a measure of
reproductive output per flower, total seed mass per flower was calculated
as the sum of the mass of predated and unpredated seeds. We included the
weight of the predated seeds since predation rate could vary among seeds
from completely eaten (with negligible weight) to minor damage, leaving
most of the seed intact. Because we have no information on the germination
probability of damaged seeds, the most conservative approach, that does
not exaggerate the effect of predation on reproductive output, is to add
the weight of predated seeds. As a measure of reproductive output per
plant, total seed mass per plant was calculated as the sum of the seed
mass of all flowers on that plant. For the analysis, we used a categorical
variable for predation occurrence at flower and plant level with two
categories: predated or unpredated (‘predation’ hereafter). A flower was
considered predated if at least one seed showed signs of predation and a
plant was considered predated if at least one flower was predated.