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Flowering synchrony drives reproductive success in a wind- pollinated tree

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Synchronised and quasi-periodic production of seeds by plant populations, known as masting, is implicated in many ecological processes, but how it arises remains poorly understood. Flowering and pollination dynamics are hypothesised to provide the mechanistic link for the observed relationship between weather and population-level seed production. We report the first experimental test of the phenological synchrony hypotheses as a driver of pollen limitation in mast seeding oaks (Quercus ilex). Higher flowering synchrony yielded greater pollination efficiency, which resulted in 2-fold greater seed set in highly synchronised oaks compared to asynchronous individuals. Pollen addition removed the negative effect of asynchronous flowering on seed set. Because phenological synchrony operates through environmental variation, this result suggests that oak masting is syn-chronised by exogenous rather than endogenous factors. It also points to a mechanism by which changes in flowering phenology can affect plant reproduction of mast-seeding plants, with subsequent implications for community dynamics.
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LETTER Flowering synchrony drives reproductive success in a wind-
pollinated tree
Michał Bogdziewicz,
1
*
Mario Pesendorfer,
2
Elizabeth E. Crone,
3
Carlos P
erez-Izquierdo
4
and
Raul Bonal
4
Abstract
Synchronised and quasi-periodic production of seeds by plant populations, known as masting, is
implicated in many ecological processes, but how it arises remains poorly understood. Flowering
and pollination dynamics are hypothesised to provide the mechanistic link for the observed rela-
tionship between weather and population-level seed production. We report the first experimental
test of the phenological synchrony hypotheses as a driver of pollen limitation in mast seeding oaks
(Quercus ilex). Higher flowering synchrony yielded greater pollination efficiency, which resulted in
2-fold greater seed set in highly synchronised oaks compared to asynchronous individuals. Pollen
addition removed the negative effect of asynchronous flowering on seed set. Because phenological
synchrony operates through environmental variation, this result suggests that oak masting is syn-
chronised by exogenous rather than endogenous factors. It also points to a mechanism by which
changes in flowering phenology can affect plant reproduction of mast-seeding plants, with subse-
quent implications for community dynamics.
Keywords
Flowering phenology, flowering synchrony, mast seeding, pollen addition, wind pollination.
Ecology Letters (2020)
INTRODUCTION
Synchronous and highly variable seed production among
years by a population of perennial plants, or masting, is impli-
cated in many important ecological processes, from macronu-
trient cycles to resource pulses that have cascading effects on
plant and animal population dynamics, and disease risk in
humans (Ostfeld and Keesing, 2000; Bogdziewicz et al., 2016;
Clark et al., 2019). Several hypotheses have been proposed to
explain the proximate drivers of masting, yet there have been
few experimental tests of underlying theory (Bogdziewicz
et al., 2020a). To date, few manipulative studies have experi-
mentally tested putative proximate drivers of masting (Crone
and Rapp, 2014). This lack of studies has prevented the con-
firmation of causal links, thereby precluding meaningful pre-
dictions about the consequences of changing environments for
plant reproductive patterns and global vegetation dynamics.
Proximately, masting arises by combining two processes:
interannual variability in seed production, and synchronisation
among individuals (Pearse et al., 2016). These two processes are
believed to be the consequence of external factors, such as
resource availability and environmental cues, internal resource
dynamics of plants and pollination success (Crone and Rapp,
2014; Bogdziewicz et al., 2020a). The importance of resource
dynamics as a driver of interannual variability of seed produc-
tion is supported by a number of modelling studies (Rees et al.,
2002; Crone et al., 2005; Bogdziewicz et al., 2018; Schermer
et al., 2019), and also by limited number of resource-manipula-
tion experiments (Crone et al., 2009; Smaill et al., 2011;
Miyazaki et al., 2014). Resource dynamics alone, however, can-
not account for the high synchrony in seed set among plants
within a region, since each plant could presumably maintain its
own unique schedule of high and low seed production years
(Satake and Iwasa, 2000; Rees et al., 2002).
Pollen limitation is an effective method of synchronising
individual plants because processes that prevent flowers from
developing are generally more effective at creating synchrony
than those that affect resource gain (Rees et al., 2002; Crone
and Rapp, 2014; Bogdziewicz et al., 2018). However, pollen
limitation can maintain synchrony of interannual variation in
seed set in at least two ways that differ fundamentally in how
they operate, although they are not mutually exclusive. Pollen
coupling is an endogenous process in which pollination suc-
cess increases with flowering plant density, reinforcing annual
variation in flower production (Kelly et al., 2001; Satake and
Iwasa, 2002). In contrast, a pollination Moran effect is an
exogenous, density independent, synchronising mechanism in
which pollination efficiency is driven by environmental factors
(Pearse et al., 2015b; Pesendorfer et al., 2016).
Recently, Koenig et al. (2015) formulated a hypothesis for a
mechanism underlying the pollination Moran effect, propos-
ing that weather is linked to seed production by its effect on
flowering synchrony and associated pollination efficiency. The
phenology synchrony hypothesis posits that interannual differ-
ences in spring weather determine the onset of flowering for
each plant. In years when weather conditions result in asyn-
chronous flowering, low flowering synchrony decreases pollen
availability and increases pollen limitation. In contrast, in
1
Department of Systematic Zoology, Faculty of Biology, Adam Mickiewicz
University, Pozna
n, Poland
2
Department of Forest and Soil Sciences, Institute of Forest Ecology, Univer-
sity of Natural Resources and Life Sciences, Vienna, Austria
3
Department of Biology, Tufts University, Medford, MA, USA
4
INDEHESA, Forest Research Group, University of Extremadura, Plasencia,
Spain
*Correspondence: E-mail: michalbogdziewicz@gmail.com
©2020 John Wiley & Sons Ltd.
Ecology Letters, (2020) doi: 10.1111/ele.13609
years when plants flower in synchrony with a high number of
other individuals, pollination failure is limited. Recently,
Pearse et al. (2015) showed that pollen addition in Quercus
lobata reduces female flower abortion rates, increasing seed
set and that this effect was limited to a subset of years. This
study demonstrated that pollen limitation varies between years
a key assumption of theoretical models but did not test
the potential drivers of this variation. Here, we expand on this
work and report the first experimental evaluation of pheno-
logical synchrony hypothesis as drivers of pollen limitation in
mast seeding trees.
We tested the phenological synchrony hypothesis using a
pollen addition experiment in Holm oak (Quercus ilex). In this
experiment, we compared effects of pollen supplementation
on trees that varied in their flowering synchrony with con-
specific trees. We hypothesised that pollen addition would
reverse the effects of spatial isolation and asynchronous flow-
ering on reproductive success. The experiment therefore
explicitly tests the causal link between flowering synchrony
and variation in reproductive success in a masting plant:
poorly synchronised flowering in certain years limits reproduc-
tive success of individual plants, leading to intermittent failure
and, by extension, to mast years. We also tested whether
effects of pollen supplementation differed with spatial isola-
tion of trees as a broad test for density dependence. Finally,
to better understand the dynamics of resource and pollen limi-
tation in this system, we compared the effects of seed set in
1 year on flowering in the next, and quantified the relative
contributions of differences in flower production and matura-
tion to differences in seed production among individual trees.
METHODS
Study system and site
We conducted our study in Malpartida de Plasencia, Extrema-
dura, located c. 200 km west of Madrid in Spain. Pollen sup-
plementation experiments were conducted on Las Carboneras
dehesa (39°56’29.2"N, 5°58’47.1"W), an oak savannah agroe-
cosystem resulting from the human use of Mediterranean for-
ests over centuries (Fig. S1). Tree clearing has produced
landscapes with oaks interspersed within a grassland matrix,
which are mainly used for ranching. Our site is occupied
solely by the broadleaved evergreen Holm oak (Quercus ilex
L.), the most widely distributed tree species in the Iberian
Peninsula. It inhabits a wide range of habitats but predomi-
nates in dry Mediterranean regions with strong summer
droughts. Q.ilex budburst takes place in late March and early
April. Flowering usually occurs in AprilMay and acorns
grow throughout the summer until early autumn. Past correla-
tive studies found that the duration of the pollen season, used
as an index of flowering synchrony, correlated negatively with
the acorn production, indicating that phenological synchrony
potentially plays vital role in shaping the interannual variation
in crop size in Q.ilex (Bogdziewicz et al., 2017). In this sys-
tem, summer drought often leads to severe pre-mature acorn
abscission (Espelta et al., 2008; Bogdziewicz et al., 2017),
which modulates the relationship between phenological syn-
chrony and acorn production.
Data collection
We conducted the pollen supplementation experiment with a
population of 81 marked Q.ilex trees in 2018 and 2019
(Fig. S1 & Fig. S2). At each plant, we selected two branches
facing south, and haphazardly assigned one branch to pollen-
supplementation and one to be a control. Previous work has
shown that within-plant comparisons may lead to overestima-
tion of pollen limitation when pollen-supplemented flowers
compete for resources with control flowers (Knight et al.,
2006). We attempted to minimise this effect by choosing
branches that were separated by at least 5 m of vascular tis-
sue. Because trees are often modular in their carbohydrate use
(Hoch, 2005; Han and Kabeya, 2017), these distant branches
are less likely to compete for resources than neighbouring
flowers on smaller plants (Pearse et al., 2015b). Experimental
studies performing defoliation, flower removal, branch gird-
ling and stable isotope analysis have reported that separate
branches behave as if autonomous for fruit maturation in at
least some trees species (Obeso, 1998; Hasegawa et al., 2003;
Sala et al., 2012). On pollen supplementation branches, we
individually marked three shoots and hand-pollinated flowers
(c. 2000 over the course of two years, median per shoot =3,
min =1, max =39) with a mix of conspecific pollen collected
from at least five local trees from outside the experimental
population. We added pollen when flowers were receptive,
that is when their stigmas were swollen and yellowish. Flowers
on each shoot received pollen supplementation twice with a
23-day break between additions. On control branches, we
marked three shoots and handled them in similar ways, but
did not apply hand-pollination. We visited all trees every 2
3 days, starting during the first week of flowering. At each
visit, we counted all female flowers on marked shoots, and
scored flowering phenology at the tree level by examining the
catkin stage (0 not active; 1up to 50% of the crown active;
3over 50% of the crown active; 4 spent). We used male
flowering as the measure of phenology because it was rela-
tively easy to quantify objectively on a large scale. The sur-
veys were continued until all trees finished shedding pollen.
We evaluated seed set on the marked shoots twice: in early
June to evaluate the effects of pollen addition before drought-
induced acorn abortion, and in mid-September, to evaluate
the cumulative effects of pollen addition and drought on seed
set.
We measured acorn production of individual trees in mid-
September by means of visual surveys in which two observers
(MB and RB) counted as many acorns as they could on each
tree in a 30-s period from two different orientations (south
and north). This acorn count method has been found to pro-
vide a good index of acorn availability under most conditions
(Koenig et al., 1994). The counts of acorns for each tree were
added together for the analysis. We measured diameter at
breast height of all trees in the experimental population in
2019 (mean =53.23, SD =8.33).
Statistical analysis
We quantified flowering synchrony as the mean pairwise over-
lap in flowering phenology among all individuals within the
©2020 John Wiley & Sons Ltd.
2M. Bogdziewicz et al. Letter
experimental population. We define flowering here as the time
during which plants are shedding pollen. Flowering synchrony
between each pair of plants was calculated using the number
of days both individuals were flowering divided by the num-
ber of days either individual was available for mating (see
Ison et al., 2014) in the mateable R package version 0.3.1
(Wagenius et al., 2020). To evaluate the effects of plant den-
sity on pollen limitation, we calculated local density of flower-
ing plants, that is, the number of conspecifics within a 50-m
radius (Fig. S1). This cut-off was based on past studies relat-
ing seed production to local plants density in oaks (Knapp
et al., 2001). Because the spatial scale at which density can
affect pollen limitation in trees is essentially unknown (Koenig
et al., 2017), we repeated this analysis using other cut-offs
(1070 m, with a 10-m step). Choice of cutoff distance did
not alter the conclusions and is not discussed further.
To evaluate the effect of flowering synchrony, conspecific
density and pollen addition on seed set, we built a generalised
linear mixed model (GLMM) with a binomial error distribu-
tion, logit link and tree ID as a random intercept. The
response variable was seed set, expressed as the proportion of
flowers that developed to acorns censused in June. As is stan-
dard in binomial GLMMs, the analysis was based on counts
of successes and failures, not calculated proportions. The
model included tree-level flowering synchrony (as described in
the previous paragraph) and density in an interaction with
treatment (pollen addition or control). We also included year
and tree diameter at breast height as covariates. We detected
overdispersion, and accounted for it by including an observa-
tion-level random intercept (Zuur et al., 2009). We arrived at
the final model by removing non-significant interaction terms.
We quantified the relative importance of flower production
and post-flowering processes (pollination and seed abortion)
for reproductive success of individual trees. This analysis used
a log-link, negative binomial GLMM, with tree ID as a ran-
dom intercept. The response variable was the tree-level visual
acorn count, noting that the log-link plays a similar role to log-
transformation. Fixed factors were flower abundance and the
proportion of flowers that successfully matured to acorns at the
branch level. We also included tree diameter at breast height as
covariate. For this analysis, the proportion of matured flowers
was calculated based only on control branches. We z-standard-
ised predictors to allow direct comparisons of effect sizes. All
statistics were run in R version 4.0.0. (R Core Team 2020), and
GLMMs were implemented via glmmTMB package 1.0.1.
(Brooks et al., 2017). Model checking revealed no temporal or
spatial autocorrelation of residuals. Because all our tests were
evaluations of continuous predictors or factors with two levels,
we evaluated statistical significance using the p-values from the
glmer.summary function.
RESULTS
In 2018, the flowering season started April 22nd and lasted until
May 2nd. In 2019, flowering onset was almost a month earlier
and started March 27th and finished April 26th (Fig. 1). In the
later and shorter 2018 season, flowering was highly synchronised
in most trees (mean synchrony SD: 0.49 0.13), whereas in
2019 flowering synchrony was lower (0.41 0.12, LMM with
tree ID as random intercept: v
2
=17.03, P<0.001). Temperature
in the early-flowering season (2019) was higher than in the late-
flowering season (2018; mean daily temperature in January-
March in 2018: 9.2 °C vs. 2019: 11.4 °C).
The proportion of flowers that developed into acorns was
significantly affected by flowering synchrony, suggesting
effects of among-tree variation in synchrony on pollen limita-
tion. In this statistical model, there was a significant interac-
tion of flowering synchrony and pollen addition (bSE:
5.13 1.43, z=3.59, P<0.001). Overlap in flowering phe-
nology increased seed set of control branches (regression
slope: bSE: 2.53 1.15, z=2.20, P=0.03), but decreased
seed set of pollen-supplemented branches (regression slope:
bSE: 2.65 1.21, z=2.19, P=0.03). Asynchronous
trees were severely pollen limited (seed set c. 23%) which was
relaxed after pollen supplementation (seed set ~69%)
(Fig. 2). Seed set of well-synchronised trees did not differ
between treatments, suggesting that some other factor become
more limiting in such plants. Seed set was higher in 2019
(47%) compared to 2018 (37%) (logit-scale group difference,
bSE: 0.40 0.21, z=1.96, P=0.05), while tree DBH had
no effect (regression slope, bSE =0.006 0.02, z=0.43,
P=0.71). The interaction term of tree density and treatment
was not statistically significant (P=0.49) and was removed
from the final model. Conspecific tree density was not a statis-
tically significant predictor of seed set (regression slope:
bSE =0.02 0.06, z=0.32, P=0.75).
Tree-level reproductive success (i.e. acorn crop size) was gen-
erally larger in trees that produced more flowers (regression
slope, bSE =0.27 0.07, z=3.44, P<0.001), and had
higher acorn maturation rates (i.e. the proportion of flowers
that reached full maturity) (bSE =0.24 0.07, z=3.09,
P<0.001). The effect sizes were comparable for both predic-
tors (Fig. 3). DBH had no effect on crop size, possibly because
of relatively small among-tree variation in size (regression slope,
bSE =0.02 0.07, z=0.28, P=0.78).
DISCUSSION
Our study demonstrates the causal link between flowering syn-
chrony and seed set of masting trees, as proposed by the pheno-
logical synchrony hypothesis. Natural variation in flowering
synchrony resulted in pollen limitation for asynchronous trees,
reducing seed set to half the seed set of synchronous trees.
Experimental pollen addition reversed this pollen limitation,
resulting in high pollination success, even in asynchronous
trees. Conspecific density, another potential driver of pollen
availability, did not correlate with pollination success. Thus,
this research provides the first experimental evidence that pollen
limitation due to asynchronous flowering reduces seed set, a key
assumption of the phenological synchrony hypothesis. This
hypothesis integrates environmental conditions and pollen
dynamics, and therefore brings together the two major factors
thought to influence synchrony of interannual variation in seed
production in species which gain an economy of scale from
wind pollination efficiency (Kelly & Sork 2002; Koenig et al.,
2015). In addition, the results support the notion that phenolog-
ical synchrony of flowering, rather than density dependence,
was the driver of pollen limitation in our study.
©2020 John Wiley & Sons Ltd.
Letter 3
Interannual variation in masting is synchronised in popula-
tions thousands of kilometres distant a pattern that is
strongly linked to synchrony in regional weather patterns
(Koenig and Knops, 1998; Vacchiano et al., 2017; LaMon-
tagne et al., 2020). Weather can synchronise seed production
through at least two mechanisms: (1) environmental cues that
induce changes in plant physiology and subsequently regulate
flower production and maturation (Kelly et al., 2013), and (2)
direct abiotic effects on population-wide pollen limitation
(Pearse et al., 2016; Pesendorfer et al., 2016; Bogdziewicz
et al., 2020a). Our study provides unique experimental sup-
port for the latter, indicating that flowering synchrony effects
of weather regulate pollen limitation in mast-seeding oaks.
The importance of phenological synchrony in mast seeding is
interesting because changes in the timing of flowering and
leaf-out phenology are among the most conspicuous finger-
prints of climate change in temperate forests (Fu et al., 2015,
2019; Renner and Zohner, 2018). Most of these studies focus
on changes in the average or onset of phenological events,
with less emphasis on changes in the length of flowering peri-
ods or changes in variation among individuals within popula-
tions (Zohner et al., 2018). Our results suggest that the nature
of changes in flowering phenology can be a critical component
to patterns of mast-seeding in trees, with subsequent cascad-
ing effects on consumer communities (Ostfeld and Keesing,
2000; Touzot et al. 2020).
Flower production was a key determinant of crop size in Q.
ilex, along with seed set. Therefore, pollination alone is not
Figure 1 Flowering onset and flowering synchrony during the study years. Flowering synchrony between each pair of plants was based on the number of
days both individuals were flowering divided by the number of days either individual was flowering. Spatial distribution of differently synchronised trees is
given in Figure S2.
Figure 2 Asynchronous trees are pollen limited, which is removed by pollen supplementation (a). Tree spatial isolation had no effect on pollen limitation
(b). The lines are based on significant GLMM predictions, and the shading indicates the 95% confidence intervals. Pollination success is the flower to
acorn transition rate, and points are the per-branch, per-year means of 81 Quercus ilex trees.
©2020 John Wiley & Sons Ltd.
4M. Bogdziewicz et al. Letter
sufficient to explain mast seeding. Understanding factors con-
trolling interannual variation in flower production is a neces-
sary next research step. Interannual variation in flower
production can be a product of large seasonal deviations from
mean weather values, which trigger changes in flowering gene
expression and associated hormone synthesis responsible for
initiating bud formation and flower induction (weather cuing
hypothesis; Kelly et al., 2013; Satake et al., 2019). Alterna-
tively, the resource budget hypothesis predicts that seed pro-
duction depletes resources, limiting allocation to flowering in
the following year (Isagi et al., 1997; Sala et al., 2012). These
hypotheses are not mutually exclusive in that resource levels
can control gene expression and hormone secretion at the
same time (Miyazaki et al., 2014). Previously, we fit resource
budget models to a time series of Q.ilex seed production pat-
terns (Bogdziewicz et al., 2019). This analysis indicated that
resource depletion was not important in determining interan-
nual variation in Q.ilex crop size. Our short-term data from
this study also indicate a positive correlation between crop
size in 1 year and flower production in the following year
(Online Appendix, Figure S3); we would expect the opposite
pattern if reproduction strongly depleted stored resources. It
would be fascinating to manipulate hormonal levels in plant
organs, perhaps in combination with experimental flower
removal, to explicitly evaluate hormonal cueing vs. resource
depletion as mechanisms of supra-annual reproduction within
individual plants (Turnbull et al., 2012). Oaks are ‘fruit matu-
ration’ species, in which fruit abortion is expected to be key
driver of masting variation Compared to oaks, interannual
variation in flower production should be much stronger in
‘flowering masting’ species in which annual variability in seed-
ing is primarily driven by differences in flower production
(e.g. Fagus,Chionochloa; Kelly et al., 2001; Abe et al., 2016).
Our results are consistent with models of mast seeding that
implicate pollen limitation as a factor that synchronises seed set
(Crone and Rapp, 2014; Pearse et al., 2016; Pesendorfer et al.,
2016). Regardless of specific assumptions, nearly all models of
mast-seeding require a mechanism for coupling seed production
of nearby plants (Satake and Iwasa, 2000; Lyles et al., 2015;
Noble et al., 2018). Interestingly, the spatial scales of coupling
seem to differ dramatically among systems (Koenig and Ashley,
2003; Noble et al., 2018). Pollination synchrony has the poten-
tial to be such a mechanism, and further exploration of the spa-
tial scales of factors that determine both flowering synchrony
and pollen dispersal could be a valuable avenue for future
research. So far, studies of oaks in California imply that pheno-
logical synchrony can be an important factor synchronising
masting at local spatial scales (Koenig et al., 2017), and that the
effective pollen transfer is mostly local (Knapp et al., 2001; Sork
et al., 2002). Another broad implication of our results is that a
single season with pollen limitation does not necessarily reduce
plant fitness. In fact, if seed failure in some years allows plants
to reproduce more in the next year, then pollination failure
could help synchronise reproduction and increase plant fitness.
Thus, pollen limitation could have evolved as a mechanism to
synchronise reproduction and enhance overall fitness through
mast-seeding and its associated economies of scale, that is
decreased seed predation and increased pollination efficiency in
mast years (Bogdziewicz et al., 2020b, 2020c).
Pollen addition increased seed set in asynchronous oaks more
strongly than in synchronous oaks (c. 70% vs. c. 50% respec-
tively). This difference indicates that, in addition to pollen limita-
tion, synchrony is correlated with another factor limiting seed
set. Flowering onset of asynchronous trees was delayed com-
pared to synchronous ones (Online Appendix, Figure S4). One
hypothesis is that early trees suffered more folivore damage,
Figure 3 Acorn production is determined by flower abundance and their maturation rate. (a) Average number of flowers, successfully pollinated flowers and
matured acorns. (b) The lines at (b) and (c) are based on significant GLMM predictions, and the shading indicates the 95% confidence intervals. Points are
the per-branch, per-year observations of 81 Quercus ilex trees.
©2020 John Wiley & Sons Ltd.
Letter 5
which could decrease their photosynthetic capacity and limit seed
set. In support of this hypothesis, in one past study, Quercus
lobata individuals with earlier budburst suffered more leaf dam-
age, which reduced their seed production (Pearse et al., 2015a).
Past experiments in our study system indicated that insect her-
bivory can decrease Q.ilex seed set by half (Canelo et al., 2018).
Early trees gain the advantage of reduced pollen limitation, but
may suffer reduced seed set due to other factors, such as her-
bivory. The relationship between plant phenology and plantfoli-
vore interactions is increasingly of interest, because climate
warming can shift the phenology of plants and their folivores
(Singer and Parmesan, 2010). These shifts in phenology may also
prove crucial to our understanding of masting dynamics.
The capacity of future forests to support biodiversity and deli-
ver ecosystem services will depend on the ability of seed produc-
tion to allow plant ranges to track climate change (LaDeau and
Clark, 2001; Ib
a~
nez et al., 2009; McDowell et al., 2020). How-
ever, fecundity is the only major demographic process that lacks
field-based estimates in models of global vegetation change
(McDowell et al., 2020). The sensitive dependence of pollination
effects on synchrony implies complex interactions among phenol-
ogy, pollination and herbivory. This complexity is daunting in
the context of predicting effects of climate change on plant fecun-
dity, and points to the importance of actions to mitigate climate
change. Our study is an important step towards process-based
understanding of links between climate and plant fecundity, that
can subsequently be incorporated into broader ecosystem-scale
models to aid predictions of vegetation dynamics.
ACKNOWLEDGMENTS
I dedicate this work to my beloved father (M.B.). We thank
Dave Kelly and two Anonymous Reviewers for their construc-
tive comments on the earlier version of the text. We thank
Agnieszka Amborska-Bogdziewicz for invaluable help during
field work. The study was supported by the Polish National
Science Centre grants Sonatina no. 2017/24/C/NZ8/00151
(MB), and the MICNN project AGL2014-54739-R (RB).
CONFLICT OF INTEREST
The authors declare no conflict of interests.
AUTHOR CONTRIBUTIONS
All authors designed the study. MB and RB ran the experi-
ments. MB analysed the data and drafter the manuscript. All
authors contributed critically to the interpretation of the
results and text revisions.
PEER REVIEW
The peer review history for this article is available at https://
publons.com/publon/10.1111/ele.13609.
DATA AVAILABILITY STATEMENT
Data available from the Dryad Digital Repository: https://d
oi.org/10.5061/dryad.sn02v6x2b.
REFERENCES
Abe, T., Tachiki, Y., Kon, H., Nagasaka, A., Onodera, K., Minamino,
K. et al. (2016). Parameterisation and validation of a resource budget
model for masting using spatiotemporal flowering data of individual
trees. Ecol. Lett., 19, 11291139.
Bogdziewicz, M., Ascoli, D., Hacket-Pain, A., Koenig, W.D., Pearse, I.,
Pesendorfer, M. et al. (2020a). From theory to experiments for testing
the proximate mechanisms of mast seeding: an agenda for an
experimental ecology. Ecol. Lett., 23, 210220.
Bogdziewicz, M., Fern
andez-Mart
ınez, M., Bonal, R., Belmonte, J. &
Espelta, J.M. (2017). The Moran effect and environmental vetoes:
phenological synchrony and drought drive seed production in a
Mediterranean oak. Proceedings of the Royal Society B: Biological
Sciences, 284, 20171784.
Bogdziewicz, M., Kelly, D., Tanentzap, A.J., Thomas, P.A., Lageard,
J.G.A. & Hacket-Pain, A. (2020b). Climate change strengthens
selection for mast seeding in european beech. Curr. Biol., 30(17), 3477
3483. https://doi.org/10.1016/j.cub.2020.06.056.
Bogdziewicz, M., Steele, M.A., Marino, S. & Crone, E.E. (2018).
Correlated seed failure as an environmental veto to synchronize
reproduction of masting plants. New Phytol., 219, 98108.
Bogdziewicz, M., Szymkowiak, J., Tanentzap, A.J., Calama, R., Marino,
S., Steele, M.A. et al. (2020c). Seed predation selects for reproductive
variability and synchrony in perennial plants. New Phytol., 10.1111/
nph.16835.
Bogdziewicz, M., Zwolak, R. & Crone, E.E. (2016). How do vertebrates
respond to mast seeding? Oikos, 125, 300307.
Bogdziewicz, M., _
Zywiec, M., Espelta, J.M., Fern
andez-Martinez, M.,
Calama, R., Ledwo
n, M. et al. (2019). Environmental veto synchronizes
mast seeding in four contrasting tree species. Am. Nat., 194, 246259.
Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg,
C.W., Nielsen, A. et al. (2017). glmmTMB balances speed and
flexibility among packages for zero-inflated generalized linear mixed
modeling. The R journal, 9, 378400.
Canelo, T., Gayt
an,
A., Gonz
alez-Bornay, G. & Bonal, R. (2018). Seed loss
before seed predation: experimental evidence of the negative effects of leaf
feeding insects on acorn production. Integrative Zoology, 13, 238250.
Clark, J.S., Nu~
nez, C.L. & Tomasek, B. (2019). Foodwebs based on
unreliable foundations: spatiotemporal masting merged with consumer
movement, storage, and diet. Ecol. Monogr., 89, e01381.
Crone, E.E., Miller, E. & Sala, A. (2009). How do plants know when
other plants are flowering? Resource depletion, pollen limitation and
mast-seeding in a perennial wildflower. Ecol. Lett., 12, 11191126.
Crone, E.E., Polansky, L. & Lesica, P. (2005). Empirical models of pollen
limitation, resource acquisition, and mast seeding by a bee-pollinated
wildflower. Am. Nat., 166, 396408.
Crone, E.E. & Rapp, J.M. (2014). Resource depletion, pollen coupling,
and the ecology of mast seeding. Ann. N. Y. Acad. Sci., 1322, 2134.
Espelta, J.M., Cort
es, P., Molowny-Horas, R., S
anchez-Humanes, B. &
Retana, J. (2008). Masting mediated by summer drought reduces acorn
predation in Mediterranean oak forests. Ecology, 89, 805817.
Fu, Y.H., Zhang, X., Piao, S., Hao, F., Geng, X., Vitasse, Y. et al.
(2019). Daylength helps temperate deciduous trees to leaf-out at the
optimal time. Glob. Change Biol., 25, 24102418.
Fu, Y.H., Zhao, H., Piao, S., Peaucelle, M., Peng, S., Zhou, G. et al.
(2015). Declining global warming effects on the phenology of spring
leaf unfolding. Nature, 526, 104107.
Han, Q. & Kabeya, D. (2017). Recent developments in understanding
mast seeding in relation to dynamics of carbon and nitrogen resources
in temperate trees. Ecol. Res., 32, 771778.
Hasegawa, S., Koba, K., Tayasu, I., Takeda, H. & Haga, H. (2003).
Carbon autonomy of reproductive shoots of Siberian alder (Alnus
hirsuta var. sibirica). J Plant Res, 116, 183188.
Hoch, G. (2005). Fruit-bearing branchlets are carbon autonomous in mature
broad-leaved temperate forest trees. Plant, Cell Environ., 28, 651659.
Ib
a~
nez, I., Clark, J.S. & Dietze, M.C. (2009). Estimating colonization
potential of migrant tree species. Glob. Change Biol., 15, 11731188.
©2020 John Wiley & Sons Ltd.
6M. Bogdziewicz et al. Letter
Isagi, Y., Sugimura, K., Sumida, A. & Ito, H. (1997). How does masting
happen and synchronize? J. Theor. Biol., 187, 231239.
Ison, J.L., Wagenius, S., Reitz, D. & Ashley, M.V. (2014). Mating between
Echinacea angustifolia (Asteraceae) individuals increases with their
flowering synchrony and spatial proximity. Am. J. Bot., 101, 180189.
Kelly, D., Geldenhuis, A., James, A., Penelope Holland, E., Plank, M.J.,
Brockie, R.E. et al. (2013). Of mast and mean: differential-temperature cue
makes mast seeding insensitive to climate change. Ecol. Lett.,16,9098.
Kelly, D., Hart, D.E. & Allen, R.B. (2001). Evaluating the wind
pollination benefits of mast seeding. Ecology, 82, 117126.
Kelly, D. & Sork, V.L. (2002). Mast seeding in perennial plants: why,
how, where? Annu. Rev. Ecol. Evol. Syst., 33(1), 427447.
Knapp, E.E., Goedde, M.A. & Rice, K.J. (2001). Pollen-limited
reproduction in blue oak: implications for wind pollination in
fragmented populations. Oecologia, 128, 4855.
Knight, T.M., Steets, J.A. & Ashman, T.-L. (2006). A quantitative
synthesis of pollen supplementation experiments highlights the
contribution of resource reallocation to estimates of pollen limitation.
Am. J. Bot., 93, 271277.
Koenig, W.D. & Ashley, M.V. (2003). Is pollen limited? The answer is
blowin’ in the wind. Trends Ecol. Evol., 18, 157159.
Koenig, W.D. & Knops, J.M. (1998). Scale of mast-seeding and tree-ring
growth. Nature, 396, 225.
Koenig, W.D., Knops, J.M., Carmen, W.J. & Pearse, I.S. (2015). What drives
masting? The phenological synchrony hypothesis. Ecology, 96, 184192.
Koenig, W.D., Knops, J.M.H., Carmen, W.J., Stanback, M.T. &
Mumme, R.L. (1994). Estimating acorn crops using visual surveys.
Can. J. For. Res., 24, 21052112.
Koenig, W.D., Knops, J.M.H., Pesendorfer, M.B., Zaya, D.N. & Ashley,
M.V. (2017). Drivers of synchrony of acorn production in the valley
oak (Quercus lobata) at two spatial scales. Ecology, 98, 30563062.
LaDeau, S.L. & Clark, J.S. (2001). Rising CO2 levels and the fecundity of
forest trees. Science, 292, 9598.
LaMontagne, J.M., Pearse, I.S., Greene, D.F. & Koenig, W.D. (2020).
Mast seeding patterns are asynchronous at a continental scale. Nature
Plants, 6(5), 460465.
Lyles, D., Rosenstock, T.S. & Hastings, A. (2015). Plant reproduction and
environmental noise: How do plants do it? J. Theor. Biol., 371, 137144.
McDowell, N.G., Allen, C.D., Anderson-Teixeira, K., Aukema, B.H.,
Bond-Lamberty, B., Chini, L. et al. (2020). Pervasive shifts in forest
dynamics in a changing world. Science, 368.
Miyazaki, Y., Maruyama, Y., Chiba, Y., Kobayashi, M.J., Joseph, B.,
Shimizu, K.K. et al. (2014). Nitrogen as a key regulator of flowering in
Fagus crenata: understanding the physiological mechanism of masting
by gene expression analysis. Ecol. Lett., 17, 12991309.
Noble, A.E., Rosenstock, T.S., Brown, P.H., Machta, J. & Hastings, A.
(2018). Spatial patterns of tree yield explained by endogenous forces
through a correspondence between the Ising model and ecology. PNAS,
115, 18251830.
Obeso, J.R. (1998). Effects of defoliation and girdling on fruit production
in Ilex aquifolium. Funct. Ecol., 12, 486491.
Ostfeld, R.S. & Keesing, F. (2000). Pulsed resources and community
dynamics of consumers in terrestrial ecosystems. Trends Ecol. Evol., 15,
232237.
Pearse, I.S., Funk, K.A., Kraft, T.S. & Koenig, W.D. (2015a). Lagged
effects of early-season herbivores on valley oak fecundity. Oecologia,
178, 361368.
Pearse, I.S., Koenig, W.D., Funk, K.A. & Pesendorfer, M.B. (2015b).
Pollen limitation and flower abortion in a wind-pollinated, masting
tree. Ecology, 96, 587593.
Pearse, I.S., Koenig, W.D. & Kelly, D. (2016). Mechanisms of mast seeding:
resources, weather, cues, and selection. New Phytol.,212,546562.
Pesendorfer, M.B., Koenig, W.D., Pearse, I.S., Knops, J.M.H. & Funk,
K.A. (2016). Individual resource limitation combined with population-
wide pollen availability drives masting in the valley oak (Quercus
lobata). J. Ecol., 104, 637645.
Rees, M., Kelly, D. & Bjørnstad, O.N. (2002). Snow tussocks, chaos, and
the evolution of mast seeding. Am. Nat., 160, 4459.
Renner, S.S. & Zohner, C.M. (2018). Climate change and phenological
mismatch in trophic interactions among plants, insects, and vertebrates.
Annu. Rev. Ecol. Evol. Syst., 49, 165182.
Sala, A., Hopping, K., McIntire, E.J.B., Delzon, S. & Crone, E.E. (2012).
Masting in whitebark pine (Pinus albicaulis) depletes stored nutrients.
New Phytol., 196, 189199.
Satake, A. & Iwasa, Y. (2000). Pollen coupling of forest trees: forming
synchronized and periodic reproduction out of chaos. J. Theor. Biol.,
203, 6384.
Satake, A. & Iwasa, Y. (2002). Spatially limited pollen exchange and a
long-range synchronization of trees. Ecology, 83, 9931005.
Satake, A., Kawatsu, K., Teshima, K., Kabeya, D. & Han, Q. (2019).
Field transcriptome revealed a novel relationship between nitrate
transport and flowering in Japanese beech. Sci. Rep.,9,112.
Schermer,
E., Bel-Venner, M.-C., Fouchet, D., Siberchicot, A., Boulanger,
V., Caignard, T. et al. (2019). Pollen limitation as a main driver of
fruiting dynamics in oak populations. Ecol. Lett., 22, 98107.
Singer, M.C. & Parmesan, C. (2010). Phenological asynchrony between
herbivorous insects and their hosts: signal of climate change or pre-
existing adaptive strategy? Philosophical Transactions of the Royal
Society B: Biological Sciences, 365, 31613176.
Smaill, S.J., Clinton, P.W., Allen, R.B. & Davis, M.R. (2011). Climate
cues and resources interact to determine seed production by a masting
species. J. Ecol., 99, 870877.
Sork, V.L., Davis, F.W., Smouse, P.E., Apsit, V.J., Dyer, R.J.,
Fernandez-M, J.F. et al. (2002). Pollen movement in declining
populations of California Valley oak, Quercus lobata: where have all
the fathers gone? Mol. Ecol., 11, 16571668.
Touzot, L., Schermer,
E., Venner, S., Delzon, S., Rousset, C., Baubet,
E.
et al. (2020). How does increasing mast seeding frequency affect
population dynamics of seed consumers? Wild boar as a case study.
Ecol. Appl., 30(6), e02134.
Turnbull, M.H., Pharis, R.P., Kurepin, L.V., Sarfati, M., Mander, L.N.
& Kelly, D. (2012). Flowering in snow tussock (Chionochloa spp.) is
influenced by temperature and hormonal cues. Functional Plant Biol.,
39, 3850.
Vacchiano, G., Hacket-Pain, A., Turco, M., Motta, R., Maringer, J.,
Conedera, M. et al. (2017). Spatial patterns and broad-scale weather
cues of beech mast seeding in Europe. New Phytol., 215, 595608.
Wagenius, S., Beck, J. & Kiefer, G. (2020). Fire synchronizes flowering
and boosts reproduction in a widespread but declining prairie species.
PNAS, 117, 30003005.
Zohner, C.M., Mo, L. & Renner, S.S. (2018). Global warming reduces
leaf-out and flowering synchrony among individuals. eLife, 7, e40214.
Zuur, A., Ieno, E.N., Walker, N., Saveliev, A.A. & Smith, G.M. (2009).
Mixed Effects Models and Extensions in Ecology with R. Springer-
Verlag , New York.
SUPPORTING INFORMATION
Additional supporting information may be found online in
the Supporting Information section at the end of the article.
Editor, Richard Ostfeld
Manuscript received 8 July 2020
First decision made 16 August 2020
Manuscript accepted 24 August 2020
©2020 John Wiley & Sons Ltd.
Letter 7
... Our findings of S p to decreased precipitation in the three temperate steppes could fill the above critical knowledge gap and provide vital evidence for the improvement of future model prediction. In addition, the significant differences in S p to decreased precipitation among the three steppes imply that spatial heterogeneity of flowering phenology would be amplified under drought, which could favor the interactions between plants and pollinators and thus promote the pollination and reproductive success under low water availability at the regional scale (Lawson and Rand, 2019;Bogdziewicz et al., 2020;Ettinger et al., 2022). By contrast, no differences in S p to increased precipitation among the three steppes observed in this study suggest a convergence of flowering sensitivities under higher precipitation in temperate steppes with different soil water availabilities. ...
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... Bogdziewiczet al. (2020a) investigated drivers of seed production for three European wind pollinated tree species and identified pollen abundance as the best predictor. They also linked pollen abundance to warm preceding summers and short pollen season to warm spring temperatures (Bogdziewicz et al., 2020b). Future impacts on flowering and pollination can be expected but it remains unclear to which extent and in which direction, as some species may regenerate prolifically while others retreat (cf. ...
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... They found that wind-pollinated taxa, not insect-pollinated ones, tend to bear fruits massively only during some years. Their results comfort previous findings showing that masting is more common and more pronounced in wind-pollinated taxa than in animal-pollinated taxa (Kelly and Sork 2002;Bogdziewicz et al. 2020). In the study of Garcia et al. (2021), chestnut was an outlier, because it had one of the lowest coefficient of variation for yield across years, a characteristic typical of animalpollinated taxa. ...
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... At time intervals plant populations in a wider area spend these resources in highly synchronous mass reproduction (Koenig et al., 2015). Masting is typical for many wind-pollinated woody species (Pearse et al., 2016) including Betula, Quercus, and Fraxinus (Bogdziewicz et al., 2020;Dahl et al., 2013;Dahl & Strandhede, 1996;Tapper, 1992). The correlation of weather with synchronous fluctuations in pollination success of isolated populations (known as pollination Moran effect) acts on individuals of the same taxon but also across taxa and ecosystems (Hansen et al., 2020;Pearse et al., 2016). ...
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Information on the allergenic pollen season provides insight on the state of the environment of a region and facilitates allergy symptom management. We present a retrospective analysis of the duration and severity of the allergenic pollen season and the role of meteorological factors in Istanbul, Turkey. Aerobiological sampling from January 2013 to June 2016, pollen identification and counting followed current standard methodology. Pollen seasons were defined according to 95% of the Annual Pollen Integral (APIn) and the season start date was compared with the first day of 5 day consecutive non-zero records. Generalized additive models (GAMs) were created to study the effect of meteorological factors on flowering. The main pollen contributors were taxa of temperate and Mediterranean climates, and neophytic Ambrosia . Cupressaceae, Poaceae, Pinaceae, Quercus and Ambrosia had the greatest relative abundance. The pollen season defined on 95% of the APIn was adequate for our location with total APIns around 10.000 pollen*day*m ⁻³ . Woody taxa had generally shorter seasons than herbaceous taxa. In trees, we see precipitation as the main limiting factor for assimilate production prior to anthesis. A severe tree pollen season in 2016 suggests intense synchronous flowering across taxa and populations triggered by favourable water supply in the preceding year. GAM models can explain the effect of weather on pollen concentrations during anthesis. Under the climatic conditions over the study period, temperature had a negative effect on spring flowering trees, and a positive one on summer flowering weeds. Humidity, atmospheric pressure and precipitation had a negative effect on weeds. Our findings contribute to environmental and allergological knowledge in southern Europe and Turkey with relevancy in the assessment of impacts of climate change and the management of allergic disease.
... Fire appears to stimulate flowering in many plant species in fire-prone habitats (Ehrenreich & Aikman, 1963;Pemble et al., 1981;Hartnett, 1990;Peter, 2002a,b;Pilon et al., 2018;Zirondi et al., 2021), as we found in L. aspera (Table 1). Synchronized flowering, which we conceptualize as a continuous trait, at least in perennial prairie species, may be an adaptive trait, as posited for masting species (Janzen, 1971;Bogdziewicz et al., 2020Bogdziewicz et al., , 2021Kelly, 2021). However, studies quantifying fire effects on flowering synchrony and reproduction are still rare and warrant further investigation. ...
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... Flowering phenology plays a critical role in plant reproductive success (Bogdziewicz et al., 2020;Elzinga et al., 2007;Waters et al., 2020), species fitness (Lázaro et al., 2020;Zhao et al., 2020), and plant-pollinator interactions (Hegland et al., 2009;Kharouba et al., 2018Kharouba et al., , 2020Maglianesi et al., 2020), and consequently has a substantial impact on ecosystem structure and function (Burkle et al., 2013;CaraDonna et al., 2014;Cleland et al., 2007;Peñuelas and Filella, 2001). As an important component of flowering phenology, the flowering season can affect fruit production of plant species, and thus disrupt reproductive rhythms, as well as interactions between plants and pollinators (CaraDonna et al., 2014;Høye et al., 2013;Miller-Rushing and Inouye, 2009;Rafferty et al., 2016). ...
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... This adaptation has evolved separately many times across the plant Tree of Life (ToL) [3][4][5], because it can ultimately increase fitness by conferring economies of scale that reduce the costs of reproduction per surviving offspring [2]. Masting is selected by different pressures [2], such as pollination efficiency [6,7] or predator satiation [8][9][10][11][12]. However, little is known about whether it changes evolutionary processes across species, that is macroevolution, defined by rates of speciation, extinction and phenotypic evolution. ...
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Masting characterizes large, intermittent and highly synchronous seeding events among individual plants and is found throughout the plant Tree of Life (ToL). Although masting can increase plant fitness, little is known about whether it results in evolutionary changes across entire clades, such as by promoting speciation or enhanced trait selection. Here, we tested if masting has macroevolutionary consequences by combining the largest existing dataset of population-level reproductive time series and time-calibrated phylogenetic tree of vascular plants. We found that the coefficient of variation (CV p ) of reproductive output for 307 species covaried with evolutionary history, and more so within clades than expected by random. Speciation rates estimated at the species level were highest at intermediate values of CV p and regional-scale synchrony (S r ) in seed production, that is, there were unimodal correlations. There was no support for monotonic correlations between either CV p or S r and rates of speciation or seed size evolution. These results were robust to different sampling decisions, and we found little bias in our dataset compared with the wider plant ToL. While masting is often adaptive and encompasses a rich diversity of reproductive behaviours, we suggest it may have few consequences beyond the species level. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.
... This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'. temperate regions where wind is the predominant pollination syndrome among forest trees [4,[10][11][12]. Early reviews on whether pollination syndrome predicts the tendency for masting had difficulty gathering sufficient data on insectpollinated and animal-dispersed taxa [5,6]. ...
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Cyclical fluctuations in reproductive output are widespread among perennial plants, from multi-year masting cycles in forest trees to alternate bearing in horticultural crops. In natural systems, ecological drivers such as climate and pollen limitation can result in synchrony among plants. Agricultural practices are generally assumed to outweigh ecological drivers that might synchronize alternate-bearing individuals, but this assumption has not been rigorously assessed and little is known about the role of pollen limitation as a driver of synchrony in alternate-bearing crops. We tested whether alternate-bearing perennial crops show signs of alternate bearing at a national scale and whether the magnitude of national-scale alternate bearing differs across pollination syndromes. We analysed the Food and Agriculture Organization of the United Nations time series (1961–2018) of national crop yields across the top-producing countries of 27 alternate-bearing taxa, 6 wind-pollinated and 21 insect-pollinated. Alternate bearing was common in these national data and more pronounced in wind-pollinated taxa, which exhibited a more negative lag-1 autocorrelation and a higher coefficient of variation (CV). We highlight the mutual benefits of integrating ecological theory and agricultural data for (i) advancing our understanding of perennial plant reproduction across time, space and taxa, and (ii) promoting stable farmer livelihoods and global food supply. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.
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In plants, processes from flowering to seed maturation are influenced by various factors, including weather conditions, resource supply, and damage inflicted by seed predators, that collectively contribute to annual variability in seed production. To identify the important factors associated with sound acorn production in Quercus serrata, from 2014 to 2020, we investigated the demographic processes from flowering to acorn maturation in six individual trees within a stand in a warm‐temperate secondary forest in western Japan. We found that the annual production of female flowers was positively correlated with the difference in April temperatures between successive years. However, their fluctuation was low and unaffected by either seed or flower production in the previous year. Compared with those of female flowers, the annual variability in sound acorn production within an individual was significantly higher and more synchronized. Key factor analyses revealed that reproductive losses due to the oviposition and sap‐sucking activities of Mechoris ursulus were the most prominent factors contributing to the observed annual variation in total predispersal losses at an individual level, and their effects were synchronized among individuals within a population. Survival from female flowering to sound acorn maturation was strongly predicted by the temperature in June, which corresponds to the period of adult M. ursulus emergence. Our findings indicate that the damage inflicted by the main seed predator during the predispersal stage can sufficiently regulate the sound acorn production patterns in Q. serrata that appear to resemble masting behavior (the highly variable and synchronized production of acorns within individuals). Annual variability in the number of (a) female flowers and (b) sound acorns for each individual trees within a stand. Compared with those of female flowers, the annual variability in sound acorn production within an individual was significantly higher and more synchronized, implying that synchronized abortion among individuals occurs until acorn maturation.
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Mast flowering and seeding is a well-known reproductive strategy of tree species with many ecological consequences regulating synchronous year-to-year flowering intensity variations at the population level. In contrast to flowering timing, the effects of climate change on flowering intensity across space, time, and species are largely unexplored. In this study, a long-term data set on flowering intensities for eight common tree species (Alnus glutinosa, Fagus sylvatica, Larix decidua, Picea abies, Pinus sylvestris, Pseudotsuga menziesii, Quercus petraea, and Quercus robur) in Germany was reassembled to analyse flowering mechanisms and strategies by applying GAMLSS (Generalised Additive Models for Location Scale and Shape) models together with climatic data (temperature, precipitation, and drought) and various time-lagged effects. All species showed increasing flowering intensities in the period 1954–2019. The flowering intensity of Larix and Pinus differed significantly across their respective ecological provenances. Time series revealed higher synchrony among broadleaf than conifer species, although correlation coefficients of both their flowering intensities generally increased over time. GAMLSS modelling mainly explained flowering intensities well, with R² ranging between 0.58 (Pseudotsuga) and 0.25 (Alnus). Flowering intensity of almost all species was significantly influenced by flowering in previous years, indicating autocorrelative influences pointing to resource depletion and accumulation. Growing season temperature was modelled to be the main factor among weather cues, with the general pattern of flower masting being correlated negatively with temperature two years before masting and positively with temperature one year before masting. In addition, the short-term drought estimated by Standardised Precipitation-Evapotranspiration Index (12 months) increased flowering intensity in almost all cases. Therefore, it can be inferred that the heavy flowering of European common tree species has been regulated by sufficient resources and prevailing optimal climatic conditions.
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Full-text available
Annually variable and synchronous seed production by plant populations, or masting, is a widespread reproductive strategy in long-lived plants. Masting is thought to be selectively beneficial because inter-annual variability and synchrony increase the fitness of plants through economies of scale that decrease the cost of reproduction per surviving offspring. Predator satiation is believed to be a key economy of scale, but whether it can drive phenotypic evolution for masting in plants has been rarely explored.  We used data from seven plant species (Quercus humilis, Q. ilex, Q. rubra, Q. alba, Q. montana, Sorbus aucuparia, and Pinus pinea) to determine whether pre-dispersal seed predation selects for plant phenotypes that mast.  Predation selected for inter-annual variability in Mediterranean oaks (Q. humilis and Q. ilex), for synchrony in Q. rubra, and for both inter-annual variability and reproductive synchrony in S. aucuparia and P. pinea. Predation never selected for negative temporal autocorrelation of seed production.  Predation by invertebrates appears to select for only some aspects of masting, most importantly high CVi, supporting individual-level benefits of the population-level phenomenon of mast seeding. Determining the selective benefits of masting is complex because of interactions with other seed predators, which may impose contradictory selective pressures.
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Mast‐fruiting trees represent a pulsed resource that both supports and destabilizes consumer populations. Whereas a reliable resource is abundant on average and with limited variation in time and space, masting is volatile and localized, and that variability ramifies throughout food webs. Theory is developed to evaluate how the space‐time structure of masting interacts with consumers who exploit alternative hosts, forage widely in space, and store reserves in time. We derive the space‐time‐species covariance in resource supply and combine it with the space‐time‐diet breadth of consumers, or ambit. Direct connection to data is made possible with Mast Inference and Forecasting (MASTIF), a state‐space autoregressive model that fits seed‐trap and canopy observations and predicts resource availability within the canopy and on the forest floor with full uncertainty. A resource score can be assigned to each consumer‐habitat combination that integrates the benefits of a high mean supply weighed against the variance cost. As the consumer ambit increases, the volatility of an unreliable resource shifts from a variance‐cost to a mean‐benefit. Consumers foraging in the canopy (arboreal arthropods and rodents, song birds) experience space‐time covariance between host trees. Consumers on the forest floor (seed and damping‐off fungi, arthropods, rodents, ground‐nesting birds, mammals) experience instead a redistribution of that covariance by dispersal. For consumers lacking mobility, demographic storage in the form of episodic birth cohorts following mast years is important for population persistence. Consumers additionally compensate volatility with diet breadth. Depending on the dominant masting strategies of host tree species in the diet, habitats differentially limit consumers depending on the misalignment be tween consumer ambit and spatio‐temporal covariance of hosts. The impact of adding or subtracting a diet item can be gauged with the standard error (SE) rule, the benefit of an added diet item balanced against the variance cost, both of which depend on the existing diet, the abundance of the new host, and the consumer's foraging ambit. Results rank habitats by their capacities to support wildlife and other consumers from a resource perspective. Results are connected directly to data, with full uncertainty, by MASTIF. This article is protected by copyright. All rights reserved.