Introduction
Despite the evolutionary and ecological advantage of seed reproduction
for herbaceous plants, investment in seed reproductive structures,
including the inflorescence, is very costly (Reekie & Bazzaz 1987;
Schoen & Dubuc 1990). Therefore, as an alternative investment,
polycarpic species may reduce flowering in a given year if it proves
costly relative to available resources and increase non-reproductive
biomass production (Fujita et al. 2014). Due to this trade-off,
reproductive allocation (RA, the ratio of reproductive structure biomass
to total biomass) between herbaceous species in the community can be
highly variable (Thompson & Eckert 2004) and even opposite, leading to
species and individual asynchrony in generative reproduction.
Plant populations can be highly synchronous in their flowering, with
species flowering extensively together during one growing season, but
restricting their flowering in other years (i.e. year-to-year synchrony)
(Pesendorfer et al. 2021). Synchronicity in plant reproduction was
identified early as a consequence of resource matching (i.e., theresource matching hypothesis , Klebs 1904). According to resource
matching theory, environmentally optimal years, characterised as
resource pulses, induce an increase in seed reproduction across the
community (Monks et al. 2016; Pearse et al. 2016; Bogdziewicz et al.
2020). A fixed proportion of resources is consistently allocated to both
reproductive and vegetative growth each year, maintaining a constant RA
(\(\frac{\text{dRA}}{\text{dt}}=0\)). As such, it serves as a baseline
assumption for masting, where variations in annual seed production are
not considered to be indicative of adaptive strategies (Bogdziewicz et
al. 2020). Conversely, significant deviations from the fixed proportion
of resources allocated to reproduction may indicate an adaptive response
(\(\frac{\text{dRA}}{\text{dt}}\neq 0)\). In this case, resource
limitation triggers an evolutionary trade-off between reproductive and
vegetative growth investments (Fernández-Martínez et al. 2019). Plants
can either prioritize reproduction even at the expense of growth by
increasing RA (as proposed by the resource switching hypothesis ,
Hacket‐Pain et al. 2018) or they can delay by decreasing RA until
resources are sufficiently accumulated (as proposed by theresource budget hypothesis ; Isagi et al. 1997; Satake & Iwasa
2000; Han et al. 2014). Empirical tests of these hypotheses have yielded
diverse outcomes for different limiting resources (such as light,
carbohydrates, nutrients, and water; Crone et al. 2009; Miyazaki et al.
2014; Smaill et al. 2011; Montesinos et al. 2012; Sala et al. 2012;
Pulido et al. 2014), highlighting the species-specific dependence of RA
on resource constraints (Pearse et al. 2016).
RA studies have traditionally used single-resource models, which
consider a single resource limitation and overlook the complexity of
multiple simultaneous limitations that plant communities typically face.
Contrasting resource requirements and competitive strategies among
species are also ignored. Coexistence in a multi-species community is
driven by life history trade-offs associated with different essential
resources (Tilman & Pacala 1993). The most contrasting species
life-history trade-offs arise from resource limitation for light at
optimal sites and belowground resource limitation (moisture and
nutrients) in stressful environments (Dybzinski & Tilman 2007). The
competitively dominant species are less tolerant of belowground
limitations, but exclude other plants by their superior competitive
ability above ground. Conversely, stress-tolerant species are weaker
competitors under optimal growth conditions where strong light
competition prevails (Grime & Hunt 1975). This trade-off has been
proposed to explain the alternation of species with different resource
acquisition strategies along moisture and other resource gradients
(Liancourt et al. 2005; Gross et al. 2009; Mariotte et al. 2013; Doudová
& Douda 2020; Douda et al. 2021), but the multiple-resource limitation
model has not yet been applied to explain species RA patterns and their
synchrony.
The multiple-resource limitation model implies that plant species differ
in their RA responses based on their tolerance to above- and belowground
resource availability. Competitively dominant species are expected to be
mainly dependent on the availability of belowground resources, and as
these resources become less available, RA is reduced (Reekie & Bazzaz
1987; van Lent et al. 1995; Kettenring et al. 2011; Johnson et al.
2017). Conversely, subordinate species, whose growth is mainly limited
by aboveground competition, are expected to allocate more resources to
seed production under stress conditions, when competition with dominant
species is less intense (Chaloupecká & Lepš, 2004). In environments
where belowground resources fluctuate, competition for light may be
particularly intense during resource pulses, forcing subordinate species
to accelerate their reproductive efforts relative to dominant species in
resource scarcity period (Sun & Frelich 2011). As a result, subordinate
species may be driven to flower either before or after optimal
conditions for competitively dominant species (Martínková et al. 2002;
Williamson & Ickes 2002; Catorci et al. 2012). Reproductive allocation
patterns of subordinate species may therefore be more consistent with
the resource-matching or switching hypothesis, as they need to produce
more seeds quickly in the window of opportunity when competition for
light with dominant species is temporarily reduced. Under
resource-limited conditions, slower growing dominant species may
gradually accumulate belowground resources, delaying future flowering,
consistent with the resource budget hypothesis. While this may increase
RA synchrony between subordinate species, it may also increase
asynchrony between subordinate and dominant species during scarcity
period.
Resource limitation may have different effects on intraspecific
synchrony in RA compared to the interspecific level. An increase in
intraspecific synchrony is associated with a reduction in intraspecific
variability in RA. This reduction could lead to increased
differentiation in RA between species, potentially increasing asynchrony
at the interspecific level. Furthermore, evolutionary dynamics may also
play a role in the observed differences between inter- and intraspecific
synchrony. In particular, plants that synchronise flowering with
conspecifics may have reduced reproductive costs. Predator satiation
during years of abundant seed production (Silvertown 1980; Zwolak et al.
2022), increased pollination efficiency during periods of increased
flowering (Nilsson & Wastljung 1987; Kelly et al. 2001), and individual
kinship (Bogdziewicz et al. 2024) are factors that favour intraspecific
rather than interspecific synchrony. In particular, subordinate species
may be highly intra-specifically synchronised in flowering to maximise
reproductive output, as they have a limited time to reproduce when
belowground resources decline and competition from dominant species
decreases. Dominant species may show a more dispersed reproductive
pattern in years with favourable resource conditions.
Here, we tested for the first time the multiple-resource limitation
model by quantifying the contribution of belowground resource limitation
and light competition to species RA and community flowering patterns
(i.e. the extent of synchronous RA both inter- and intraspecifically).
We established an experimental wetland plant community and exposed
plants to different drought stress regimes and a dominant removal
treatment. The drought stress regimes simulated either fluctuating
resource levels under interannual drought by alternating between
well-watered (optimal) and dry (suboptimal) conditions, or sustained
drought stress over several years (Douda et al. 2018; Doudová & Douda
2020). The interannual drought allowed us to assess whether interannual
variation in RA is driven by actual resource levels, as predicted by the
resource switching hypothesis. The permanent drought regime assessed the
ability of species to accumulate resources over several years to
increase RA. Both regimes were compared to a scenario of continuous
water availability throughout the experiment. The effect of
interspecific interactions on three subordinate species was estimated by
removing a dominant species. Lastly, we investigated whether
intraspecific synchrony responded to resource levels and species
interactions in a similar way to interspecific synchrony.