Summer solstice orchestrates the subcontinental-scale synchrony of mast seeding.

High interannual variation in seed production in perennial plants can be synchronized at subcontinental scales with wide consequences for ecosystem functioning, but how such synchrony is generated is unclear1-3. We investigated the factors contributing to masting synchrony in European beech (Fagus sylvatica), which extends to a geographic range of 2,000 km. Maximizing masting synchrony via spatial weather coordination, known as the Moran effect, requires a simultaneous response to weather conditions across distant populations. A celestial cue that occurs simultaneously across the entire hemisphere is the longest day (the summer solstice). We show that European beech abruptly opens its temperature-sensing window on the solstice, and hence widely separated populations all start responding to weather signals in the same week. This celestial 'starting gun' generates ecological events with high spatial synchrony across the continent.

Evolution of masting in plants is linked to investment in low tissue mortality.

Masting, a variable and synchronized variation in reproductive effort is a prevalent strategy among perennial plants, but the factors leading to interspecific differences in masting remain unclear. Here, we investigate interannual patterns of reproductive investment in 517 species of terrestrial perennial plants, including herbs, graminoids, shrubs, and trees. We place these patterns in the context of the plants' phylogeny, habitat, form and function. Our findings reveal that masting is widespread across the plant phylogeny. Nonetheless, reversion from masting to regular seed production is also common. While interannual variation in seed production is highest in temperate and boreal zones, our analysis controlling for environment and phylogeny indicates that masting is more frequent in species that invest in tissue longevity. Our modeling exposes masting-trait relationships that would otherwise remain hidden and provides large-scale evidence that the costs of delayed reproduction play a significant role in the evolution of variable reproduction in plants.

Masting is uncommon in trees that depend on mutualist dispersers in the context of global climate and fertility gradients.

The benefits of masting (volatile, quasi-synchronous seed production at lagged intervals) include satiation of seed predators, but these benefits come with a cost to mutualist pollen and seed dispersers. If the evolution of masting represents a balance between these benefits and costs, we expect mast avoidance in species that are heavily reliant on mutualist dispersers. These effects play out in the context of variable climate and site fertility among species that vary widely in nutrient demand. Meta-analyses of published data have focused on variation at the population scale, thus omitting periodicity within trees and synchronicity between trees. From raw data on 12 million tree-years worldwide, we quantified three components of masting that have not previously been analysed together: (i) volatility, defined as the frequency-weighted year-to-year variation; (ii) periodicity, representing the lag between high-seed years; and (iii) synchronicity, indicating the tree-to-tree correlation. Results show that mast avoidance (low volatility and low synchronicity) by species dependent on mutualist dispersers explains more variation than any other effect. Nutrient-demanding species have low volatility, and species that are most common on nutrient-rich and warm/wet sites exhibit short periods. The prevalence of masting in cold/dry sites coincides with climatic conditions where dependence on vertebrate dispersers is less common than in the wet tropics. Mutualist dispersers neutralize the benefits of masting for predator satiation, further balancing the effects of climate, site fertility and nutrient demands.

Forecasting seed production in perennial plants: identifying challenges and charting a path forward.

Interannual variability of seed production, known as masting, has far-reaching ecological impacts including effects on forest regeneration and the population dynamics of seed consumers. Because the relative timing of management and conservation efforts in ecosystems dominated by masting species often determines their success, there is a need to study masting mechanisms and develop forecasting tools for seed production. Here, we aim to establish seed production forecasting as a new branch of the discipline. We evaluate the predictive capabilities of three models - foreMast, ΔT, and a sequential model - designed to predict seed production in trees using a pan-European dataset of Fagus sylvatica seed production. The models are moderately successful in recreating seed production dynamics. The availability of high-quality data on prior seed production improved the sequential model's predictive power, suggesting that effective seed production monitoring methods are crucial for creating forecasting tools. In terms of extreme events, the models are better at predicting crop failures than bumper crops, likely because the factors preventing seed production are better understood than the processes leading to large reproductive events. We summarize the current challenges and provide a roadmap to help advance the discipline and encourage the further development of mast forecasting.

How to measure mast seeding?

The periodic production of large seed crops, or masting, is a widespread phenomenon in perennial plants. This behavior can enhance the reproductive efficiency of plants, leading to increased fitness, and produce ripple effects on food webs. While variability from year to year is a defining characteristic of masting, the methods used to quantify this variability are highly debated. The commonly used coefficient of variation lacks the ability to account for the serial dependence in mast data and can be influenced by zeros, making it a less suitable choice for various applications based on individual-level observations, such as phenotypic selection, heritability, and climate change studies, which rely on individual-plant-level datasets that often contain numerous zeros. To address these limitations, we present three case studies and introduce volatility and periodicity, which account for the variance in the frequency domain by emphasizing the significance of long intervals in masting. By utilizing examples of Sorbus aucuparia, Pinus pinea, Quercus robur, Quercus pubescens, and Fagus sylvatica, we demonstrate how volatility captures the effects of variance at both high and low frequencies, even in the presence of zeros, leading to improved ecological interpretations of the results. The growing availability of long-term, individual-plant datasets promises significant advancements in the field, but requires appropriate tools for analysis, which the new metrics provide.

Mechanisms driving interspecific variation in regional synchrony of trees reproduction.

Seed production in many plants is characterized by large interannual variation, which is synchronized at subcontinental scales in some species but local in others. The reproductive synchrony affects animal migrations, trophic responses to resource pulses and the planning of management and conservation. Spatial synchrony of reproduction is typically attributed to the Moran effect, but this alone is unable to explain interspecific differences in synchrony. We show that interspecific differences in the conservation of seed production-weather relationships combine with the Moran effect to explain variation in reproductive synchrony. Conservative timing of weather cues that trigger masting allows populations to be synchronized at distances >1000 km. Conversely, if populations respond to variable weather signals, synchrony cannot be achieved. Our study shows that species vary in the extent to which their weather cueing is spatiotemporally conserved, with important consequences, including an interspecific variation of masting vulnerability to climate change.

Limits to reproduction and seed size-number trade-offs that shape forest dominance and future recovery.

The relationships that control seed production in trees are fundamental to understanding the evolution of forest species and their capacity to recover from increasing losses to drought, fire, and harvest. A synthesis of fecundity data from 714 species worldwide allowed us to examine hypotheses that are central to quantifying reproduction, a foundation for assessing fitness in forest trees. Four major findings emerged. First, seed production is not constrained by a strict trade-off between seed size and numbers. Instead, seed numbers vary over ten orders of magnitude, with species that invest in large seeds producing more seeds than expected from the 1:1 trade-off. Second, gymnosperms have lower seed production than angiosperms, potentially due to their extra investments in protective woody cones. Third, nutrient-demanding species, indicated by high foliar phosphorus concentrations, have low seed production. Finally, sensitivity of individual species to soil fertility varies widely, limiting the response of community seed production to fertility gradients. In combination, these findings can inform models of forest response that need to incorporate reproductive potential.

Globally, tree fecundity exceeds productivity gradients.

Lack of tree fecundity data across climatic gradients precludes the analysis of how seed supply contributes to global variation in forest regeneration and biotic interactions responsible for biodiversity. A global synthesis of raw seedproduction data shows a 250-fold increase in seed abundance from cold-dry to warm-wet climates, driven primarily by a 100-fold increase in seed production for a given tree size. The modest (threefold) increase in forest productivity across the same climate gradient cannot explain the magnitudes of these trends. The increase in seeds per tree can arise from adaptive evolution driven by intense species interactions or from the direct effects of a warm, moist climate on tree fecundity. Either way, the massive differences in seed supply ramify through food webs potentially explaining a disproportionate role for species interactions in the wet tropics.

Is there tree senescence? The fecundity evidence.

Despite its importance for forest regeneration, food webs, and human economies, changes in tree fecundity with tree size and age remain largely unknown. The allometric increase with tree diameter assumed in ecological models would substantially overestimate seed contributions from large trees if fecundity eventually declines with size. Current estimates are dominated by overrepresentation of small trees in regression models. We combined global fecundity data, including a substantial representation of large trees. We compared size-fecundity relationships against traditional allometric scaling with diameter and two models based on crown architecture. All allometric models fail to describe the declining rate of increase in fecundity with diameter found for 80% of 597 species in our analysis. The strong evidence of declining fecundity, beyond what can be explained by crown architectural change, is consistent with physiological decline. A downward revision of projected fecundity of large trees can improve the next generation of forest dynamic models.

Crown defoliation decreases reproduction and wood growth in a marginal European beech population.

BACKGROUND AND AIMS: Abiotic and biotic stresses related to climate change have been associated with increased crown defoliation, decreased growth and a higher risk of mortality in many forest tree species, but the impact of stresses on tree reproduction and forest regeneration remains understudied. At the dry, warm margin of species distributions, flowering, pollination and seed maturation are expected to be affected by drought, late frost and other stresses, eventually resulting in reproduction failure. Moreover, inter-individual variation in reproductive performance versus other performance traits (growth, survival) could have important consequences for population dynamics. This study investigated the relationships among individual crown defoliation, growth and reproduction in a drought-prone population of European beech, Fagus sylvatica. METHODS: We used a spatially explicit mating model and marker-based parentage analyses to estimate effective female and male fecundities of 432 reproductive trees, which were also monitored for basal area increment and crown defoliation over 9 years. KEY RESULTS: Female and male fecundities varied markedly between individuals, more than did growth. Both female fecundity and growth decreased with increasing crown defoliation and competition, and increased with size. Moreover, the negative effect of defoliation on female fecundity was size-dependent, with a slower decline in female fecundity with increasing defoliation for the large individuals. Finally, a trade-off between growth and female fecundity was observed in response to defoliation: some large trees maintained significant female fecundity at the expense of reduced growth in response to defoliation, while some other defoliated trees maintained high growth at the expense of reduced female fecundity. CONCLUSIONS: Our results suggest that, while decreasing their growth, some large defoliated trees still contribute to reproduction through seed production and pollination. This non-coordinated decline of growth and fecundity at individual level in response to stress may compromise the evolution of stress-resistance traits at population level, and increase forest tree vulnerability.

Correlative climatic niche models predict real and virtual species distributions equally well.

Climate is one of the main factors driving species distributions and global biodiversity patterns. Obtaining accurate predictions of species' range shifts in response to ongoing climate change has thus become a key issue in ecology and conservation. Correlative species distribution models (cSDMs) have become a prominent tool to this aim in the last decade and have demonstrated good predictive abilities with current conditions, irrespective of the studied taxon. However, cSDMs rely on statistical association between species' presence and environmental conditions and have rarely been challenged on their actual capacity to reflect causal relationships between species and climate. In this study, we question whether cSDMs can accurately identify if climate and species distributions are causally linked, a prerequisite for accurate prediction of range shift in relation to climate change. We compared the performance of cSDMs in predicting the distributions of 132 European terrestrial species, chosen randomly within five taxonomic groups (three vertebrate groups and two plant groups), and of 1,320 virtual species whose distribution is causally fully independent from climate. We found that (1) for real species, the performance of cSDMs varied principally with range size, rather than with taxonomic groups and (2) cSDMs did not predict the distributions of real species with a greater accuracy than the virtual ones. Our results unambiguously show that the high predictive power of cSDMs can be driven by spatial autocorrelation in climatic and distributional data and does not necessarily reflect causal relationships between climate and species distributions. Thus, high predictive performance of cSDMs does not ensure that they accurately depict the role of climate in shaping species distributions. Our findings therefore call for strong caution when using cSDMs to provide predictions on future range shifts in response to climate change.