Masting and Efficient Production of Seedlings: Balancing Costs of Variation Through Synchronised Fruiting.

The efficient conversion of tissues into reproductive success is a crucial aspect affecting the evolution of life histories. Masting, the interannually variable and synchronous seed production in perennial plants, is a strategy that can enhance reproductive efficiency by mitigating seed predation and pollen limitation. However, evaluating benefits is insufficient to establish whether efficiency has improved, as such assessments neglect the associated costs of masting, particularly during the critical seed-to-seedling stage. We conducted a parentage analysis of seedlings and adults in a population of 209 Sorbus aucuparia trees, monitored over 23 years, providing pioneering documentation of the effects of masting on the fitness of individual trees beyond the seed stage. Our results show high costs of interannual variation that can be mitigated by high synchrony and reveal the existence of phenotypes that appear to reap the benefits of masting while avoiding its costs through regular reproduction.

Tail-dependence of masting synchrony results in continent-wide seed scarcity.

Spatial synchrony may be tail-dependent, meaning it is stronger for peaks rather than troughs, or vice versa. High interannual variation in seed production in perennial plants, called masting, can be synchronized at subcontinental scales, triggering extensive resource pulses or famines. We used data from 99 populations of European beech (Fagus sylvatica) to examine whether masting synchrony differs between mast peaks and years of seed scarcity. Our results revealed that seed scarcity occurs simultaneously across the majority of the species range, extending to populations separated by distances up to 1800 km. Mast peaks were spatially synchronized at distances up to 1000 km and synchrony was geographically concentrated in northeastern Europe. Extensive synchrony in the masting lower tail means that famines caused by beech seed scarcity are amplified by their extensive spatial synchrony, with diverse consequences for food web functioning and climate change biology.

A North American climate-masting-irruption teleconnection and its change under future climate.

Atmospheric variability can impact biological populations by triggering facultative migrations, but the stability of these atmosphere-biosphere connections may be vulnerable to climate change. As an example, we consider the leading mode of continental-scale facultative migration of Pine Siskins, where the associated ecological mechanism is changes in resource availability, with a mechanistic pathway of climate conditions affecting mast seeding patterns in trees which in turn drive bird migration. The three summers prior to pine siskin irruption feature an alternating west-east mast-seeding dipole in conifer trees with opposite anomalies over western and eastern North America. The climate driver of this west-east mast-seeding dipole, referred to as the North American Dipole, occurs during summer in the historical record, but shifts to spring in response to future climate warming during this century in a majority of global climate models. Identification of future changes in the timing of the climate driver of boreal forest mast seeding have broadly important implications for the dynamics of forest ecosystems.

Mast seeding is stronger in taller plants.

Introduction: Two economies of scale, predator satiation and pollination efficiency, have been proposed to explain the evolutionary mechanisms of mast seeding adopted by some long-lived plants. Plant height is strongly selected by pollination vectors and may also provide economies of scale; however, it remains unknown whether there is a close relationship between adult plant height and mast seeding intensity. Methods: Here, we analyzed mast seeding intensity of 158 plant species to test if adult plant height can select for mast seeding. Results: We show that mast seeding intensities are higher in taller plant species irrespective of phylogeny, life form, pollination vector, and type of Spermatophytes. We also show that anemophily rather than entomophily selects for taller plant species and higher mast seeding intensities. Discussion: The linear correlations and evolutionary links between adult plant height and mast seeding intensity provide evidence that mast seeding could have evolved as an adaptation to taller strategy of perennial plant species.

Mast seeding in European beech (Fagus sylvatica L.) is associated with reduced fungal sporocarp production and community diversity.

Mast seeding is a well-documented phenomenon across diverse forest ecosystems. While its effect on aboveground food webs has been thoroughly studied, how it impacts the soil fungi that drive soil carbon and nutrient cycling has not yet been explored. To evaluate the relationship between mast seeding and fungal resource availability, we paired a Swiss 29-year fungal sporocarp census with contemporaneous seed production for European beech (Fagus sylvatica L.). On average, mast seeding was associated with a 55% reduction in sporocarp production and a compositional community shift towards drought-tolerant taxa across both ectomycorrhizal and saprotrophic guilds. Among ectomycorrhizal fungi, traits associated with carbon cost did not explain species' sensitivity to seed production. Together, our results support a novel hypothesis that mast seeding limits annual resource availability and reproductive investment in soil fungi, creating an ecosystem 'rhythm' to forest processes that is synchronized above- and belowground.

Relatives reproduce in synchrony: kinship and individual condition shape intraspecific variation in masting phenotype.

Masting (synchronous and interannually variable seed production) is frequently called a reproductive strategy; yet it is unclear whether the reproductive behaviour of individuals has a heritable component. To address this, we used 22 years of annual fruit production data from 110 Sorbus aucuparia L. trees to examine the contributions of genetic factors to the reproductive phenotype of individuals, while controlling for environmental variation. Trees sharing close genetic relationships and experiencing similar habitat conditions exhibited similar levels of reproductive synchrony. Trees of comparable sizes displayed similar levels of year-to-year variation in fruiting, with relatedness contributing to this variation. External factors, such as shading, influenced the time intervals between years with abundant fruit production. The effects of genetic relatedness on the synchrony of reproduction among trees and on interannual variation provide long-awaited evidence that the masting phenotype is heritable, and can respond to natural selection.

Masting, fire-stimulated flowering, and the evolutionary ecology of synchronized reproduction.

Synchronized episodic reproduction among long-lived plants shapes ecological interactions, ecosystem dynamics, and evolutionary processes worldwide. Two active scientific fields investigate the causes and consequences of such synchronized reproduction: the fields of masting and fire-stimulated flowering. While parallels between masting and fire-stimulated flowering have been previously noted, there has been little dialogue between these historically independent fields. We predict that the synthesis of these fields will facilitate new insight into the causes and consequences of synchronized reproduction. Here we briefly review parallels between masting and fire-stimulated flowering, using two case studies and a database of 1870 plant species to facilitate methodological, conceptual, geographical, taxonomic, and phylogenetic comparisons. We identify avenues for future research and describe three key opportunities associated with synthesis. First, the taxonomic and geographic complementarity of empirical studies from these historically independent fields highlights the potential to derive more general inferences about global patterns and consequences of synchronized reproduction in perennial plants. Second, masting's well developed conceptual framework for evaluating adaptive hypotheses can help guide empirical studies of fire-stimulated species and enable stronger inferences about the evolutionary ecology of fire-stimulated flowering. Third, experimental manipulation of reproductive variation in fire-stimulated species presents unique opportunities to empirically investigate foundational questions about ecological and evolutionary processes underlying synchronized reproduction. Synthesis of these fields and their complementary insights offers a unique opportunity to advance our understanding of the evolutionary ecology of synchronized reproduction in perennial plants.

Granivore abundance shapes mutualism quality in plant-scatterhoarder interactions.

Conditional mutualisms involve costs and benefits that vary with environmental factors, but mechanisms driving these dynamics remain poorly understood. Scatterhoarder-plant interactions are a prime example of this phenomenon, as scatterhoarders can either increase or reduce plant recruitment depending on the balance between seed dispersal and predation. We explored factors that drive the magnitude of net benefits for plants in this interaction using a mathematical model, with parameter values based on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). We measured benefits as the percentage of germinating seeds, and examined how varying rodent survival (reflecting, e.g. changes in predation pressure), the rate of seed loss to other granivores, the abundance of alternative food resources, and changes in masting patterns affect the quality of mutualism. We found that increasing granivore abundance can degrade the quality of plant-scatterhoarder mutualism due to increased cache pilferage. Scatterhoarders are predicted to respond by increasing immediate consumption of gathered seeds, leading to higher costs and reduced benefits for plants. Thus, biotic changes that are detrimental to rodent populations can be beneficial for tree recruitment due to adaptive behavior of rodents. When scatterhoarder populations decline too drastically (< 5 individuals ha-1 ); however, tree recruitment may also suffer.

Reproductive collapse in European beech results from declining pollination efficiency in large trees.

Climate warming increases tree mortality which will require sufficient reproduction to ensure population viability. However, the response of tree reproduction to climate change remains poorly understood. Warming can reduce synchrony and interannual variability of seed production ("masting breakdown") which can increase seed predation and decrease pollination efficiency in trees. Here, using 40 years of observations of individual seed production in European beech (Fagus sylvatica), we showed that masting breakdown results in declining viable seed production over time, in contrast to the positive trend apparent in raw seed count data. Furthermore, tree size modulates the consequences of masting breakdown on viable seed production. While seed predation increased over time mainly in small trees, pollination efficiency disproportionately decreased in larger individuals. Consequently, fecundity declined over time across all size classes, but the overall effect was greatest in large trees. Our study showed that a fundamental biological relationship-correlation between tree size and viable seed production-has been reversed as the climate has warmed. That reversal has diverse consequences for forest dynamics; including for stand- and biogeographical-level dynamics of forest regeneration. The tree size effects suggest management options to increase forest resilience under changing climates.

Climate drivers of seed rain phenology of subtropical forest communities along an elevational gradient.

Seed rain phenology (the start and end date of seed rain) is an essential component of plant phenology, critical for understanding population regeneration and community dynamics. However, intra- and inter-annual changes of seed rain phenology along environmental gradients have rarely been studied and the responses of seed rain phenology to climate variations are unclear. We monitored seed rain phenology of four forest communities in four years at different elevations (900 m, 1450 m, 1650 m, 1900 m a.s.l.) of a subtropical mountain in Central China. We analyzed the spatiotemporal patterns of seed rain phenology of 29 common woody plant species (total observed species in the seed rain), and related the phenological variations to seed number and climatic variables using mixed-effect models with the correlation matrix of phylogeny. We found that changes in the period length were mainly driven by the end rather than the start date. The end date and the period length of seed rain were significantly different between the mast and non-mast seeding years, while no significant elevation-related trend was detected in seed rain phenology variation. Seed number, mean temperature in spring (Tspr), and winter (Twin), summer precipitation (Psum) had significant effects on seed rain phenology. When Tspr increased, the start date of seed rain advanced, while the end date was delayed and the seed rain period length was mainly prolonged by a higher seed number, Twin and Psum. Forest canopy might have a buffering effect on understory climatic conditions, especially in precipitation that lead to difference in seed rain phenology between canopy and shrub species. Our novel evidence of seed rain phenology can improve prediction of community regeneration dynamics in responding to climate changes.

Reproduction alternation in trees: testing the resource depletion hypothesis using experimental fruit removal in Quercus ilex.

The keystones of resource budget models to explain mast seeding are that fruit production depletes tree stored resources, which become subsequently limiting to flower production the following year. These two hypotheses have, however, rarely been tested in forest trees. Using a fruit removal experiment, we tested whether preventing fruit development would increase nutrient and carbohydrates storage and modify allocation to reproduction and vegetative growth the following year. We removed all the fruits from nine adult Quercus ilex L. trees shortly after fruit set and compared, with nine control trees, the concentrations of nitrogen (N), phosphorus (P), zinc (Zn), potassium (K) and starch in leaves, twigs and trunk before, during and after the development of female flowers and fruits. The following year, we measured the production of vegetative and reproductive organs as well as their location on the new spring shoots. Fruit removal prevented the depletion of N and Zn in leaves during fruit growth. It also modified the seasonal dynamics in Zn, K and starch in twigs, but had no effect on reserves stored in the trunk. Fruit removal increased the production of female flowers and leaves the following year, and decreased the production of male flowers. Our results show that resource depletion operates differently for male and female flowering, because the timing of organ formation and the positioning of flowers in shoot architecture differ between male and female flowers. Our results suggest that N and Zn availability constrain flower production in Q. ilex, but also that other regulatory pathways might be involved. They strongly encourage further experiments manipulating fruit development over multiple years to describe the causal relationships between variations in resource storage and/or uptake, and male and female flower production in masting species.

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.

Amplified Cyclicality in Mast Seeding Dynamics Positively Influences the Dynamics of a Seed Consumer Species.

AbstractTemporal autocorrelation in environmental conditions influences population dynamics through its effects on vital rates. However, a comprehensive understanding of how and to what extent temporal autocorrelation shapes population dynamics is still lacking because most empirical studies have unrealistically assumed that environmental conditions are temporally independent. Mast seeding is a biological event characterized by highly fluctuating and synchronized seed production at the tree population scale as well as a marked negative temporal autocorrelation. In the current context of global change, mast seeding events are expected to become more frequent, leading to strengthened negative temporal autocorrelations and thereby amplified cyclicality in mast seeding dynamics. Theory predicts that population growth rates are maximized when the environmental cyclicality of consumer resources and their generation times are closely matched. To test this prediction, we took advantage of the long-term monitoring of a wild boar population, a widespread seed consumer species characterized by a short generation time (∼2 years). As expected, simulations indicated that its stochastic population growth rate increased as mast seeding dynamics became more negatively autocorrelated. Our findings demonstrate that accounting for temporal autocorrelations in environmental conditions relative to the generation time of the focal population is required, especially under conditions of global warming, where the cyclicality in resource dynamics is likely to change.

Tropical-temperate comparisons in insect seed predation vary between study levels and years.

The biotic interaction hypothesis, which states the species interaction becomes stronger in the tropics, is deeply rooted in classic ecological literature and widely accepted to contribute to the latitudinal gradients of biodiversity. Tests in latitudinal insect-plant interaction have emphasized leaf-eating insects on a single or a few plant species rather than within an entire community and mixed accumulating evidence, leaving the biotic interaction hypothesis disputed. We aimed to test the hypothesis by quantifying insect seed predation in a pair of tropical and temperate forest communities with similar elevations. We applied a consistent study design to sample predispersal seeds with systematically set seed traps in 2019-2020 and examined internally feeding insects. The intensity of seed predation was measured and further applied to tropical versus temperate comparison at two levels (cross-species and community-wide). Our results showed every latitudinal pattern associated with different study levels and years, that is, negative (greater granivory in the tropics in community-wide comparison in 2020), positive (less granivory in the tropics in community-wide and cross-species comparison in 2019), and missing (similar level of granivory in the tropics in cross-species comparisons in 2020). The cross-species level analyses ignore differences among species in seed production and weaken or even lose the latitudinal trend detected by community-wide comparisons. The between-year discrepancy in tropical-temperate comparisons relates to the highly variable annual seed composition in the temperate forest due to mast seeding of dominant species. Our study highlights that long-term community-level researches across biomes are essential to assess the latitudinal biotic interaction hypothesis.

El Niño-Southern Oscillation affects the species-level temporal variation in seed and leaf fall in a mixed temperate forest.

El Niño-Southern Oscillation (ENSO), the variation between anomalously cold (La Niña) and warm conditions (El Niño), is one of the most prominent large-scale climate patterns with worldwide effects. Elevated seed and leaf fall has been found at the positive phase of ENSO (El Niño) in tropical forests. However, how seed and leaf fall respond to ENSO at species level is understudied, especially in temperate forests. In this study, we monitored seed and leaf fall at the species-level at 150 points across a 25-ha temperate forest in northeastern China over a span of 12 years. Using time series and wavelet analyses, we assessed three hypotheses: 1) temperate tree species' seed and leaf fall are strongly, but differently, correlated with ENSO and, 2) community synchrony in seed and leaf occurred both at seasonal and ENSO scales; finally, 3) local climatic modulated the effects of ENSO on seed and leaf fall. We found that ENSO was significantly correlated with seed and leaf fall of all species, although correlation strength varied across species (r = 0.206-0.658). Specifically, ENSO indices (ENSO12 or ENSO34) accounted for the most variation in seed and leaf fall of Acer pseudo-sieboldianum (40 % and 34 %, respectively) and ranged 4 %-31 % in all other species. Leaf fall was synchronous with ENSO cycles with a period of 2-7 years, but community synchrony of seed fall was only detected at seasonal scales. ENSO influenced seed fall of Fraxinus mandshurica and Tilla amurensis by mediating rainfall and relative humidity, respectively, highlighting the interactive effects of local climate and ENSO. Our findings highlight the potential effects of ENSO on ecosystems outside of tropical regions and improve our ability to predict regeneration dynamics and nutrient cycling of temperate forests under the context of global change.

Emerging infectious disease triggered a trophic cascade and enhanced recruitment of a masting tree.

There are several mechanisms that allow plants to temporarily escape from top-down control. One of them is trophic cascades triggered by top predators or pathogens. Another is satiation of consumers by mast seeding. These two mechanisms have traditionally been studied in separation. However, their combined action may have a greater effect on plant release than either process alone. In 2015, an outbreak of a disease (African swine fever, ASF) caused a crash in wild boar (Sus scrofa) abundance in Bialowieza Primeval Forest. Wild boar are important consumers of acorns and are difficult to satiate relative to less mobile granivores. We hypothesized that the joint action of the ASF outbreak and masting would enhance regeneration of oaks (Quercus robur). Data from ungulate exclosures demonstrated that ASF led to reduction in acorn predation. Tree seedling data indicated that oak recruitment increased twofold relative to pre-epidemic period. Our results showed that perturbations caused by wildlife disease travel through food webs and influence forest dynamics. The outbreak of ASF acted synergistically with masting and removed herbivore top-down control of oaks by mobile consumers. This illustrates that the ASF epidemic that currently occurs across Europe can have broad effects on forest dynamics.

Costs and benefits of masting: economies of scale are not reduced by negative density-dependence in seedling survival in Sorbus aucuparia.

Masting is a widespread reproductive strategy in plants that helps to reduce seed predation and increase pollination. However, masting can involve costs, notably negative density-dependent (NDD) seedling survival caused by concentrating reproduction in intermittent events. Masting benefits have received widespread attention, but the costs are understudied, which precludes understanding why some plant species have evolved intense masting, while others reproduce regularly. We followed seed production, seed predation (both 13 yr), and seedling recruitment and survival (11 yr) in Sorbus aucuparia. We tested whether NDD in seedling survival after mast years can reduce the benefits of pulsed reproduction that come through predator satiation. Seed predation rates were extreme in our population (mean = 75%), but were reduced by masting. The commonly accepted, but untested, assertion that pulsed recruitment is associated with strong NDD was unsupported. Consequently, the proportion of seedlings that survived their first year increased with fruit production. This provides a rare test of economies of scale beyond the seed stage. Our results provide estimation of the costs of mast seeding, and indicate that these may be lower than expected. Low masting costs, if common, may help explain why masting is such a widespread reproductive strategy throughout the plant kingdom.

A novel TFL1 gene induces flowering in the mast seeding alpine snow tussock, Chionochloa pallens (Poaceae).

Masting, the synchronous, highly variable flowering across years by a population of perennial plants, has been reported to be precipitated by various factors including nitrogen levels, drought conditions, and spring and summer temperatures. However, the molecular mechanism leading to the initiation of flowering in masting plants in particular years remains largely unknown, despite the potential impact of climate change on masting phenology. We studied genes controlling flowering in the alpine snow tussock Chionochloa pallens (Poaceae), a strongly masting perennial grass. We used a range of in situ and manipulated plants to obtain leaf samples from tillers (shoots) which subsequently remained vegetative or flowered. Here, we show that a novel orthologue of TERMINAL FLOWER 1 (TFL1; normally a repressor of flowering in other species) promotes the induction of flowering in C. pallens (hence Anti-TFL1), a conclusion supported by structural, functional and expression analyses. Global transcriptomic analysis indicated differential expression of CpTPS1, CpGA20ox1, CpREF6 and CpHDA6, emphasizing the role of endogenous cues and epigenetic regulation in terms of responsiveness of plants to initiate flowering. Our molecular-based study provides insights into the cellular mechanism of flowering in masting plants and will supplement ecological and statistical models to predict how masting will respond to global climate change.

How will global change affect plant reproduction? A framework for mast seeding trends.

Forest ecology traditionally focuses on plant growth and survival, leaving seed production as a major demographic process lacking a framework for how it will be affected by global change. Understanding plant reproductive responses to changing climate is complicated by masting, the annually variable seed production synchronized within populations. Predicting trends in masting is crucial, because masting impacts seed predation and pollination enough to override simple trends in mean seed production. Proximate mechanisms of seed production patterns in perennial plants are gathered to identify processes through which masting may be affected by a changing environment. Predicting trends in masting will require understanding the mechanisms that cause predictable seed failure after high-seed years, and the stochastic mechanisms that synchronize individuals in high-seed years.

A brief history of masting research.

Although it has long been recognized that seed production by many forest trees varies greatly from year to year, masting (along with 'mast fruiting', 'mast seeding' and 'masting behaviour') as a concept referring to such variability is a relatively recent development. Here, I provide a brief history of masting research, highlighting some of the early contributions by foresters, zoologists and others that paved the way for the burgeoning number of studies currently being conducted by researchers around the world. Of particular current interest is work attempting to understand the proximate mechanisms, evolutionary drivers and community effects of this important ecological phenomenon as well as the ways that climate change may influence masting behaviour in the future. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.