Evolutionary ecology of masting: mechanisms, models, and climate change.

Many perennial plants show mast seeding, characterized by synchronous and highly variable reproduction across years. We propose a general model of masting, integrating proximate factors (environmental variation, weather cues, and resource budgets) with ultimate drivers (predator satiation and pollination efficiency). This general model shows how the relationships between masting and weather shape the diverse responses of species to climate warming, ranging from no change to lower interannual variation or reproductive failure. The role of environmental prediction as a masting driver is being reassessed; future studies need to estimate prediction accuracy and the benefits acquired. Since reproduction is central to plant adaptation to climate change, understanding how masting adapts to shifting environmental conditions is now a central question.

Widespread breakdown in masting in European beech due to rising summer temperatures.

Climate change effects on tree reproduction are poorly understood, even though the resilience of populations relies on sufficient regeneration to balance increasing rates of mortality. Forest-forming tree species often mast, i.e. reproduce through synchronised year-to-year variation in seed production, which improves pollination and reduces seed predation. Recent observations in European beech show, however, that current climate change can dampen interannual variation and synchrony of seed production and that this masting breakdown drastically reduces the viability of seed crops. Importantly, it is unclear under which conditions masting breakdown occurs and how widespread breakdown is in this pan-European species. Here, we analysed 50 long-term datasets of population-level seed production, sampled across the distribution of European beech, and identified increasing summer temperatures as the general driver of masting breakdown. Specifically, increases in site-specific mean maximum temperatures during June and July were observed across most of the species range, while the interannual variability of population-level seed production (CVp) decreased. The declines in CVp were greatest, where temperatures increased most rapidly. Additionally, the occurrence of crop failures and low seed years has decreased during the last four decades, signalling altered starvation effects of masting on seed predators. Notably, CVp did not vary among sites according to site mean summer temperature. Instead, masting breakdown occurs in response to warming local temperatures (i.e. increasing relative temperatures), such that the risk is not restricted to populations growing in warm average conditions. As lowered CVp can reduce viable seed production despite the overall increase in seed count, our results warn that a covert mechanism is underway that may hinder the regeneration potential of European beech under climate change, with great potential to alter forest functioning and community dynamics.

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.

MASTREE+: Time-series of plant reproductive effort from six continents.

Significant gaps remain in understanding the response of plant reproduction to environmental change. This is partly because measuring reproduction in long-lived plants requires direct observation over many years and such datasets have rarely been made publicly available. Here we introduce MASTREE+, a data set that collates reproductive time-series data from across the globe and makes these data freely available to the community. MASTREE+ includes 73,828 georeferenced observations of annual reproduction (e.g. seed and fruit counts) in perennial plant populations worldwide. These observations consist of 5971 population-level time-series from 974 species in 66 countries. The mean and median time-series length is 12.4 and 10 years respectively, and the data set includes 1122 series that extend over at least two decades (≥20 years of observations). For a subset of well-studied species, MASTREE+ includes extensive replication of time-series across geographical and climatic gradients. Here we describe the open-access data set, available as a.csv file, and we introduce an associated web-based app for data exploration. MASTREE+ will provide the basis for improved understanding of the response of long-lived plant reproduction to environmental change. Additionally, MASTREE+ will enable investigation of the ecology and evolution of reproductive strategies in perennial plants, and the role of plant reproduction as a driver of ecosystem dynamics.

Aún existen importantes vacíos en la comprensión de la respuesta reproductiva de las plantas al cambio medioambiental, en parte, porque su monitoreo en especies de plantas longevas requiere una observación directa durante muchos años, y estos conjuntos de datos rara vez han estado disponibles. Aquí presentamos a MASTREE +, una base de datos que recopila series de tiempo de la reproducción de las plantas de todo el planeta, poniendo a disposición estos datos de libre acceso para la comunidad científica. MASTREE + incluye 73.828 puntos de observación de la reproducción anual georreferenciados (ej. conteos de semillas y frutos) en poblaciones de plantas perennes en todo el mundo. Estas observaciones consisten en 5971 series temporales a nivel de población provenientes de 974 especies en 66 países. La mediana de la duración de las series de tiempo es de 10 años (media = 12.4 años) y el conjunto de datos incluye 1.122 series de al menos dos décadas (≥20 años de observaciones). Para un subconjunto de especies bien estudiadas, MASTREE +incluye un amplio conjunto de series temporales replicadas en gradientes geográficos y climáticos. Describimos el conjunto de datos de acceso abierto disponible como un archivo.csv y presentamos una aplicación web asociada para la exploración de datos. MASTREE+ proporcionará la base para mejorar la comprensión sobre la respuesta reproductiva de plantas longevas al cambio medioambiental. Además, MASTREE+ facilitará los avances en la investigación de la ecología y la evolución de las estrategias reproductivas en plantas perennes y el papel de la reproducción vegetal como determinante de la dinámica de ecosistemas.

Diversity and Interrelations Among the Constitutive VOC Emission Blends of Four Broad-Leaved Tree Species at Seedling Stage.

Volatile organic compounds (VOCs) emitted by plants consist of a broad range of gasses which serve purposes such as protecting against herbivores, communicating with insects and neighboring plants, or increasing the tolerance to environmental stresses. Evidence is accumulating that the composition of VOC blends plays an important role in fulfilling these purposes. Constitutional emissions give insight into species-specific stress tolerance potentials and are an important first step in linking metabolism and function of co-occurring VOCs. Here, we investigate the blend composition and interrelations among co-emitted VOCs in unstressed seedlings of four broad-leaved tree species, Quercus robur, Fagus sylvatica, Betula pendula, and Carpinus betulus. VOCs of Q. robur and F. sylvatica mainly emitted isoprene and monoterpenes, respectively. B. pendula had relatively high sesquiterpene emission; however, it made up only 1.7% of its total emissions while the VOC spectrum was dominated by methanol (∼72%). C. betulus was emitting methanol and monoterpenes in similar amounts compared to other species, casting doubt on its frequent classification as a close-to-zero VOC emitter. Beside these major VOCs, a total of 22 VOCs could be identified, with emission rates and blend compositions varying drastically between species. A principal component analysis among species revealed co-release of multiple compounds. In particular, new links between pathways and catabolites were indicated, e.g., correlated emission rates of methanol, sesquiterpenes (mevalonate pathway), and green leaf volatiles (hexanal, hexenyl acetate, and hexenal; lipoxygenase pathway). Furthermore, acetone emissions correlated with eugenol from the Shikimate pathway, a relationship that has not been described before. Our results thus indicate that certain VOC emissions are highly interrelated, pointing toward the importance to improve our understanding of VOC blends rather than targeting dominant VOCs only.

The ecology and evolution of synchronized reproduction in long-lived plants.

Populations of many long-lived plants exhibit spatially synchronized seed production that varies extensively over time, so that seed production in some years is much higher than on average, while in others, it is much lower or absent. This phenomenon termed masting or mast seeding has important consequences for plant reproductive success, ecosystem dynamics and plant-human interactions. Inspired by recent advances in the field, this special issue presents a series of articles that advance the current understanding of the ecology and evolution of masting. To provide a broad overview, we reflect on the state-of-the-art of masting research in terms of underlying proximate mechanisms, ontogeny, adaptations, phylogeny and applications to conservation. While the mechanistic drivers and fitness consequences of masting have received most attention, the evolutionary history, ontogenetic trajectory and applications to plant-human interactions are poorly understood. With increased availability of long-term datasets across broader geographical and taxonomic scales, as well as advances in molecular approaches, we expect that many mysteries of masting will be solved soon. The increased understanding of this global phenomenon will provide the foundation for predictive modelling of seed crops, which will improve our ability to manage forests and agricultural fruit and nut crops in the Anthropocene. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Fire history and weather interact to determine extent and synchrony of mast-seeding in rhizomatous scrub oaks of Florida.

In disturbance-prone ecosystems, fitness consequences of plant reproductive strategies are often determined by the relative timing of seed production and disturbance events, but the role of disturbances as proximate drivers of seed production has been overlooked. We use long-term data on seed production in Quercus chapmanii, Q. geminata and Q. inopina, rhizomatous oaks found in south central Florida's oak scrub, to investigate the role of fire history and its interaction with weather in shaping acorn production and its synchrony. Acorn production increased with the time since last fire, combined with additive or interactive effects of spring precipitation (+) or drought (-). Furthermore, multiple matrix regression models revealed that ramet pairs with shared fire history were more synchronous in seed production than ones that burned in different years. Long-term trends suggest that increasingly drier spring weather, in interaction with fire frequency, may drive a decline of seed production. Such declines could affect the community of acorn-reliant vertebrates in the Florida scrub, including endangered Florida scrub-jays (Aphelocoma coerulescens). These results illustrate that fire can function as a proximate driver of seed production in mast-seeding species, highlighting the increasingly recognized importance of interactions among reproductive strategies and disturbance regimes in structuring plant populations and communities. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Understanding mast seeding for conservation and land management.

Masting, the intermittent and synchronous production of large seed crops, can have profound consequences for plant populations and the food webs that are built on their seeds. For centuries, people have recorded mast crops because of their importance in managing wildlife populations. In the past 30 years, we have begun to recognize the importance of masting in conserving and managing many other aspects of the environment: promoting the regeneration of forests following fire or other disturbance, conserving rare plants, conscientiously developing the use of edible seeds as non-timber forest products, coping with the consequences of extinctions on seed dispersal, reducing the impacts of plant invasions with biological control, suppressing zoonotic diseases and preventing depredation of endemic fauna. We summarize current instances and future possibilities of a broad set of applications of masting. By exploring in detail several case studies, we develop new perspectives on how solutions to pressing conservation and land management problems may benefit by better understanding the dynamics of seed production. A lesson common to these examples is that masting can be used to time management, and often, to do this effectively, we need models that explicitly forecast masting and the dynamics of seed-eating animals into the near-term future. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Natural disturbances and masting: from mechanisms to fitness consequences.

The timing of seed production and release is highly relevant for successful plant reproduction. Ecological disturbances, if synchronized with reproductive effort, can increase the chances of seeds and seedlings to germinate and establish. This can be especially true under variable and synchronous seed production (masting). Several observational studies have reported worldwide evidence for co-occurrence of disturbances and seed bumper crops in forests. Here, we review the evidence for interaction between disturbances and masting in global plant communities; we highlight feedbacks between these two ecological processes and posit an evolutionary pathway leading to the selection of traits that allow trees to synchronize seed crops with disturbances. Finally, we highlight relevant questions to be tested on the functional and evolutionary relationship between disturbances and masting. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Differential spatial responses of rodents to masting on forest sites with differing disturbance history.

Mast seeding, the synchronized interannual variation in seed production of trees, is a well-known bottom-up driver for population densities of granivorous forest rodents. Such demographic effects also affect habitat preferences of the animals: After large seed production events, reduced habitat selectivity can lead to spillover from forest patches into adjacent alpine meadows or clear-cuts, as has been reported for human-impacted forests. In unmanaged, primeval forests, however, gaps created by natural disturbances are typical elements, yet it is unclear whether the same spillover dynamics occur under natural conditions. To determine whether annual variation in seed production drives spillover effects in naturally formed gaps, we used 14 years of small mammal trapping data combined with seed trap data to estimate population densities of Apodemus spp. mice and bank voles (Myodes glareolus) on 5 forest sites with differing disturbance history. The study sites, located in a forest dominated by European beech (Fagus sylvatica), Norway spruce (Picea abies), and silver fir (Abies alba), consisted of two primeval forest sites with small canopy gaps, two sites with larger gaps (after an avalanche event and a windthrow event), and a managed forest stand with closed canopy as a control. Hierarchical Bayesian N-mixture models revealed a strong influence of seed rain on small rodent abundance, which were site-specific for M. glareolus but not for Apodemus spp. Following years of moderate or low seed crop, M. glareolus avoided open habitat patches but colonized those habitats in large numbers after full mast events, suggesting that spillover events also occur in unmanaged forests, but not in all small rodents. The species- and site-specific characteristics of local density responding to food availability have potentially long-lasting effects on forest gap regeneration dynamics and should be addressed in future studies.

Flowering synchrony drives reproductive success in a wind-pollinated tree.

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 synchronised 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.

Investigating the relationship between climate, stand age, and temporal trends in masting behavior of European forest trees.

Masting-temporally variable seed production with high spatial synchrony-is a pervasive strategy in wind-pollinated trees that is hypothesized to be vulnerable to climate change due to its correlation with variability in abiotic conditions. Recent work suggests that aging may also have strong effects on seed production patterns of trees, but this potential confounding factor has not been considered in previous times series analysis of climate change effects. Using a 54 year dataset for seven dominant species in 17 forests across Poland, we used the proportion of seed-producing trees (PST) to contrast the predictions of the climate change and aging hypotheses in Abies alba, Fagus sylvatica, Larix decidua, Picea abies, Pinus sylvestris, Quercus petraea, and Quercus robur. Our results show that in all species, PST increased over time and that this change correlated most strongly with stand age, while the standardized precipitation-evapotranspiration index, a measure of drought, contributed to temporal trends in PST of F. sylvatica and Q. robur. Temporal variability of PST also increased over time in all species except P. sylvestris, while trends in temporal autocorrelation and among-stand synchrony reflect species-specific masting strategies. Our results suggest a pivotal role of plant ontogeny in driving not only the extent but also variability and synchrony of reproduction in temperate forest trees. In a time of increasing forest regrowth in Europe, we therefore call for increased attention to demographic effects such as aging on plant reproductive behavior, particularly in studies examining global change effects using long-term time series data.

From theory to experiments for testing the proximate mechanisms of mast seeding: an agenda for an experimental ecology.

Highly variable and synchronised production of seeds by plant populations, known as masting, is implicated in many important ecological processes, but how it arises remains poorly understood. The lack of experimental studies prevents underlying mechanisms from being explicitly tested, and thereby precludes meaningful predictions on the consequences of changing environments for plant reproductive patterns and global vegetation dynamics. Here we review the most relevant proximate drivers of masting and outline a research agenda that takes the biology of masting from a largely observational field of ecology to one rooted in mechanistic understanding. We divide the experimental framework into three main processes: resource dynamics, pollen limitation and genetic and hormonal regulation, and illustrate how specific predictions about proximate mechanisms can be tested, highlighting the few successful experiments as examples. We envision that the experiments we outline will deliver new insights into how and why masting patterns might respond to a changing environment.

Weather cues associated with masting behavior dampen the negative autocorrelation between past and current reproduction in oaks.

PREMISE OF THE STUDY: The influence of weather conditions on masting and the ecological advantages of this reproductive behavior have been the subject of much interest. Weather conditions act as cues influencing reproduction of individual plants, and similar responses expressed across many individuals lead to population-level synchrony in reproductive output. In turn, synchrony leads to benefits from economies of scale such as enhanced pollination success and seed predator satiation. However, there may also be individual-level benefits from reproductive responses to weather cues, which may explain the origin of masting in the absence of economies of scale. In a previous study, we found support for a mechanism whereby individual responses to weather cues attenuate the negative autocorrelation between past and current annual seed production-a pattern typically attributed to resource limitation and reproductive tradeoffs among years. METHODS: Here we provide a follow-up and more robust evaluation of this hypothesis in 12 species of oaks (Quercus spp.), testing for a negative autocorrelation (tradeoff) between past and current reproduction and whether responses to weather cues associated with masting reduce the strength of this negative autocorrelation. KEY RESULTS: Our results showed a strong negative autocorrelation for 11 of the species, and that species-specific reproductive responses to weather cues dampened this negative autocorrelation in 10 of them. CONCLUSIONS: This dampening effect presumably reflects a reduction in resource limitation or increased resource use associated with weather conditions, and suggests that responses to weather cues conferring these advantages should be selected for based on individual benefits.

Stay Gathered Rather than Scattered: Strategies of Common Marmosets during Agonistic Interactions with Birds in the Atlantic Rain Forest.

To reduce the vulnerability of their small body size, common marmosets live in large and cohesive social groups. Thus, we hypothesized that in order to compensate for small body size and predation risk, individuals of common marmosets will stay gathered rather than scattered when foraging for eggs and/or nestling birds. Furthermore, in order to avoid costly injuries and eventual predation risks, for both sides, the majority of interactions among common marmosets and small birds will not involve direct physical contact. The study was developed in a small fragment of Atlantic Forest in the northeast of Brazil. We recorded a total of 115 interactions between common marmosets (Callithrix jacchus) with 7 different bird species. As expected, agonistic interactions were significantly more frequent when the marmosets were gathered. Also, most agonistic interactions by the birds toward common marmosets involved overflights without physical contact. Apparently, the set of avoidance behavior leads to a reduced predation risk for both sides. It appears that dispersed marmosets do not represent an imminent threat that justifies an agonistic reaction by the birds as the latter appear to avoid exposing themselves to unnecessary danger during agonistic interactions, especially when the marmosets are gathered.

Effects of mistletoe (Phoradendron villosum) on California oaks.

Mistletoes are a widespread group of plants often considered to be hemiparasitic, having detrimental effects on growth and survival of their hosts. We studied the effects of the Pacific mistletoe, Phoradendron villosum, a member of a largely autotrophic genus, on three species of deciduous California oaks. We found no effects of mistletoe presence on radial growth or survivorship and detected a significant positive relationship between mistletoe and acorn production. This latter result is potentially explained by the tendency of P. villosum to be present on larger trees growing in nitrogen-rich soils or, alternatively, by a preference for healthy, acorn-producing trees by birds that potentially disperse mistletoe. Our results indicate that the negative consequences of Phoradendron presence on their hosts are negligible-this species resembles an epiphyte more than a parasite-and outweighed by the important ecosystem services mistletoe provides.

Drivers of synchrony of acorn production in the valley oak (Quercus lobata) at two spatial scales.

We investigated spatial synchrony of acorn production by valley oaks (Quercus lobata) among individual trees at the within-population, local level and at the among-population, statewide level spanning the geographic range of the species. At the local level, the main drivers of spatial synchrony were water availability and flowering phenology of individual trees, while proximity, temperature differences between trees, and genetic similarity failed to explain a significant proportion of variance in spatial synchrony. At the statewide level, annual rainfall was the primary driver, while proximity was significant by itself but not when controlling for rainfall; genetic similarity was again not significant. These results support the hypothesis that environmental factors, the Moran effect, are key drivers of spatial synchrony in acorn production at both small and large geographic scales. The specific environmental factors differed depending on the geographic scale, but were in both cases related to water availability. In addition, flowering phenology, potentially affecting either density-independent pollination failure (the pollination Moran effect) or density-dependent pollination efficiency (pollen coupling), plays a key role in driving spatial synchrony at the local geographic scale.

Masting in wind-pollinated trees: system-specific roles of weather and pollination dynamics in driving seed production.

Masting, the highly variable production of synchronized large seed crops, is a common reproductive strategy in plant populations. In wind-pollinated trees, flowering and pollination dynamics are hypothesized to provide the mechanistic link for the well-known relationship between weather and population-level seed production. Several hypotheses make predictions about the effect of weather on annual pollination success. The pollen coupling hypothesis predicts that weather and plant resources drive the flowering effort of trees, which directly translates into the size of seed crops through efficient pollination. In contrast, the pollination Moran effect hypothesis predicts that weather affects pollination efficiency, leading to occasional bumper crops. Furthermore, the recently formulated phenology synchrony hypothesis predicts that Moran effects can arise because of weather effects on flowering synchrony, which, in turn, drives pollination efficiency. We investigated the relationship between weather, airborne pollen, and seed production in common European trees, two oak species (Quercus petraea and Q. robur) and beech (Fagus sylvatica) with a 19-yr data set from three sites in Poland. Our results show that warm summers preceding flowering correlated with high pollen abundance and warm springs resulted in short pollen seasons (i.e., high flowering synchrony) for all three species. Pollen abundance was the best predictor for seed crops in beech, as predicted under pollen coupling. In oaks, short pollen seasons, rather than pollen abundance, correlated with large seed crops, providing support for the pollination Moran effect and phenology synchrony hypotheses. Fundamentally different mechanisms may therefore drive masting in species of the family Fagacae.

Testing the Terminal Investment Hypothesis in California Oaks.

The terminal investment hypothesis-which proposes that reproductive investment should increase with age-related declines in reproductive value-has garnered support in a range of animal species but has not been previously examined in long-lived plants, such as trees. We tested this hypothesis by comparing relative acorn production and radial growth among 1,000+ mature individuals of eight species of California oaks (genus Quercus) followed for up to 37 years, during which time 70 trees died apparently natural deaths. We found no significant differences in the radial growth, acorn production, or index of reproductive effort, taking into consideration both growth and reproduction among dying trees relative to either conspecific trees at the same site that did not die or growth and reproduction from earlier years for the focal trees that did eventually die. Furthermore, we found no consistent trade-off between growth and reproduction among trees that died, nor did dying trees significantly alter their relative investment in reproduction even as they underwent physical decline. Trees approaching the end of their lives are often in poor physical condition but do not appear to differentially invest more of their diminished resources in reproduction compared with healthy trees.

Spatially biased dispersal of acorns by a scatter-hoarding corvid may accelerate passive restoration of oak habitat on California's largest island.

Scatter hoarding by corvids (crows, jays, magpies, and nutcrackers) provides seed dispersal for many large-seeded plants, including oaks and pines. When hoarding seeds, corvids often choose nonrandom locations throughout the landscape, resulting in differential survival of seeds. In the context of habitat restoration, such disproportional storing of seeds in areas suitable for germination and establishment can accelerate expansion and recovery of large-seeded tree populations and their associated ecosystems. Here, we investigate the spatial preferences of island scrub jays Aphelocoma insularis during scatter hoarding of acorns (Quercus spp.) on Santa Cruz Island. We use a large behavioral data set on the birds' behavior in combination with seedling surveys and spatial analysis to determine whether 1) island scrub jays disproportionally cache seeds in specific habitat types, and 2) whether the preferred habitat type is suitable for oak regeneration. Our results show that the jays nonrandomly cache acorns across the landscape; they use chaparral and coastal sage scrub disproportionally while avoiding open and grassy areas. The areas used most often for caching were also the areas with the highest oak seedling densities. We discuss the potential role of these findings for the recovery of Santa Cruz Island's oak habitat since the 1980s.