Climate change and plant reproduction: trends and drivers of mast seeding change

Climate change is reshaping global vegetation through its impacts on plant mortality, but recruitment creates the next generation of plants and will determine the structure and composition of future communities. Recruitment depends on mean seed production, but also on the interannual variability and among-plant synchrony in seed production, the phenomenon known as mast seeding. Thus, predicting the long-term response of global vegetation dynamics to climate change requires understanding the response of masting to changing climate. Recently, data and methods have become available allowing the first assessments of long-term changes in masting. Reviewing the literature, we evaluate evidence for a fingerprint of climate change on mast seeding and discuss the drivers and impacts of these changes. We divide our discussion into the main characteristics of mast seeding: interannual variation, synchrony, temporal autocorrelation, and mast frequency. Data indicate that masting patterns, are changing, but the direction of that change varies, likely reflecting the diversity of proximate factors underlying masting across taxa. Experiments to understand the proximate mechanisms underlying masting, in combination with the analysis of long-term datasets, will enable us to understand this observed variability in the response of masting. This will allow us to predict future shifts in masting patterns, and consequently ecosystem impacts of climate change via its impacts on masting.</p

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

AbstractMasting, 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.</jats:p

Environmental variation drives continental-scale synchrony of European beech reproduction.

Spatial synchrony is the tendency of spatially separated populations to display similar temporal fluctuations. Synchrony affects regional ecosystem functioning, but it remains difficult to disentangle its underlying mechanisms. We leveraged regression on distance matrices and geography of synchrony to understand the processes driving synchrony of European beech masting over the European continent. Masting in beech shows distance-decay, but significant synchrony is maintained at spatial scales of up to 1,500 km. The spatial synchrony of the weather cues that drive interannual variation in reproduction also explains the regional spatial synchrony of masting. Proximity played no apparent role in influencing beech masting synchrony after controlling for synchrony in environmental variation. Synchrony of beech reproduction shows a clear biogeographical pattern, decreasing from the northwest to southeast Europe. Synchrony networks for weather cues resemble networks for beech masting, indicating that the geographical structure of weather synchrony underlies the biogeography of masting synchrony. Our results support the hypothesis that environmental factors, the Moran effect, are key drivers of spatial synchrony in beech seed production at regional scales. The geographical patterns of regional synchronization of masting have implications for regional forest production, gene flow, carbon cycling, disease dynamics, biodiversity, and conservation

Macroevolutionary consequences of mast seeding.

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 (CVp) 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 CVp and regional-scale synchrony (Sr) in seed production, that is, there were unimodal correlations. There was no support for monotonic correlations between either CVp or Sr 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'

Growth of male and female Araucaria araucana trees respond differently to regional mast events, creating sex-specific patterns in their tree-ring chronologies

Araucaria araucana is a dioecious evergreen conifer endemic from temperate forests of south Argentina and Chile. It is a long-lived species (maximum age > 1000 years), and it presents a high potential for tree-ring based climate reconstructions. However, the species’ dioecious habit can result in distinct sex-specific growth patterns, which introduce novel challenges in the interpretation of tree-ring chronology variations. We used a network of 10 tree-ring chronologies from northwest Patagonia (Argentina) to analyze sex-specific growth patterns in A. araucana and, for the first time, demonstrate that they result from the contrasting responses of ring width index of male (RWImale) and female (RWIfemale) trees to regional mast events (years with high seed production). During the year of seed maturation and seed dispersal, the growth of females was strongly and significantly reduced, while a growth response of similar magnitude was found in male trees in the previous year, corresponding to the year of pollination. We interpret these growth responses as representing contrasting allocation shifts between growth and reproduction in males and females. The sex-specific growth responses associated with mast events resulted in a particularly strong and distinct signal in a RWImale–RWIfemale chronology. Male and female tree-ring chronologies shared a strong common signal, and responded similarly (but not exactly) to broad-scale climatic conditions in the growing season. Our results indicate that sex-specific tree-ring chronologies can be used to isolate mast events in A. araucana chronologies, providing an opportunity to develop unique multi-century reconstructions of large mast events, and improve dendroclimatic calibration for this species.Fil: Hadad, Martín Ariel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - San Juan. Centro de Investigaciones de la Geosfera y Biosfera. Universidad Nacional de San Juan. Facultad de Ciencias Exactas Físicas y Naturales. Centro de Investigaciones de la Geosfera y Biosfera; ArgentinaFil: Roig Junent, Fidel Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales. Provincia de Mendoza. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales. Universidad Nacional de Cuyo. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales; Argentina. Universidad Mayor; ChileFil: Arco Molina, Julieta Gabriela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales. Provincia de Mendoza. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales. Universidad Nacional de Cuyo. Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales; ArgentinaFil: Hacket Pain, Andrew. University of Liverpool; Reino Unid

Temperature and masting control Norway spruce growth, but with high individual tree variability

Tree growth and reproduction are subject to trade-offs in resource allocation. At the same time, they are both influenced by climate. In this study, we combined long records of reproductive effort at the individual- (29 years), population- (41 years) and regional (up to 53 years) scale, and tree ring chronologies, to investigate the effects of climate and reproductive allocation on radial growth in an Alpine Norway spruce forest. Seed and cone production was highly variable between years (mean individual CV = 1.39, population CV = 1.19), but showed high reproductive synchrony between individuals (mean inter-tree correlation = 0.72). No long-term trend in reproductive effort was detected over four decades of observations. At the stand scale, cone production was dominated by a small number of individuals (\u201csuper-producers\u201d), who remained dominant over three decades. Individual tree growth responded positively to summer temperature, but the response to cone production varied between individual trees. Consequently, we found some evidence that mast years were associated with a divergence in growth between high and low cone producing individuals, and a decline in within-population growth synchrony. At the population level we found limited evidence of a relationship between growth and reproduction. Radial growth was lower than average in some mast years, but not in others. This was partly explained by summer temperature during the year of growth, with growth reductions restricted to mast years that coincided with colder than average summers. Regional mast records and tree ring chronologies provided some support to indicate that our results were consistent in other spruce stands, although the effect of mast years on growth appeared to vary between sites. Tree ring variation at the individual and population level, and between-tree growth synchrony are influenced by masting, and consequently dendrochronologists should consider both the occurrence of masting and the individual differences in reproductive effort when interpreting tree ring datasets. Our results also indicate that tree ring chronologies contain information to facilitate reconstruction of mast events, which will help address outstanding questions regarding the future response of masting to climate change

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

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