• Energy Research

Climate change is altering patterns of seed production worldwide [1-4], but the potential for evolutionary responses to these changes is poorly understood. Masting (synchronous, annually variable seed production by plant populations) is selectively beneficial through economies of scale that decrease the cost of reproduction per surviving offspring [5-7]. Masting is particularly widespread in temperate trees [8, 9] impacting food webs, macronutrient cycling, carbon storage, and human disease risk [10-12], so understanding its response to climate change is important. Here, we analyze inter-individual variability in plant reproductive patterns and two economies of scale-predator satiation and pollination efficiency-and document how natural selection acting upon them favors masting. Four decades of observations for European beech (Fagus sylvatica) show that predator satiation and pollination efficiency select for individuals with higher inter-annual variability of reproduction and higher reproductive synchrony between individuals. This result confirms the long-standing theory that masting, a population-level phenomenon, is generated by selection on individuals. Furthermore, recent climate-driven increases in mean seed production have increased selection pressure from seed predators but not from pollination efficiency. Natural selection is thus acting to restore the fitness benefits of masting, which have previously decreased under a warming climate [13]. However, selection will likely take far longer (centuries) than climate warming (decades), so in the short-term, tree reproduction will be reduced because masting has become less effective at satiating seed predators. Over the long-term, evolutionary responses to climate change could potentially increase inter-annual variability of seed production of masting species.

AbstractClimate 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.

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.This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

AbstractIndirect climate effects on tree fecundity that come through variation in size and growth (climate-condition interactions) are not currently part of models used to predict future forests. Trends in species abundances predicted from meta-analyses and species distribution models will be misleading if they depend on the conditions of individuals. Here we find from a synthesis of tree species in North America that climate-condition interactions dominate responses through two pathways, i) effects of growth that depend on climate, and ii) effects of climate that depend on tree size. Because tree fecundity first increases and then declines with size, climate change that stimulates growth promotes a shift of small trees to more fecund sizes, but the opposite can be true for large sizes. Change the depresses growth also affects fecundity. We find a biogeographic divide, with these interactions reducing fecundity in the West and increasing it in the East. Continental-scale responses of these forests are thus driven largely by indirect effects, recommending management for climate change that considers multiple demographic rates.

Many plants benefit from synchronous year-to-year variation in seed production, called masting. Masting benefits plants because it increases the efficiency of pollination and satiates predators, which reduces seed loss. Here, using a 39-year-long dataset, we show that climate warming over recent decades has increased seed production of European beech but decreased the year-to-year variability of seed production and the reproductive synchrony among individuals. Consequently, the benefit that the plants gained from masting has declined. While climate warming was associated with increased reproductive effort, we demonstrate that less effective pollination and greater losses of seeds to predators offset any benefits to the plants. This shows that an apparently simple benefit of climate warming unravels because of complex ecological interactions. Our results indicate that in masting systems, the main beneficiaries of climate-driven increases in seed production are seed predators, not plants.

AbstractMasting—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.

AbstractSpatial 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.