Inter-annual and decadal changes in teleconnections drive continental-scale synchronization of tree reproduction

Climate teleconnections drive highly variable and synchronous seed production (masting) over large scales. Disentangling the effect of high-frequency (inter-annual variation) from low-frequency (decadal trends) components of climate oscillations will improve our understanding of masting as an ecosystem process. Using century-long observations on masting (the MASTREE database) and data on the Northern Atlantic Oscillation (NAO), we show that in the last 60 years both high-frequency summer and spring NAO, and low-frequency winter NAO components are highly correlated to continent-wide masting in European beech and Norway spruce. Relationships are weaker (non-stationary) in the early twentieth century. This finding improves our understanding on how climate variation affects large-scale synchronization of tree masting. Moreover, it supports the connection between proximate and ultimate causes of masting: indeed, large-scale features of atmospheric circulation coherently drive cues and resources for masting, as well as its evolutionary drivers, such as pollination efficiency, abundance of seed dispersers, and natural disturbance regimes

Climate Change Strengthens Selection for Mast Seeding in European Beech

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

Climate warming causes mast seeding to break down by reducing sensitivity to weather cues

Climate change is altering patterns of seed production worldwide with consequences for population recruitment and migration potential. For the many species that regenerate through synchronized, quasiperiodic reproductive events termed masting, these changes include decreases in the synchrony and interannual variation in seed production. This breakdown in the occurrence of masting features harms reproduction by decreasing the efficiency of pollination and increasing seed predation. Changes in masting are often paralleled by warming temperatures, but the underlying proximate mechanisms are unknown. We used a unique 39-year study of 139 European beech (Fagus sylvatica) trees that experienced masting breakdown to track the seed developmental cycle and pinpoint phases where weather effects on seed production have changed over time. A cold followed by warm summer led to large coordinated flowering efforts among plants. However, trees failed to respond to the weather signal as summers warmed and the frequency of reproductive cues changed fivefold. Less synchronous flowering resulted in less efficient pollination that further decreased the synchrony of seed maturation. As global temperatures are expected to increase this century, perennial plants that fine-tune their reproductive schedules based on temperature cues may suffer regeneration failures

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.EEA Santa CruzFil: Hacket-Pain, Andrew. University of Liverpool. School of Environmental Sciences. Department of Geography and Planning; Reino UnidoFil: Foest, Jessie J. University of Liverpool. School of Environmental Sciences. Department of Geography and Planning; Reino UnidoFil: Pearse, Ian S. U.S. Fort Collins Science Center. Geological Survey; Estados UnidosFil: LaMontagne, Jalene M. DePaul University. Department of Biological Sciences; Estados UnidosFil: Koenig, Walter D. University of California Berkeley. Hastings Reservation; Estados UnidosFil: Vacchiano, Giorgio. University of Milan. Milan Department of Agricultural and Environmental Sciences; Italia.Fil: Bogdziewicz, Michał. Adam Mickiewicz University. Faculty of Biology. Institute of Environmental Biology; PoloniaFil: Bogdziewicz, Michał. University Grenoble Alpes. INRAE, LESSEM; FranciaFil: Caignard, Thomas. Université Bordeaux. INRAE, BIOGECO; FranciaFil: Celebias, Paulina. Adam Mickiewicz University. Faculty of Biology. Institute of Environmental Biology; PoloniaFil: Peri, Pablo Luis. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Santa Cruz; Argentina.Fil: Peri, Pablo Luis. Universidad Nacional de la Patagonia Austral; Argentina.Fil: Peri, Pablo Luis. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina.Fil: Ascoli, Davide. University of Torino. Department of Agricultural. Forest and Food Sciences (DISAFA); ItaliaFil: Gallo, Leonardo Ariel. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Bariloche; ArgentinaFil: Gallo, Leonardo Ariel. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones Forestales y Agropecuarias Bariloche; ArgentinaFil: Marchelli, Paula. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Bariloche; ArgentinaFil: Marchelli, Paula. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Instituto de Investigaciones Forestales y Agropecuarias Bariloche; Argentin

Climatically controlled reproduction drives interannual growth variability in a temperate tree species

Climatically controlled allocation to reproduction is a key mechanism by which climate influences tree growth and may explain lagged correlations between climate and growth. We used continent‐wide datasets of tree‐ring chronologies and annual reproductive effort in Fagus sylvatica from 1901 to 2015 to characterise relationships between climate, reproduction and growth. Results highlight that variable allocation to reproduction is a key factor for growth in this species, and that high reproductive effort (‘mast years’) is associated with stem growth reduction. Additionally, high reproductive effort is associated with previous summer temperature, creating lagged climate effects on growth. Consequently, understanding growth variability in forest ecosystems requires the incorporation of reproduction, which can be highly variable. Our results suggest that future response of growth dynamics to climate change in this species will be strongly influenced by the response of reproduction.Additional co-authors: Ernst van der Maaten, Marieke van der Maaten‐Theunissen, Lena Muffler, Renzo Motta, Catalin‐Constantin Roibu, Ionel Popa, Tobias Scharnweber, Robert Weigel, Martin Wilmking, Christian S Zan

Two centuries of masting data for European beech and Norway spruce across the European continent

Tree masting is one of the most intensively studied ecological processes. It affects nutrient fluxes of trees, regeneration dynamics in forests, animal population densities, and ultimately influences ecosystem services. Despite a large volume of research focused on masting, its evolutionary ecology, spatial and temporal variability and environmental drivers are still matter of debate. Understanding the proximate and ultimate causes of masting at broad spatial and temporal scales will enable us to predict tree reproductive strategies and their response to changing environment. Here we provide broad spatial (distribution range-wide) and temporal (century) masting data for the two main masting tree species in Europe, European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) H. Karst.). We collected masting data from a total of 359 sources through an extensive literature review and from unpublished surveys. The dataset has a total of 1747 series and 18348 yearly observations from 28 countries and covering a time span of years 1677-2016 and 1791-2016 for beech and spruce, respectively. For each record, the following information is available: identification code; species; year of observation; proxy of masting (flower, pollen, fruit, seed, dendrochronological reconstructions); statistical data type (ordinal, continuous); data value; unit of measurement (only in case of continuous data); geographical location (country, Nomenclature of Units for Territorial Statistics NUTS-1 level, municipality, coordinates); first and last record year and related length; type of data source (field survey, peer reviewed scientific literature, grey literature, personal observation); source identification code; date when data were added to the database; comments. To provide a ready-to-use masting index we harmonized ordinal data into five classes. Furthermore, we computed an additional field where continuous series with length >4 years where converted into a five classes ordinal index. To our knowledge, this is the most comprehensive published database on species-specific masting behaviour. It is useful to study spatial and temporal patterns of masting and its proximate and ultimate causes, to refine studies based on tree-ring chronologies, to understand dynamics of animal species and pests vectored by these animals affecting human health, and it may serve as calibration-validation data for dynamic forest models.The paper was partly funded by the “Fondo di Ricerca Locale 2015-2016” of the University of Torino and by the Stiftelsen Stina Werners fond (grant SSWF 10-1/29-3 to I.D.)

The influence of masting phenomenon on growth-climate relationships in trees: Explaining the influence of previous summers' climate on ring width

Tree growth is frequently linked to weather conditions prior to the growing season but our understanding of these lagged climate signatures is still poorly developed. We investigated the influence of masting behaviour on the relationship between growth and climate in European Beech (Fagus sylvatica L.) using a rare long-term dataset of seed production and a new regional tree ring chronology. Fagus sylvatica is a masting species with synchronous variations in seed production which are strongly linked to the temperature in the previous two summers. We noted that the weather conditions associated with years of heavy seed production (mast years) were the same as commonly reported correlations between growth and climate for this species. We tested the hypothesis that a trade-off between growth and reproduction in mast years could be responsible for the observed lagged correlations between growth and previous summers' temperatures. We developed statistical models of growth based on monthly climate variables, and show that summer drought (negative correlation), temperature of the previous summer (negative) and temperature of the summer 2 years previous (positive) are significant predictors of growth. Replacing previous summers' temperature in the model with annual seed production resulted in a model with the same predictive power, explaining the same variance in growth. Masting is a common behaviour in many tree species and these findings therefore have important implications for the interpretation of general climate-growth relationships. Lagged correlations can be the result of processes occurring in the year of growth (that are determined by conditions in previous years), obviating or reducing the need for 'carry-over' processes such as carbohydrate depletion to be invoked to explain this climate signature in tree rings. Masting occurs in many tree species and these findings therefore have important implications for the interpretation of general climate-growth relationships