Abstract
The benefits of masting (volatile, quasi-synchronous seed production at lagged intervals) include satiation of seed predators, but these benefits come with a cost to mutualist pollen and seed dispersers. If the evolution of masting represents a balance between these benefits and costs, we expect mast avoidance in species that are heavily reliant on mutualist dispersers. These effects play out in the context of variable climate and site fertility among species that vary widely in nutrient demand. Meta-analyses of published data have focused on variation at the population scale, thus omitting periodicity within trees and synchronicity between trees. From raw data on 12 million tree-years worldwide, we quantified three components of masting that have not previously been analysed together: (i) volatility, defined as the frequency-weighted year-to-year variation; (ii) periodicity, representing the lag between high-seed years; and (iii) synchronicity, indicating the tree-to-tree correlation. Results show that mast avoidance (low volatility and low synchronicity) by species dependent on mutualist dispersers explains more variation than any other effect. Nutrient-demanding species have low volatility, and species that are most common on nutrient-rich and warm/wet sites exhibit short periods. The prevalence of masting in cold/dry sites coincides with climatic conditions where dependence on vertebrate dispersers is less common than in the wet tropics. Mutualist dispersers neutralize the benefits of masting for predator satiation, further balancing the effects of climate, site fertility and nutrient demands.
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Data availability
Seed production data are available at the Duke Data Repository https://doi.org/10.7924/r4348ph5t. Species traits are downloaded from TRY Plant Trait database at https://www.try-db.org/TryWeb/Home.php. Cation exchange capacity data were obtained at https://soilgrids.org/. Climate data were extracted from Terraclimate at http://www.climatologylab.org/ and CHELSA at https://chelsa-climate.org/.
Code availability
R statistical software v.4.0.2 was used in this work. All analyses used published R packages, with details stated in Methods. MASTIF includes code in R and C++, which is published on CRAN at https://cran.r-project.org/web/packages/mastif/index.html.
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Acknowledgements
For access to sites and logistical support, we thank the National Ecological Observatory Network (NEON). The project has been funded continuously since 1992 by National Science Foundation grants to J.S.C., most recently DEB-1754443, and by the Belmont Forum (1854976), NASA (AIST16-0052, AIST18-0063) and the Programme d’Investissement d’Avenir under project FORBIC (18-MPGA-0004)(‘Make Our Planet Great Again’). T.Q. acknowledges support from the start-up funds provided by Pennsylvania State University. Puerto Rico data were funded by NSF grants to M.U., most recently DEB 0963447 and LTREB 11222325. Data from the Andes Biodiversity and Ecosystem Research Group were funded by the Gordon and Betty Moore Foundation and NSF LTREB 1754647 to M.S. Additional funding to M.Z. came from the W. Szafer Institute of Botany of the Polish Academy of Sciences and the Polish National Science Foundation (2019/33/B/NZ8/0134). M.B. was supported by Polish National Agency for Academic Exchange Bekker programme PPN/BEK/2020/1/00009/U/00001. F.R.S. was supported by FEDER 2014–2020 and Consejeria de Economia, Conocimiento, Empresas y Universidad of Junta de Andalucia (grant US-1381388). J.F.F.’s data remain accessible through NSF LTER DEB-1440409. USDA Forest Service and USGS research were funded by those agencies. Any use of trade, firm or product names does not imply endorsement by the US Government.
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J.S.C. and T.Q. designed the study, performed analyses and wrote the paper. J.S.C. compiled the MASTIF data and wrote the MASTIF model and software. M.B., B.C., V.J. and G.K. co-wrote the paper. T.Q., M.-C.A., D.A., Y.B., M.B., T.B., R.B., T.C., M.C., R.C., S.D.C., J.J.C., C.-H.C-Y., J.C., F.C., B.C., A.C., A.J.D., N.D., S.D., M.D., L.D., J.M.E., T.J.F., W.F.-R., J.F.F., C.A.G., G.S.G., G.G., C.H.G., A.G., Q.G., A.H.-P., A.H., Q.H., J.H., K.H., I.I., J.F.J., V.J., T.K., J.M.H.K., G.K., H.K., J.G.A.L., J.M.L., F.L., T.L., J.-M.L., J.A.L., D.M., A.M., E.J.B.M., C.M.M., E.M., R.M., J.A.M., T.A.N., S.N., M.N., M.O., R.P., I.S.P., I.M.P.-R., L.P., T.P., J.P., M.D.R., C.D.R., K.C.R., F.R.-S., P.S., J.D.S., C.L.S., B.S., S. Sharma, M. Shibata, M. Silman, M.A.S., N.L.S., J.N.S., S. Sutton, J.J.S., M. Swift, P.A.T., M.U., G.V., A.V.W., T.G.W., A.P.W., S.J.W., K.Z., J.K.Z., M.Z. and J.S.C. contributed data and revised the paper.
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Extended data
Extended Data Fig. 1 MASTIF sites.
The summary of MASTIF sites with symbol size proportional to observations. Detailed data distribution is in the supplementary csv file.
Extended Data Fig. 2 Correlations between volatility and quasi-periodicity.
Correlations between volatility and quasi-periodicity at ecoregion/species level within phylogenetic groups (see methods). Top-left labels include Pearson’s correlation coefficients (two-sided test), including those that are significant (~, *, **, and ***) indicate 0.1, 0.05, 0.01, and 0.001 significant level, respectively. Shading represents positive (brown) and negative (teal) correlations. Colors of the points indicate different genera within each phylogenetic group. Across all ecoregion/species level observations, volatility is negatively correlated with quasi-periodicity (-0.28, 95% CI = (-0.36,-0.21)).
Extended Data Fig. 3 Correlations between volatility and synchronicity.
Correlations between volatility and synchronicity at the ecoregion-species level within phylogenetic groups (see Methods). Symbology follows the extended data fig. 2. Volatility is negatively associated with synchronicity for animal pollinated (AP) species (-0.17, 95% CI = (-0.06,-0.26)) while positively associated with synchronicity for wind pollinated (WP) species (0.26, 95% CI = (0.13,0.39)). Blue lines in AP and WP panels indicate linear regression.
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Qiu, T., Aravena, MC., Ascoli, D. et al. Masting is uncommon in trees that depend on mutualist dispersers in the context of global climate and fertility gradients. Nat. Plants 9, 1044–1056 (2023). https://doi.org/10.1038/s41477-023-01446-5
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DOI: https://doi.org/10.1038/s41477-023-01446-5
