Dry Climate Filters Gymnosperms but Not Angiosperms through Seed Mass

In the context of climate change in recent years, the fate of woody plant seed has an important impact on forest regeneration. Seed mass is an important reproductive strategy of plants. There are huge differences between gymnosperms (mainly conifers) and angiosperms (flowering plants) in terms of reproduction and hydraulic strategies; however, little is known about changes in seed mass along climate aridity gradients between taxonomical groups such as gymnosperms and angiosperms, which limit our understanding on the fate of woody plants under warming-induced climate drying. We collected seed mass data from a total of 2575 woody plant individuals, including 145 species of gymnosperms and 1487 species of angiosperms, across different climatic zones in China. We mapped the distribution pattern of gymnosperm and angiosperm seed mass in China, with angiosperms being maximal near the 400 mm iso-precipitation line. Our phylogenetic analysis results show that seed mass exhibited significant phylogenic signals (p < 0.001) and was also strongly influenced by functional traits (growth type, fruit type, and dispersal mode). The results of linear regression and hierarchical partitioning analysis showed a stronger correlation between gymnosperm seed mass and environmental factors, and a higher independent aridity index effect on gymnosperm seed mass than angiosperm seed mass. The different patterns of seed mass along a climate aridity gradient between gymnosperms and angiosperms may point to different future fates for these two taxonomic groups, while the higher sensitivity of gymnosperm seed mass to environmental conditions may reduce their reproductive rate under the background of climate warming and drying.

[1]  R. Zomer,et al.  Version 3 of the Global Aridity Index and Potential Evapotranspiration Database , 2022, Scientific Data.

[2]  Anping Chen,et al.  Timing and Order of Extreme Drought and Wetness Determine Bioclimatic Sensitivity of Tree Growth , 2022, Earth's Future.

[3]  Xiuchen Wu,et al.  Modeling vegetation greenness and its climate sensitivity with deep‐learning technology , 2021, Ecology and evolution.

[4]  E. Notivol,et al.  Selection patterns on early-life phenotypic traits in Pinus sylvestris are associated with precipitation and temperature along a climatic gradient in Europe. , 2020, The New phytologist.

[5]  P. Ciais,et al.  Temporal trade-off between gymnosperm resistance and resilience increases forest sensitivity to extreme drought , 2020, Nature Ecology & Evolution.

[6]  J. Linares,et al.  Low growth resilience to drought is related to future mortality risk in trees , 2020, Nature Communications.

[7]  Renske E. Onstein,et al.  Darwin's second 'abominable mystery': trait flexibility as the innovation leading to angiosperm diversity. , 2020, The New phytologist.

[8]  H. Qian,et al.  V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants , 2019, Ecography.

[9]  N. Emery,et al.  Environmental factors influencing fruit production and seed biology of the critically endangered Persoonia pauciflora (Proteaceae) , 2019, Folia Geobotanica.

[10]  A. Nicotra,et al.  A research agenda for seed-trait functional ecology. , 2018, The New phytologist.

[11]  Stephen A. Smith,et al.  Constructing a broadly inclusive seed plant phylogeny. , 2018, American journal of botany.

[12]  Stephen E. Fick,et al.  WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas , 2017 .

[13]  P. Shi,et al.  Spatiotemporal patterns of annual and seasonal precipitation extreme distributions across China and potential impact of tropical cyclones , 2017 .

[14]  R. Hubbard,et al.  Climate change may restrict dryland forest regeneration in the 21st century. , 2017, Ecology.

[15]  S. Richardson,et al.  Soil–climate interactions explain variation in foliar, stem, root and reproductive traits across temperate forests , 2016 .

[16]  Eike Lena Neuschulz,et al.  Pollination and seed dispersal are the most threatened processes of plant regeneration , 2016, Scientific Reports.

[17]  F. Parcy,et al.  Evolution of the Plant Reproduction Master Regulators LFY and the MADS Transcription Factors: The Role of Protein Structure in the Evolutionary Development of the Flower , 2016, Front. Plant Sci..

[18]  S. Piao,et al.  Spatial patterns of climatological temperature lapse rate in mainland China: A multi–time scale investigation , 2015 .

[19]  T. Brodribb,et al.  Conifer species adapt to low-rainfall climates by following one of two divergent pathways , 2014, Proceedings of the National Academy of Sciences.

[20]  Nadejda A. Soudzilovskaia,et al.  Which is a better predictor of plant traits: temperature or precipitation? , 2014 .

[21]  G. B. Williamson,et al.  Seed and fruit tradeoffs – the economics of seed packaging in Amazon pioneers , 2014 .

[22]  J. Kattge,et al.  Whole‐plant trait spectra of North American woody plant species reflect fundamental ecological strategies , 2013 .

[23]  C. Leuschner,et al.  Increased Summer Temperatures Reduce the Growth and Regeneration of Larix sibirica in Southern Boreal Forests of Eastern Kazakhstan , 2013, Ecosystems.

[24]  A. Hamann,et al.  Recent declines of Populus tremuloides in North America linked to climate , 2013 .

[25]  A. Nardini,et al.  Global convergence in the vulnerability of forests to drought , 2012, Nature.

[26]  Daniel M. Johnson,et al.  Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? , 2012, Plant science : an international journal of experimental plant biology.

[27]  M. Adams,et al.  Disentangling respiratory acclimation and adaptation to growth temperature by Eucalyptus. , 2012, The New phytologist.

[28]  Liam J. Revell,et al.  phytools: an R package for phylogenetic comparative biology (and other things) , 2012 .

[29]  Fiona J. Thomson,et al.  Seed dispersal distance is more strongly correlated with plant height than with seed mass , 2011 .

[30]  M. Lawes,et al.  Costs of resprouting are traded off against reproduction in subtropical coastal dune forest trees , 2011, Plant Ecology.

[31]  Jingyun Fang,et al.  Atlas of Woody Plants in China , 2011 .

[32]  Brody Sandel,et al.  Contrasting trait responses in plant communities to experimental and geographic variation in precipitation. , 2010, The New phytologist.

[33]  Pedro P. Olea,et al.  Estimating and Modelling Bias of the Hierarchical Partitioning Public-Domain Software: Implications in Environmental Management and Conservation , 2010, PloS one.

[34]  O. Eriksson,et al.  Seed mass and the evolution of fleshy fruits in angiosperms , 2010 .

[35]  N. McDowell,et al.  A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests , 2010 .

[36]  W. Friedman.  The meaning of Darwin's 'abominable mystery'. , 2009, American journal of botany.

[37]  Karl J Niklas,et al.  Darwin's second 'abominable mystery': Why are there so many angiosperm species? , 2009, American journal of botany.

[38]  D. Hertel,et al.  Above- and below-ground response by Nothofagus pumilio to climatic conditions at the transition from the steppe–forest boundary to the alpine treeline in southern Patagonia, Argentina , 2008 .

[39]  S. Lavorel,et al.  Impact of abundance weighting on the response of seed traits to climate and land use , 2008 .

[40]  Ü. Niinemets,et al.  Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs , 2006 .

[41]  Campbell O. Webb,et al.  Factors that shape seed mass evolution. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Campbell O. Webb,et al.  A Brief History of Seed Size , 2005, Science.

[43]  Bruce H. Tiffney,et al.  VERTEBRATE DISPERSAL OF SEED PLANTS THROUGH TIME , 2004 .

[44]  D. Marks,et al.  The dynamics of rainfall interception by a seasonal temperate rainforest , 2004 .

[45]  C. Dickman,et al.  Geographical gradients in seed mass in relation to climate , 2004 .

[46]  Mark Westoby,et al.  A leaf-height-seed (LHS) plant ecology strategy scheme , 1998, Plant and Soil.

[47]  T. Callaghan,et al.  Environmental constraints on the growth, photosynthesis and reproductive development of Dryas octopetala at a high Arctic polar semi-desert, Svalbard , 1995, Oecologia.

[48]  D. Coomes,et al.  Colonization, tolerance, competition and seed-size variation within functional groups , 2003 .

[49]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[50]  T. Curt,et al.  Seed mass, seed dispersal capacity, and seedling performance in a Pinus sylvestris population , 2003 .

[51]  Peter J. Bellingham,et al.  Resprouting as a life history strategy in woody plant communities , 2000 .

[52]  O. Eriksson,et al.  Seed Size and Dispersal Systems of Early Cretaceous Angiosperms from Famalicão, Portugal , 2000, International Journal of Plant Sciences.

[53]  M. Pagel.  Inferring the historical patterns of biological evolution , 1999, Nature.

[54]  Richard M. Cowling,et al.  Resprouters vs reseeders in South African forest trees; a model based on forest canopy height , 1997 .

[55]  M. Westoby,et al.  Correlates of seed size variation: A comparison among five temperate floras , 1995 .

[56]  H. G. Baker.  Seed Weight in Relation to Environmental Conditions in California , 1972 .

[57]  John L. Harper,et al.  The Shapes and Sizes of Seeds , 1970 .