Article

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

  • Nature Ecology & Evolution 112851291 (2017)
  • doi:10.1038/s41559-017-0248-x
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Abstract

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.

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References

  1. 1.

    Allen, C. D. et al. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol. Manag. 259, 660–684 (2010).

  2. 2.

    IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) (Cambridge Univ. Press, Cambridge, 2014).

  3. 3.

    McDowell, N. et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178, 719–739 (2008).

  4. 4.

    Adams, H. D. et al. Ecohydrological consequences of drought- and infestation- triggered tree die-off: insights and hypotheses. Ecohydrology 5, 145–159 (2012).

  5. 5.

    Anderegg, W. R. L., Kane, J. M. & Anderegg, L. D. L. Consequences of widespread tree mortality triggered by drought and temperature stress. Nat. Clim. Change 3, 30–36 (2013).

  6. 6.

    McDowell, N. G. et al. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol. Evol. 26, 523–532 (2011).

  7. 7.

    McDowell, N. G. et al. Multi-scale predictions of massive conifer mortality due to chronic temperature rise. Nat. Clim. Change 6, 295–300 (2016).

  8. 8.

    Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Climate 27, 511–526 (2014).

  9. 9.

    Friend, A. D. et al. Carbon residence time dominates uncertainty in terrestrial vegetation responses to future climate and atmospheric CO2. Proc. Natl Acad. Sci. USA 111, 3280–3285 (2014).

  10. 10.

    McDowell, N. G. et al. Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytol. 200, 304–321 (2013).

  11. 11.

    Sala, A., Piper, F. & Hoch, G. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 186, 274–281 (2010).

  12. 12.

    Hartmann, H., Ziegler, W., Kolle, O. & Trumbore, S. Thirst beats hunger – declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol. 200, 340–349 (2013).

  13. 13.

    Quirk, J., McDowell, N. G., Leake, J. R., Hudson, P. J. & Beerling, D. J. Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmosphere carbon dioxide starvation. Am. J. Bot. 100, 582–591 (2013).

  14. 14.

    O’Brien, M. J., Leuzinger, S., Philipson, C. D., Tay, J. & Hector, A. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat. Clim. Change 4, 710–714 (2014).

  15. 15.

    Sevanto, S., McDowell, N. G., Dickman, L. T., Pangle, R. & Pockman, W. T. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 37, 153–161 (2014).

  16. 16.

    Piper, F. I. & Fajardo, A. Carbon dynamics of Acer pseudoplatanus seedlings under drought and complete darkness. Tree Physiol. 36, 1400–1408 (2016).

  17. 17.

    McDowell, N. G. & Sevanto, S. The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytol. 186, 264–266 (2010).

  18. 18.

    Sala, A., Woodruff, D. R. & Meinzer, F. C. Carbon dynamics in trees: feast or famine? Tree Physiol. 32, 764–775 (2012).

  19. 19.

    Fatichi, S., Leuzinger, S. & Koerner, C. Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol. 201, 1086–1095 (2014).

  20. 20.

    Hartmann, H. Carbon starvation during drought-induced tree mortality – are we chasing a myth? J. Plant Hydraul. 2, e005 (2015).

  21. 21.

    Körner, C. Paradigm shift in plant growth control. Curr. Opin. Plant Biol. 25, 107–114 (2015).

  22. 22.

    Martínez-Vilalta, J. et al. Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol. Monogr. 86, 495–516 (2016).

  23. 23.

    Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752–755 (2012).

  24. 24.

    Skelton, R. P., West, A. G. & Dawson, T. E. Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proc. Natl Acad. Sci. USA 112, 5744–5749 (2015).

  25. 25.

    Poorter, L. & Markesteijn, L. Seedling traits determine drought tolerance of tropical tree species. Biotropica 40, 321–331 (2008).

  26. 26.

    Meinzer, F. C., Johnson, D. M., Lachenbruch, B., McCulloh, K. A. & Woodruff, D. R. Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct. Ecol. 23, 922–930 (2009).

  27. 27.

    McDowell, N. G. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 155, 1051–1059 (2011).

  28. 28.

    Mitchell, P. J., O’Grady, A. P., Tissue, D. T., Worledge, D. & Pinkard, E. A. Co-ordination of growth, gas exchange and hydraulics define the carbon safety margin in tree species with contrasting drought strategies. Tree Physiol. 34, 443–458 (2014).

  29. 29.

    Mencuccini, M., Minunno, F., Salmon, Y., Martinez-Vilalta, J. & Holtta, T. Coordination of physiological traits involved in drought-induced mortality of woody plants. New Phytol. 208, 396–409 (2015).

  30. 30.

    O’Brien, M. J., Burslem, D., Caduff, A., Tay, J. & Hector, A. Contrasting nonstructural carbohydrate dynamics of tropical tree seedlings under water deficit and variability. New Phytol. 205, 1083–1094 (2015).

  31. 31.

    Landhäusser, S. M. & Lieffers, V. J. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees-Struct. Funct. 26, 653–661 (2012).

  32. 32.

    Brodribb, T. J., McAdam, S. A. M., Jordan, G. J. & Martins, S. C. V. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc. Natl Acad. Sci. USA 111, 14489–14493 (2014).

  33. 33.

    Anderegg, W. R. L. et al. Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc. Natl Acad. Sci. USA 113, 5024–5029 (2016).

  34. 34.

    Brodribb, T. J. & Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575–584 (2009).

  35. 35.

    Anderegg, W. R. L. et al. Tree mortality predicted from drought-induced vascular damage. Nat. Geosci. 8, 367–371 (2015).

  36. 36.

    Sperry, J. S. & Love, D. M. What plant hydraulics can tell us about responses to climate-change droughts. New Phytol. 207, 14–27 (2015).

  37. 37.

    Zeppel, M. J. B. et al. Drought and resprouting plants. New Phytol. 206, 583–589 (2015).

  38. 38.

    Hartmann, H. & Trumbore, S. Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know. New Phytol. 211, 386–403 (2016).

  39. 39.

    Oliva, J., Stenlid, J. & Martinez-Vilalta, J. The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol. 203, 1028–1035 (2014).

  40. 40.

    Anderegg, W. R. L. et al. Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol. 208, 674–683 (2015).

  41. 41.

    Johnson, D. M., McCulloh, K. A., Woodruff, D. R. & Meinzer, F. C. Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Sci. 195, 48–53 (2012).

  42. 42.

    Garcia-Forner, N. et al. Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation. Plant Cell Environ. 39, 38–49 (2016).

  43. 43.

    Martínez-Vilalta, J. & Garcia-Forner, N. Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant Cell Environ. 40, 962–976 (2016).

  44. 44.

    Allen, C. D., Breshears, D. D. & McDowell, N. G. On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, 129 (2015).

  45. 45.

    Adams, H. D. et al. Empirical and process-based approaches to climate-induced forest mortality models. Front. Plant Sci. 4, 438 (2013).

  46. 46.

    Mackay, D. S. et al. Interdependence of chronic hydraulic dysfunction and canopy processes can improve integrated models of tree response to drought. Water Resour. Res. 51, 6156–6176 (2015).

  47. 47.

    Sperry, J. S. et al. Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. New Phytol. 212, 577–589 (2016).

  48. 48.

    Sperry, J. S., Adler, F. R., Campbell, G. S. & Comstock, J. P. Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ. 21, 347–359 (1998).

  49. 49.

    Plaut, J. A. et al. Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought. Plant Cell Environ. 35, 1601–1617 (2012).

  50. 50.

    Quentin, A. G. et al. Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol. 35, 1146–1165 (2015).

  51. 51.

    Germino, M. J. A carbohydrate quandary. Tree Physiol. 35, 1141–1145 (2015).

  52. 52.

    Wheeler, J. K. et al. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ. 36, 1938–1949 (2013).

  53. 53.

    Nardini, A., Savi, T., Trifilò, P. & Lo Gullo, M. A. Drought Stress and the Recovery from Xylem Embolism in Woody Plants (Progress in Botany Series, Springer, Berlin, Heidelberg, 2017).

  54. 54.

    Chave, J. et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009).

  55. 55.

    Zanne, A. E. et al. Global Wood Density Database Dryad Digital Repository http://hdl.handle.net/10255/dryad.235 (2009).

  56. 56.

    Kattge, J. et al. TRY - a global database of plant traits. Glob. Change Biol. 17, 2905–2935 (2011).

  57. 57.

    Niinemets, U. Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol. 144, 35–47 (1999).

  58. 58.

    Niinemets, U. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469 (2001).

  59. 59.

    Domec, J. C. & Gartner, B. L. Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees. Trees-Struct. Funct. 15, 204–214 (2001).

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Acknowledgements

This research was supported by the US Department of Energy, Office of Science, Biological and Environmental Research and Office of Science, Next Generation Ecosystem Experiment-Tropics, the Los Alamos National Laboratory LDRD Program, the Pacific Northwest National Laboratory LDRD Program, The EU Euforinno project, the National Science Foundation LTER Program and EF-1340624, EF-1550756 and EAR-1331408, ARC DECRA DE120100518, ARC LP0989881, ARC DP110105102, the Philecology Foundation of Fort Worth, Texas, the Center for Environmental Biology at UC Irvine through a gift from D. Bren and additional funding sources listed in the Supplementary Acknowledgements. We thank A. Boutz, S. Bucci, R. Fisher, A. Meador-Sanchez, R. Meinzer and D. White for discussions on study design, analysis and interpretation of results, and T. Ocheltree for helpful comments on the manuscript. Any use of trade, product or firm names is for descriptive purposes only and does not imply endorsement by the US government.

Author information

Affiliations

  1. Department of Plant Biology, Ecology, and Evolution, Oklahoma State University, Stillwater, OK, 74078, USA

    • Henry D. Adams
  2. Department of Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    • Melanie J. B. Zeppel
  3. The Boden Institute, Charles Perkins Centre, University of Sydney, Sydney, New South Wales, 2006, Australia

    • Melanie J. B. Zeppel
  4. Department of Biology, University of Utah, Salt Lake City, UT, 84112, USA

    • William R. L. Anderegg
    • , David M. Love
    •  & John S. Sperry
  5. Biogeochemical Processes, Max-Planck Institute for Biogeochemistry, Jena, 7745, Germany

    • Henrik Hartmann
  6. Department of Renewable Resources, University of Alberta, Edmonton, AB, T6G 2E3, Canada

    • Simon M. Landhäusser
    • , David A. Galvez
    •  & Uwe G. Hacke
  7. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, 2751, Australia

    • David T. Tissue
  8. Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA

    • Travis E. Huxman
  9. Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA

    • Patrick J. Hudson
    • , Robert E. Pangle
    • , Jennifer A. Plaut
    •  & William T. Pockman
  10. School of Natural Resources, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    • Trenton E. Franz
  11. U.S. Geological Survey, Fort Collins Science Center, New Mexico Landscapes Field Station, Los Alamos, NM, 87544, USA

    • Craig D. Allen
  12. Biology, University of Washington, Seattle, WA, 98195, USA

    • Leander D. L. Anderegg
  13. B2 EarthScience, Biosphere 2, University of Arizona, Tucson, AZ, 85721, USA

    • Greg A. Barron-Gafford
  14. School of Geography & Development, University of Arizona, Tucson, AZ, 85721, USA

    • Greg A. Barron-Gafford
  15. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK

    • David J. Beerling
    •  & Joe Quirk
  16. School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, 85721, USA

    • David D. Breshears
    •  & Darin J. Law
  17. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA

    • David D. Breshears
  18. School of Biology, University of Tasmania, Hobart, Tasmania, 7001, Australia

    • Timothy J. Brodribb
  19. Forest Ecology, Department of Environmental Systems Science, ETH Zurich, Zurich, 8092, Switzerland

    • Harald Bugmann
  20. Department of Plant Pathology, University of California, Davis, CA, 95616, USA

    • Richard C. Cobb
  21. Earth and Environmental Sciences Division, Los Alamos National Laboratory, Los Alamos, NM, 87545, USA

    • Adam D. Collins
    • , L. Turin Dickman
    • , Jordan D. Muss
    • , Sanna Sevanto
    •  & Chonggang Xu
  22. Institute of Ecology and Environmental Science, Nanchang Institute of Technology, Nanchang, Jiangxi, 330099, China

    • Honglang Duan
  23. Department of Botany and Program in Ecology, University of Wyoming, Laramie, WY, 82071, USA

    • Brent E. Ewers
  24. Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, 75007, Sweden

    • Lucía Galiano
  25. Department of Life Sciences, Centre for Functional Ecology, University of Coimbra, Coimbra, 3000-456, Portugal

    • Núria Garcia-Forner
  26. School of Forestry, Northern Arizona University, Flagstaff, AZ, 86011, USA

    • Monica L. Gaylord
    •  & Thomas E. Kolb
  27. Forest Health Protection, R3-Arizona Zone, US Forest Service, Flagstaff, AZ, 86001, USA

    • Monica L. Gaylord
  28. U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, Boise, ID, 83702, USA

    • Matthew J. Germino
  29. Forest Dynamics, Swiss Federal Research Institute WSL, Birmensdorf, 8903, Switzerland

    • Arthur Gessler
  30. Department of Forest Sciences, University of Sao Paulo, Piracicaba, 13418900, Brazil

    • Rodrigo Hakamada
  31. Department of Plant Sciences, University of Oxford, Oxford, OX1 3RB, UK

    • Andy Hector
  32. Environmental Studies Department, University of California Santa Cruz, Santa Cruz, CA, 95064, USA

    • Michael W. Jenkins
  33. Department of Forestry and Wildland Resources, Humboldt State University, Arcata, CA, 95521, USA

    • Jeffrey M. Kane
  34. Louis Calder Center - Biological Field Station and Department of Biological Sciences, Fordham University, Armonk, NY, 10504, USA

    • James D. Lewis
  35. Centre d’Ecologie Fonctionnelle et Evolutive, CNRS, Montpellier, 34293, France

    • Jean-Marc Limousin
  36. U.S. Agency for International Development, Washington, DC, 20001, USA

    • Alison K. Macalady
  37. CREAF, Cerdanyola del Valles, 8193, Spain

    • Jordi Martínez-Vilalta
    •  & Maurizio Mencuccini
  38. Universitat Autònoma Barcelona, Cerdanyola del Valles, 8193, Spain

    • Jordi Martínez-Vilalta
  39. ICREA, Cerdanyola del Valles, Barcelona, 8010, Spain

    • Maurizio Mencuccini
  40. School of GeoSciences, University of Edinburgh, Edinburgh, EH9 3FF, UK

    • Maurizio Mencuccini
  41. CSIRO Land and Water, Hobart, Tasmania, 7005, Australia

    • Patrick J. Mitchell
    • , Anthony P. O’Grady
    •  & Elizabeth A. Pinkard
  42. Estación Experimental de Zonas Áridas, Consejo Superior de Investigaciones Científicas, La Cañada, Almería, E-04120, Spain

    • Michael J. O’Brien
  43. Centro de Investigación en Ecosistemas de la Patagonia, Coyhaique, 5951822, Chile

    • Frida I. Piper
  44. Instituto de Ecología y Biodiversidad, Santiago, 7800003, Chile

    • Frida I. Piper
  45. Department of Biological Sciences, Idaho State University, Pocatello, ID, 83209, USA

    • Keith Reinhardt
  46. School of Agricultural, Forest, Food and Environmental Sciences, University of Basilicata, Potenza, 85100, Italy

    • Francesco Ripullone
  47. Natural Resources Ecology Laboratory, Colorado State University, Fort Collins, CO, 80523, USA

    • Michael G. Ryan
  48. Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523, USA

    • Michael G. Ryan
  49. USDA Forest Service, Rocky Mountain Research Station, Fort Collins, CO, 80526, USA

    • Michael G. Ryan
  50. Division of Biological Sciences, University of Montana, Missoula, MT, 59812, USA

    • Anna Sala
  51. Department of Plant and Soil Sciences, University of Delaware, Newark, DE, 19716, USA

    • Rodrigo Vargas
  52. Irstea, UR RECOVER, Aix en Provence, 13182, France

    • Michel Vennetier
  53. Nicholas School of the Environment, Duke University, Durham, NC, 27708, USA

    • Danielle A. Way
  54. Department of Biology, University of Western Ontario, London, ON, N6A 5B7, Canada

    • Danielle A. Way
  55. Departamento de Ciencias del Agua y Medio Ambiente, Instituto Tecnologico de Sonora, Ciudad Obregon, Sonora, 85000, Mexico

    • Enrico A. Yepez
  56. Pacific Northwest National Laboratory, Richland, WA, 99352, USA

    • Nate G. McDowell

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  62. Search for Nate G. McDowell in:

Contributions

A.D.C., A.H., A.K.M., A.S., B.E.E., C.D.A., C.X.U., D.A.G., D.A.W., D.T.T., G.B.G., H.D.A., H.H., J.A.P., J.D.L., J.M.K., J.M.L., J.S.S., L.D.L.A., L.T.D., M.J.B.Z., M.J.G., M.M., N.G.M., P.J.H., R.C.C., R.V., S.M.L., S.S., T.E.F., T.E.H., T.E.K., U.H., W.R.L.A. and W.T.P. designed the study. A.H., A.O.G., B.E.E., D.A.G., D.D.B., D.J.B., D.M.L., D.T.T., E.A.P., E.A.Y., F.I.P., G.B.G., H.D., H.D.A., H.H., J.A.P., J.D.L., J.M.V., J.Q., J.S.S., K.R., L.D.L.A., L.G.P., L.T.D., M.J.B.Z., M.J.G., M.J.O., M.L.G., N.G.F., N.G.M., P.J.H., P.J.M., R.E.P., S.M.L., S.S., T.E.H., T.E.K., T.J.B., U.H., W.R.L.A. and W.T.P. contributed data. H.D.A., M.J.B.Z., P.J.H. and T.E.F. analysed the data. A.D.C., A.G., A.H., A.K.M., A.O.G., A.S., B.E.E., C.D.A., C.X.U., D.A.W., D.D.B., D.J.B., D.J.L., D.M.L., D.T.T., E.A.P., F.I.P., F.R., G.B.G., H.B., H.D., H.D.A., H.H., J.D.L., J.D.M., J.M.K., J.M.V., J.Q., J.S.S., K.R., L.D.L.A., L.G.P., L.T.D., M.G.R., M.J.B.Z., M.J.G., M.J.O., M.L.G., M.M., M.V., M.W.J., N.G.F., N.G.M., P.J.H., P.J.M., R.C.C., R.V., S.M.L., S.S., T.E.F., T.E.H., T.E.K., U.H., W.R.L.A. and W.T.P. contributed to the discussion of results. A.D.C., A.G., A.H., A.O.G., A.S., B.E.E., C.D.A., C.X.U., D.A.W., D.D.B., D.J.B., D.J.L., D.T.T., E.A.P., F.I.P., F.R., G.B.G., H.B., H.D.A., H.H., J.D.M., J.M.K., J.M.L., J.M.V., K.R., L.D.L.A., L.G.P., L.T.D., M.G.R., M.J.B.Z., M.J.G., M.J.O., M.L.G., M.M., M.V., M.W.J., N.G.F., N.G.M., P.J.M., R.C.C., R.H., R.E.P., R.V., S.M.L., S.S., T.E.H., T.E.K., T.J.B., U.H. and W.R.L.A. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Henry D. Adams.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Methods, Supplementary Discussion, Supplementary References, Supplementary Acknowledgments, Supplementary Tables 1–7, Supplementary Figures 1–6