A 350-million-year legacy of fire adaptation among conifers

Journal of Ecology

Volumn 104, Issue 2, 2016, Pages 352-363

  He, Tianhua ^a   Belcher, Claire M ^b   Lamont, Byron B ^a   Lim, Sim L ^a  

^a CURTIN UNIVERSITY   (Australia)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Ancestral state reconstruction; Carboniferous; Conifer; Fire adaptation; Fossil; Permian; Plant climate interactions; Resprouting; Seasonality; Serotiny

Indexed keywords

ADAPTATION; ANCESTRY; CARBONIFEROUS; CHARCOAL; EVOLUTIONARY BIOLOGY; FIRE HISTORY; FOSSIL RECORD; PERMIAN; PHYLOGENETICS; RECONSTRUCTION; RESPROUTING; SEASONALITY; SEROTINY; WOODY PLANT;

CONIFEROPHYTA; EMBRYOPHYTA;

EID: 84958897973     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12513     Document Type: Article

References (85)

1. Ahlgren, C.E. (1974) Effects of fire on temperate forests: North Central United States. Fire and Ecosystems (eds T.T. Kozlowski & C.E. Ahlgren ), pp. 195-312. Academic Press, New York, NY, USA.
2. Allen, P. (1998) Purbeck-Wealden (early Cretaceous) climates. Proceedings of the Geologists' Association, 109, 197-236.
3. Axelrod, D.I. (1980) History of the maritime closed-cone pines, Alta and Baja California, Vol. 120, pp. 1-143. University of California, Los Angeles. Publications in Geological Sciences.
4. Beaufait, W.R. (1960) Some effects of high temperatures on the cones and seeds of jack pine. Forestry Science, 6, 194-199.
5. Beerling, D.J., Chaloner, W.G. & Woodward, F.I. (1998) Preface to vegetation-climate-atmosphere interactions: past present and future. Philosophical Transactions of the Royal Society: Biological Sciences, 353, 3-4.
6. Belcher, C.M., Collinson, M.E. & Scott, A.C. (2013) A 450-million-year history of fire. Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. C.M. Belcher ), pp. 229-249. Wiley-Blackwell, Oxford, UK.
7. Belcher, C.M., Yearsley, J.M., Hadden, R.M., McElwain, J.C. & Rein, G. (2010) Baseline intrinsic flammability of Earth's ecosystems estimated from paleoatmospheric oxygen over the past 350 million years. Proceedings of the National Academy of Sciences, 107, 22448-22453.
8. Berner, R.A. (2009) GEOCARBSULF: phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. American Journal of Science, 309, 603-606.
9. Bond, W.J. & Scott, A.C. (2010) Fire and the spread of flowering plants in the Cretaceous. New Phytologist, 188, 1137-1150.
10. Bowman, D.M.J.S., Balch, J.K., Artaxo, P., Bond, W.J., Carlson, J.M., Cochrane, M.A., D' Antonio, C.M., DeFries, R.S., Doyle, J.C. & Harrison, S.P. (2009) Fire in the Earth system. Science, 324, 481-484.
11. Burns, B.R. (1993) Fire-induced dynamics of Araucaria araucana-Nothofagus antarctica forest in the southern Andes. Journal of Biogeography, 20, 669-685.
12. Bytebier, B., Antonelli, A., Bellstedt, D.U. & Linder, H.P. (2011) Estimating the age of fire in the Cape flora of South Africa from an orchid phylogeny. Proceedings of the Royal Society of London B: Biological Sciences, 278, 188-195.
13. Causley, C.L., Fowler, W.M., Lamont, B.B. & He, T. (2016) Fitness of serotiny in fire- and drought-prone environments. Plant Ecology, 217, (in press).
14. Clarke, J.T., Warnock, R.C. & Donoghue, P.C. (2011) Establishing a time-scale for plant evolution. New Phytologist, 192, 266-301.
15. Crisp, M.D. & Cook, L.G. (2011) Cenozoic extinctions account for the low diversity of extant gymnosperms compared with angiosperms. New Phytologist, 192, 997-1009.
16. Crisp, M.D., Burrows, G.E., Cook, L.G., Thornhill, A.H. & Bowman, D.M.J.S. (2011) Flammable biomes dominated by eucalypts originated at the Cretaceous-Palaeogene boundary. Nature Communications, 2, 1-8.
17. Crossley, D.I. (1956) Fruiting habits of lodgepole pine. Canadian Department of Northern Affairs and Natural Resources, Forest Research Division Technical Note 35.
18. Davies, G.M. (2013) Understanding fire regimes and the ecological effects of fire. Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. C.M. Belcher ), pp. 97-124. Wiley-Blackwell, Oxford, UK.
19. Decombeix, A.L. (2013) Bark anatomy of an early Carboniferous tree from Australia. IAWA Journal, 34, 183-196.
20. DiMichele, W.A., Mamay, S.H., Chaney, D.S., Hook, R.W. & Nelson, W.J. (2001) An early Permian flora with late Permian and Mesozoic affinities from North-Central Texas. Journal of Paleontology, 75, 449-460.
21. Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699-710.
22. Edwards, D., Jennifer, L., Morris, J.L., Richardson, J.B. & Kenrick, P. (2014) Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytologist, 202, 50-78.
23. Enright, N.J. (1995) Conifers of tropical Australia. Ecology of the Southern Conifers (eds N.J. Enright & R. S Hill ), pp. 197-222. Melbourne University Press, Melbourne, Australia.
24. Enright, N.J., Mosner, E., Miller, B.P., Johnson, N. & Lamont, B.B. (2007) Soil versus canopy seed storage and plant species coexistence in species-rich shrublands of southwestern Australia. Ecology, 88, 2292-2304.
25. Falcon-Lang, H.J. (2000) Fire ecology in the Carboniferous tropical zone. Palaeogeography Palaeoclimatology and Palaeoecology, 164, 355-371.
26. Falcon-Lang, H.J., Kurzaw, F. & Lucas, S. (2014) Coniferopsid tree-trunks preserved in sabkha facies in the Permian (Sakmarian) community pit formation in south-central New Mexico, U.S.A.: systematics and palaeoecology. Review of Palaeobotany Palynology, 200, 138-160.
27. Farjon, A. (2008) A Natural History of Conifers. Timber Press, Portland, OR, USA.
28. Galtier, J., Scott, A.C., Powell, J.H., Glover, B.W. & Waters, C.N. (1992) Anatomically preserved conifer-like stems from the Upper Carboniferous of England. Proceedings of the Royal Society of London B: Biological Sciences, 247, 211-214.
29. Glasspool, I.J. & Scott, A.S. (2010) Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nature Geosciences, 3, 627-630.
30. Greene, D.F. & Johnson, E.A. (1993) Seed mass and dispersal capacity in wind-dispersed diaspores. Oikos, 67, 69-74.
31. He, T., Lamont, B.B. & Downes, K.S. (2011) Banksia born to burn. New Phytologist, 191, 184-196.
32. He, T., Krauss, S.L., Lamont, B.B., Miller, B.P. & Enright, N.J. (2004) Long distance dispersal in a metapopulation of Banksia hookeriana inferred by population allocation from AFLP data. Molecular Ecology, 13, 1099-1109.
33. He, T., Pausas, J.G., Belcher, C.M., Schwilk, D.W. & Lamont, B.B. (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytologist, 194, 751-759.
34. Hernandez-Castillo, G.R., Rothwell, G.W., Stockey, R.A. & Mapes, G. (2003) Growth architecture of Thucydia mahoningensis, a model for primitive Walchian conifer plants. International Journal of Plant Sciences, 164, 443-452.
35. Hernandez-Castillo, G.R., Rothwell, G.W., Stockey, R.A. & Mapes, G. (2009a) Reconstructing Emporia lockardii (Emporiaceae) Voltziales, and initial thoughts on Paleozoic conifer ecology. International Journal of Plant Sciences, 170, 1056-1074.
36. Hernandez-Castillo, G.R., Rothwell, G.W., Stockey, R.A. & Mapes, G. (2009b) A new voltzialean conifer Emporia royalii sp. nov. (Emporiaceae) from the Hamilton Quarry, Kansas. International Journal of Plant Sciences, 170, 1201-1227.
37. Ho, S.Y.W. & Phillips, M.J. (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Systematic Biology, 58, 367-380.
38. Hopper, S.D. (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil, 322, 49-86.
39. Hughes, L., Dunlop, M., French, K., Leishman, M.R., Rice, B., Rodgerson, L. & Westoby, M. (1994) Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. Journal of Ecology, 82, 933-950.
40. Itzstein-Davey, F. (2004) A spatial and temporal Eocene palaeoenvironmental study, focusing on the Proteaceae family, from Kambalda, Western Australia. Review of Palaeobotany and Palynology, 131, 159-180.
41. Keeley, J.E. (2012) Ecology and evolution of pine life histories. Annals of Forest Science, 69, 445-453.
42. Keeley, J.E. & Zedler, P.H. (1998) Evolution of life histories in Pinus. Ecology and Biogeography of Pinus (ed. D.M. Richardson ), pp. 219-250. Cambridge University Press, Cambridge, UK.
43. Keeley, J.E., Pausas, J.G., Rundel, P.W., Bond, W.J. & Bradstock, R.A. (2011) Fire as an evolutionary pressure shaping plant traits. Trends in Plant Science, 16, 1360-1385.
44. Ladd, P., Midgley, J. & Nield, A. (2013) Serotiny in southern hemisphere conifers. Australian Journal of Botany, 61, 486-496.
45. Lamont, B.B. (1985) Dispersal of the winged fruits of Nuytsia floribunda (Loranthaceae). Australian Journal of Ecology, 10, 187-193.
46. Lamont, B.B. (1991) Canopy seed storage and release: what's in a name? Oikos, 60, 266-268.
47. Lamont, B.B. & Enright, N.J. (2000) Adaptive advantages of aerial seed banks. Plant Species Biology, 15, 157-166.
48. Lamont, B.B. & Downes, K.S. (2011) Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa. Plant Ecology, 212, 2111-2125.
49. Lamont, B.B., Enright, N.J. & He, T. (2011) Fitness and evolution of resprouters in relation to fire. Plant Ecology, 212, 1945-1957.
50. Lamont, B.B. & He, T. (2012) Fire-adapted Gondwanan Angiosperm floras evolved in the Cretaceous. BMC Evolutionay Biology, 12, 1-10.
51. Lamont, B.B., He, T. & Downes, K.S. (2013) Adaptive responses to directional trait selection in the Miocene enabled Cape proteas to colonize the savanna grasslands. Evolutionary Ecology, 27, 1099-1115.
52. Lamont, B.B., Witkowski, E.T.F. & Enright, N.J. (1993) Post-fire litter microsites: safe for seeds, unsafe for seedlings. Ecology, 74, 501-512.
53. Lamont, B.B., Le Maitre, D.C., Cowling, R.M. & Enright, N.J. (1991) Canopy seed storage in woody plants. The Botanical Review, 57, 277-317.
54. Lenton, T.M. (2013) Fire feedbacks on atmospheric oxygen. Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. C.M. Belcher ), pp. 289-308. Wiley-Blackwell, Oxford, UK.
55. Leslie, A.B. (2011) Shifting functional roles and the evolution of conifer pollen-producing and seed-producing cones. Paleobiology, 37, 587-602.
56. Linhart, Y.B. (1978) Maintenance of variation in cone morphology in California closed-cone pines: the roles of fire, squirrels and seed output. The Southwest Naturalist, 23, 29-40.
57. Looy, C.V. (2013) Natural history of a plant trait: branch system abscission in Paleozoic conifers and its environmental, autecological and ecosystem implications in a fire-prone world. Paleobiology, 39, 235-252.
58. Looy, C.V. & Stevenson, R.A. (2014) Earliest occurrence of autorotating seeds in conifers: the Permian (Kungurian-Roadian) Manifera talaris gen et sp nov. International Journal of Plant Sciences, 174, 841-854.
59. Macphail, M. (2007) Australian palaeoclimates: Cretaceous to Tertiary - a review of palaeobotanical and related evidence to the year 2000. Perth, Australia. CRC LEME Open File Report 151.
60. Maddison, W.P. & Maddison, D.R. (2007) Mesquite: a modular system for evolutionary analysis. Version 2.0 available at http://mesquiteproject.org.
61. de Magalhães, R.M.Q. & Schwilk, D.W. (2012) Leaf traits and litter flammability: evidence for non-additive mixture effects in a temperate forest. Journal of Ecology, 100, 1153-1163.
62. Magallon, S., Hilu, K.W. & Quandt, D. (2013) Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany, 100, 556-573.
63. Mapes, G. & Rothwell, G.W. (2003) Validation of the names Emporiaceae, Emporia, and Emporia lockardii. Taxon, 52, 327-328.
64. Merwin, L., He, T., Lamont, B.B., Enright, N.J. & Krauss, S.L. (2012) Low rate of between-population seed dispersal restricts genetic connectivity & metapopulation dynamics in a clonal shrub. PLoS ONE, 7, e50974.
65. Midgley, J.J., Bond, W.J. & Belcher, C.M. (2013) Plant adaptations to fire: an evolutionary perspective. Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. C.M. Belcher ), pp. 125-134. Wiley-Blackwell, Oxford, UK.
66. Morandini, F., Perez-Ramirez, Y., Tihay, V., Santoni, P.A. & Barboni, T. (2013) Radiant, convective and heat release characterization of vegetation fire. International Journal of Thermal Sciences, 70, 83-91.
67. Pagel, M. & Meade, A. (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. The American Naturalist, 167, 808-825.
68. Pausas, J.G. & Keeley, J.E. (2009) A burning story: the role of fire in the history of life. BioScience, 59, 593-601.
69. Perry, G.L.W. & Enright, N.J. (2002) Humans, fire and landscape pattern: understanding a maquis-forest complex, Mont Do, New Caledonia, using a spatial 'state-and-transition' model. Journal of Biogeography, 29, 1143-1158.
70. 2 climate on lightning-caused fires. Journal of Climate, 7, 1484-1494.
71. Quintiere, J.G. (1998) Principles of Fire Behavior. Delmar, Albany, NY, USA.
72. 2 variation, fire, and terrestrial ecology. Palaeogeography, Palaeoclimatology, Palaeoecology, 75, 223-240.
73. Robson, B.E., Collinson, M.E., Riegel, W., Scott, A.C. & Pancost, R.D. (2015) Early Paleogene wildfires in peat-forming environments at Schöningen, Germany. Palaeogeography, Palaeoclimatology, Palaeoecology, 437, 53-62.
74. Rothwell, G.W., Mapes, G. & Hernandez-Castillo, G.R. (2005) Hanskerpia gen. nov. and phylogenetic relationships among the most ancient conifers (Voltziales). Taxon, 54, 733-750.
75. Schemel, C.F., Simeoni, A., Biteau, H., Rivera, J.D. & Torero, J.L. (2008) A calorimetric study of wildland fuels. Experimental Thermal Fluid Science, 32, 1381-1389.
76. Schwilk, D.W. & Ackerly, D.D. (2001) Flammability and serotiny as strategies: correlated evolution in pines. Oikos, 94, 326-336.
77. Scott, A.C. (2000) Pre-Quaternary history of fire. Palaeogeography Palaeoclimatology Palaeoecology, 164, 297-345.
78. Scott, A.C. & Chaloner, W.G. (1983) The earliest fossil conifer from the Westphalian B of Yorkshire. Proceedings of the Royal Society B, 220, 163-182.
79. Scott, A.C. & Glasspool, J.J. (2006) The diversification of Paleozoic fire systems and fluctuations in the atmospheric oxygen concentration. Proceedings of the National Academy of Sciences, 103, 10861-10865.
80. Serbet, R., Escapa, I., Taylor, T.N., Taylor, E.L. & Cúneo, N.R. (2010) Additional observations on the enigmatic Permian plant Buriadia and implications on early coniferophyte evolution. Review of Palaeobotany and Palynology, 161, 168-178.
81. Stockey, R.A. (1984) Middle Eocene pines remains from British Columbia. Botanical Gazette, 145, 265-274.
82. Tewarson, A. (2002) Generation of heat and chemical compounds in fires. SFPE Handbook of Fire Protection Engineering (ed. P.J. DiNenno ), pp. 82-161. National Fire Protection Association Press, Quincy, MA, USA.
83. Tomback, D.F. & Linhart, Y.B. (1990) The evolution of bird-dispersed pines. Evolutionary Ecology, 4, 185-219.
84. Watson, A.J. & Lovelock, J.E. (2013) The dependence of flame spread and probability of ignition on atmospheric oxygen: an experimental investigation. Fire Phenomena and the Earth System: An Interdisciplinary Guide to Fire Science (ed. C.M. Belcher ), pp. 273-287. Wiley-Blackwell, Oxford, UK.
85. Zambito, J.J. & Benison, K.C. (2013) Extreme high temperatures and paleoclimate trends recorded in a Permian ephemeral lake halite. Geology, 41, 587-590.