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The Evolution of Physiological Adaptations in a Flammable Planet

  • Víctor Resco de Dios
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Part of the Managing Forest Ecosystems book series (MAFE, volume 36)

Abstract

Fire has been present on Earth since vascular plant expansion over land at the turn of the Devonian, 420 mya. It is thus to be expected that wildfires have shaped physiological plant traits. The question is which traits have evolved under fire activity and to which extent. Here we present the general hypothesis that plants have evolved bet hedging strategies, whenever possible, to jointly deal with the multiple stresses and disturbances they face during their evolutionary lifetimes. We also note that, in some instances, trade-offs in the adaptations to stress and disturbance have also developed. The traits that are most likely to have evolved in response to fire are related to post-fire recruitment and persistence. We argue that the evolution of these traits has also been shaped by drought and other environmental factors. We also discuss the evidence on whether plant traits that enhance flammability could have evolved in response to fire, but we find more plausible the explanation that plant traits affecting fire behavior emerge from plant responses to other environmental factors.

References

  1. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8(2):135–141.  https://doi.org/10.1016/j.pbi.2005.01.001CrossRefPubMedGoogle Scholar
  2. Anderson HE (1970) Forest fuel ignitibility. Fire Technol 6:312–319.  https://doi.org/10.1007/BF02588932CrossRefGoogle Scholar
  3. Axelrod DI (1980) History of the maritime closed-cone pines, Alta and Baja California. Univ Calif Publ Geol Sci 120:1–143Google Scholar
  4. Bond WJ, Midgley JJ (1995) Kill thy neighbour: an individualistic argument for the evolution of flammability. Oikos 73:79–85CrossRefGoogle Scholar
  5. Bond WJ, Midgley JJ (2003) The evolutionary ecology of sprouting in woody plants. Int J Plant Sci 164:S103–S114CrossRefGoogle Scholar
  6. Bond WJ, Midgley JJ (2012) Fire and the angiosperm revolutions. Int J Plant Sci 173:569–583.  https://doi.org/10.1086/665819CrossRefGoogle Scholar
  7. Bowman DMJS, French BJ, Prior LD (2014) Have plants evolved to self-immolate? Front Plant Sci 5:590.  https://doi.org/10.3389/fpls.2014.00590CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bradshaw SD, Dixon KW, Hopper SD, Lambers H, Turner SR (2011) Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci 16(2):69–76CrossRefGoogle Scholar
  9. Chamorro D, Luna B, Ourcival JM, Kavgaci A, Sirca C, Mouillot F, Arianoutsou M, Moreno JM (2017) Germination sensitivity to water stress in four shrubby species across the Mediterranean Basin. Plant Biol 19:23–31.  https://doi.org/10.1111/plb.12450CrossRefPubMedGoogle Scholar
  10. Chamorro D, Moreno JM (2019) Effects of water stress and smoke on germination of Mediterranean shrubs with hard or soft coat seeds. Plant Ecol 220(4–5):511–521.  https://doi.org/10.1007/s11258-019-00931-2CrossRefGoogle Scholar
  11. Chamorro D, Parra A, Moreno JM (2016) Reproductive output, seed anatomy and germination under water stress in the seeder Cistus ladanifer subjected to experimental drought. Environ Exp Bot 123:59–67.  https://doi.org/10.1016/j.envexpbot.2015.11.002CrossRefGoogle Scholar
  12. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491(7426):752–755.  https://doi.org/10.1038/nature11688CrossRefPubMedGoogle Scholar
  13. Crisp MD, Burrows GE, Cook LG, Thornhill AH, Bowman DM (2011) Flammable biomes dominated by eucalypts originated at the Cretaceous-Palaeogene boundary. Nat Commun 2:193.  https://doi.org/10.1038/ncomms1191CrossRefPubMedGoogle Scholar
  14. Cruz A, Moreno JM (2001) Lignotuber size of Erica australis and its relationship with soil resources. J Veg Sci 12:373–384CrossRefGoogle Scholar
  15. de Luis M, Verdu M, Raventós J (2008) Early to rise makes a plant healthy, wealthy, and wise. Ecology 89:3061–3071CrossRefGoogle Scholar
  16. Decombeix A-L (2013) Bark anatomy of an early Carboniferous tree from Australia. IAWA J 34(2):183–196.  https://doi.org/10.1163/22941932-00000016CrossRefGoogle Scholar
  17. Fernandes PM, Vega JA, Jiménez E, Rigolot E (2008) Fire resistance of European pines. For Ecol Manag 256(3):246–255.  https://doi.org/10.1016/j.foreco.2008.04.032CrossRefGoogle Scholar
  18. Gagnon PR, Passmore HA, Platt WJ, Myers JA, Paine CET, Harms KE (2010) Does pyrogenicity protect burning plants? Ecology 91(12):3481–3486.  https://doi.org/10.1890/10-0291.1CrossRefPubMedGoogle Scholar
  19. Gallien L, Saladin B, Boucher FC, Richardson DM, Zimmermann NE (2016) Does the legacy of historical biogeography shape current invasiveness in pines? New Phytol 209(3):1096–1105.  https://doi.org/10.1111/nph.13700CrossRefPubMedGoogle Scholar
  20. Glasspool IJ, Scott AC (2010) Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat Geosci 3:627–630.  https://doi.org/10.1038/ngeo923CrossRefGoogle Scholar
  21. Gómez-González S, Torres-Díaz C, Bustos-Schindler C, Gianoli E (2011) Anthropogenic fire drives the evolution of seed traits. Proc Natl Acad Sci 108(46):18743–18747.  https://doi.org/10.1073/pnas.1108863108CrossRefPubMedGoogle Scholar
  22. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  23. Grubb PJ (1992) A positive distrust in simplicity – lessons from plant defences from competition among plants and among animal. J Ecol 80:585–610CrossRefGoogle Scholar
  24. He T, Belcher CM, Lamont BB, Lim SL, McGlone M (2016) A 350-million-year legacy of fire adaptation among conifers. J Ecol 104(2):352–363.  https://doi.org/10.1111/1365-2745.12513CrossRefGoogle Scholar
  25. He T, Lamont BB (2018a) Baptism by fire: the pivotal role of ancient conflagrations in evolution of the Earth’s flora. Natl Sci Rev 5(2):237–254.  https://doi.org/10.1093/nsr/nwx041CrossRefGoogle Scholar
  26. He T, Lamont BB (2018b) Fire as a potent mutagenic agent among plants. Crit Rev Plant Sci 37(1):1–14.  https://doi.org/10.1080/07352689.2018.1453981CrossRefGoogle Scholar
  27. He T, Lamont BB, Downes KS (2011) Banksia born to burn. New Phytol 191(1):184–196.  https://doi.org/10.1111/j.1469-8137.2011.03663.xCrossRefPubMedGoogle Scholar
  28. He T, Lamont BB, Pausas JG (2019) Fire as a key driver of Earth’s biodiversity. Biol Rev Camb Philos Soc 94:1983–2010.  https://doi.org/10.1111/brv.12544CrossRefPubMedGoogle Scholar
  29. He T, Pausas JG, Belcher CM, Schwilk DW, Lamont BB (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol 194(3):751–759.  https://doi.org/10.1111/j.1469-8137.2012.04079.xCrossRefPubMedGoogle Scholar
  30. Hernández-Serrano A, Verdú M, Santos-Del-Blanco L, Climent J, González-Martínez SC, Pausas JG (2014) Heritability and quantitative genetic divergence of serotiny, a fire-persistence plant trait. Ann Bot 114(3):571–577.  https://doi.org/10.1093/aob/mcu142CrossRefPubMedPubMedCentralGoogle Scholar
  31. Herrera CM, Jordano P, Guitián J, Traveset A (1998) Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. Am Nat 152:576–594CrossRefGoogle Scholar
  32. Karavani A, Boer MM, Baudena M, Colinas C, Díaz-Sierra R, Pemán J, de Luís M, Enríquez-de-Salamanca Á, Resco de Dios V (2018) Fire-induced deforestation in drought-prone Mediterranean forests: drivers and unknowns from leaves to communities. Ecol Monogr 88:141–169CrossRefGoogle Scholar
  33. Keeley JE (2012) Ecology and evolution of pine life histories. Ann For Sci 69:445–453.  https://doi.org/10.1007/s13595-012-0201-8CrossRefGoogle Scholar
  34. Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2012) Fire in Mediterranean ecosystems- ecology, evolution and management. Cambridge University Press, CambridgeGoogle Scholar
  35. Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447CrossRefGoogle Scholar
  36. Korner C (2003) Carbon limitation in trees. J Ecol 91(1):4–17CrossRefGoogle Scholar
  37. Lamont BB, He T (2017) Fire-proneness as a prerequisite for the evolution of fire-adapted traits. Trends Plant Sci 22(4):278–288.  https://doi.org/10.1016/j.tplants.2016.11.004CrossRefPubMedGoogle Scholar
  38. Lamont BB, He T, Yan Z (2019) Evolutionary history of fire-stimulated resprouting, flowering, seed release and germination. Biol Rev Camb Philos Soc 94(3):903–928.  https://doi.org/10.1111/brv.12483CrossRefPubMedGoogle Scholar
  39. Luna B, Moreno JM, Cruz A, Fernández-González F (2007) Heat-shock and seed germination of a group of Mediterranean plant species growing in a burned area: an approach based on plant functional types. Environ Exp Bot 60(3):324–333.  https://doi.org/10.1016/j.envexpbot.2006.12.014CrossRefGoogle Scholar
  40. Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, van Bodegom PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A, Reich PB, Santiago LS (2015) Global effects of soil and climate on leaf photosynthetic traits and rates. Glob Ecol Biogeogr 24(6):706–717.  https://doi.org/10.1111/geb.12296CrossRefGoogle Scholar
  41. Martin RR, Gordon DA, Gutierrez ME, Lee DS, Molina DM, Schoreder RA, Sapsis DB, Stephens SL, Chambers M (1994) Assessing the flammability of domestic and wildland vegetation. In: Proceedings of the 12th conference on fire and forest meteorology, SAF Publications, 94-02. SAF, Bethesda, MD, USA, pp 130–137Google Scholar
  42. Martin-Sanz RC, San-Martin R, Poorter H, Vazquez A, Climent J (2019) How does water availability affect the allocation to bark in a Mediterranean conifer? Front Plant Sci 10:607.  https://doi.org/10.3389/fpls.2019.00607CrossRefPubMedPubMedCentralGoogle Scholar
  43. Mays C, Cantrill DJ, Bevitt JJ (2017) Polar wildfires and conifer serotiny during the Cretaceous global hothouse. Geology 45(12):1119–1122.  https://doi.org/10.1130/g39453.1CrossRefGoogle Scholar
  44. Midgley JJ (1996) Why the world’s vegetation is not totally dominated by resprouting plants; because resprouters are shorter than reseeders. Ecography 19:92–95CrossRefGoogle Scholar
  45. Midgley JJ (2013) Flammability is not selected for, it emerges. Aust J Bot 61(2):102–106.  https://doi.org/10.1071/BT12289CrossRefGoogle Scholar
  46. Mutch RW (1970) Wildland fires and ecosystems–a hypothesis. Ecology 51:1046–1051CrossRefGoogle Scholar
  47. Ne’eman G, Lev-Yadun S, Arianoutsou M (2012) Fire-related traits in Mediterranean basin plants. Isr J Ecol Evol 58.  https://doi.org/10.1560/ijee.58.2-3.177
  48. Niinemets Ü, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs. Ecol Monogr 76:521–547.  https://doi.org/10.1890/0012-9615(2006)076[0521:TTSDAW]2.0.CO;2
  49. Niklas KJ (2016) Plant evolution – an introduction to the history of life. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  50. Ojeda F (1998) Biogeography of seeder and resprouter Erica species in the Cape Floristic Region—where are the resprouters? Biol J Lin Soc 63:331–347Google Scholar
  51. Parra A, Moreno JM (2017) Post-fire environments are favourable for plant functioning of seeder and resprouter Mediterranean shrubs, even under drought. New Phytol.  https://doi.org/10.1111/nph.14454
  52. Pausas JG, Keeley JE (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytol 204(1):55–65.  https://doi.org/10.1111/nph.12921CrossRefPubMedGoogle Scholar
  53. Pausas JG, Keeley JE, Schwilk DW (2017) Flammability as an ecological and evolutionary driver. J Ecol 105:289–297.  https://doi.org/10.1111/1365-2745.12691CrossRefGoogle Scholar
  54. Pecrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M (2011) Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J Exp Bot 62(10):3587–3597.  https://doi.org/10.1093/jxb/err052CrossRefPubMedGoogle Scholar
  55. Pierce S, Negreiros D, Cerabolini BEL, Kattge J, Díaz S, Kleyer M, Shipley B, Wright SJ, Soudzilovskaia NA, Onipchenko VG, van Bodegom PM, Frenette-Dussault C, Weiher E, Pinho BX, Cornelissen JHC, Grime JP, Thompson K, Hunt R, Wilson PJ, Buffa G, Nyakunga OC, Reich PB, Caccianiga M, Mangili F, Ceriani RM, Luzzaro A, Brusa G, Siefert A, Barbosa NPU, Chapin FS, Cornwell WK, Fang J, Fernandes GW, Garnier E, Le Stradic S, Peñuelas J, Melo FPL, Slaviero A, Tabarelli M, Tampucci D (2017) A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct Ecol 31(2):444–457.  https://doi.org/10.1111/1365-2435.12722CrossRefGoogle Scholar
  56. Resco de Dios V, Arteaga C, Hedo J, Gil-Pelegrín E, Voltas J (2018) A trade-off between embolism resistance and bark thickness in conifers: are drought and fire adaptations antagonistic? Plant Ecol Divers 11(3):253–258.  https://doi.org/10.1080/17550874.2018.1504238CrossRefGoogle Scholar
  57. Rosell JA (2016) Bark thickness across the angiosperms: more than just fire. New Phytol 211(1):90–102.  https://doi.org/10.1111/nph.13889CrossRefPubMedGoogle Scholar
  58. Rosell JA (2019) Bark in woody plants: understanding the diversity of a multifunctional structure. Integr Comp Biol 59(3):535–547.  https://doi.org/10.1093/icb/icz057CrossRefPubMedGoogle Scholar
  59. Tavşanoğlu Ç, Pausas JG (2018) A functional trait database for Mediterranean Basin plants. Scient Data 5:180135.  https://doi.org/10.1038/sdata.2018.135CrossRefGoogle Scholar
  60. Thomas PB, Morris EC, Auld TD, Haigh AM (2010) The interaction of temperature, water availability and fire cues regulates seed germination in a fire-prone landscape. Oecologia 162(2):293–302.  https://doi.org/10.1007/s00442-009-1456-0CrossRefPubMedGoogle Scholar
  61. Torres I, Parra A, Moreno JM, Durka W (2018) No genetic adaptation of the Mediterranean keystone shrub Cistus ladanifer in response to experimental fire and extreme drought. PLoS One 13(6):e0199119.  https://doi.org/10.1371/journal.pone.0199119CrossRefPubMedPubMedCentralGoogle Scholar
  62. Vanneste K, Baele G, Maere S, Van de Peer Y (2014) Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res 24(8):1334–1347.  https://doi.org/10.1101/gr.168997.113CrossRefPubMedPubMedCentralGoogle Scholar
  63. Vilagrosa A, Hernandez EI, Luis VC, Cochard H, Pausas JG (2014) Physiological differences explain the co-existence of different regeneration strategies in Mediterranean ecosystems. New Phytol 201(4):1277–1288.  https://doi.org/10.1111/nph.12584CrossRefPubMedGoogle Scholar
  64. Wells PV (1969) The relation between mode of reproduction and extent of speciation in woody genera of the California chaparral. Evolution 23:264–267CrossRefGoogle Scholar
  65. Wicklow DT (1977) Germination response in Emmenanthe penduliflora (Hydrophyllaceae). Ecology 57:201–205CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Víctor Resco de Dios
    • 1
    • 2
  1. 1.School of Life Science and EngineeringSouthwest University of Science and TechnologyMianyangChina
  2. 2.Crop and Forest Sciences and JRU CTFC-AGROTECNIOUniversitat de LleidaLleidaSpain

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