Skip to main content
SpringerLink
Log in

African geoxyles evolved in response to fire; frost came later

  • Ideas & Perspectives
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

It has been proposed in separate studies that fire or frost were the critical selective agents in the evolution of subshrub geoxyles (SGs) in African subtropical grasslands. We attempt to resolve this controversy by examining the evolution of SGs among the entire genus Protea that is widespread throughout southern/central Africa. We show that SGs are not confined to grasslands but occur in a wide range of non-forest vegetation types, including mediterranean shrublands. SG proteas arose 1–11 million years ago but their multiple origins among other geoxyles, confounded by strong intraspecific variability among grassland species, makes it impossible to identify the ancestral growth form. We conclude that the evolutionary history of SG proteas has occurred under lightning-prone conditions that promoted fire and were essentially frost-free; exposure to frost has been limited to certain elevated locations in more recent times. This is supported by many SGs having pyrogenic flowering and lack of seed storage among grassland species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander LV, Zhang X, Peterson TC, Caesar J, Gleason B, Klein Tank AMG, Tagipour A (2006) Global observed changes in daily climate extremes of temperature and precipitation. J Geophys Res 111:D05109. doi:10.1029/2005JD006290

    Google Scholar 

  • Archibald S, Staver AC, Levin SA (2012) Evolution of human-driven fire regimes in Africa. Proc Natl Acad Sci 109:847–852

    Article  CAS  PubMed  Google Scholar 

  • Bannister P, Lord JM (2006) Comparative winter frost resistance of plant species from southern Africa, Australia, New Zealand, and South America grown in a common environment (Dunedin, New Zealand). NZ J Bot 44:109–119

    Article  Google Scholar 

  • Brown KS, Marean CW, Herries AIR, Jacobs Z, Tribolo C, Braun D, Roberts DL, Meyer MC, Bernatchez J (2009) Fire as an engineering tool of early modern humans. Science 325:859–862

    Article  CAS  PubMed  Google Scholar 

  • Burtt Davy J (1922) The suffrutescent habit as an adaptation to environment. J Ecol 10:211–219

    Article  Google Scholar 

  • Bytebier B, Antonelli A, Bellstedt DU, Linder HP (2011) Estimating the age of fire in the Cape flora of South Africa from an orchid phylogeny. Proc R Soc B 278:188–195

    Article  PubMed  Google Scholar 

  • Causley CL, Fowler WM, Lamont BB, He T (2016) Fitness benefits of serotiny in fire- and drought-prone environments. Plant Ecol 217:773–779

    Article  Google Scholar 

  • Chisumpa SM, Brummitt RK (1987) Taxonomic notes on tropical African species of Protea. Kew Bull 42:815–853

    Article  Google Scholar 

  • Clarke PJ, Lawes MJ, Midgley JJ, Lamont BB, Ojeda F, Burrows GE, Enright NJ, Knox KJE (2013) Resprouting as a key functional trait: how buds, protection and reserves drive persistence after fire. New Phytol 197:19–35

    Article  CAS  PubMed  Google Scholar 

  • Davies TJ, Daru BH, Bank M, Maurin O, Bond WJ (2016) Multiple routes underground? Frost alone cannot explain the evolution of underground trees. New Phytol 209:910–912

    Article  PubMed  Google Scholar 

  • Dayrell RL, Garcia QS, Negreiros D, Baskin CC, Baskin JM, Silveira FA (2017) Phylogeny strongly drives seed dormancy and quality in a climatically buffered hotspot for plant endemism. Ann Bot 119:267–277

    Article  PubMed  Google Scholar 

  • Du Rietz GE (1931) Life-forms of terrestrial flowering plants. Acta Phytogeogr Suec 3:1–95

    Google Scholar 

  • Edwards EJ, Osborne CP, Strömberg C, Smith SA, C4 Grasses Consortium (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591

    Article  CAS  PubMed  Google Scholar 

  • Enright NJ, Mosner E, Miller BP, Johnson N, Lamont BB (2007) Soil versus canopy seed storage and plant species coexistence in species-rich shrublands of southwestern Australia. Ecology 88:2292–2304

    Article  CAS  PubMed  Google Scholar 

  • Finckh M, Revermann R, Aidar MP (2016) Climate refugees going underground–a response to Maurin et al. (2014). New Phytol 209:904–909

    Article  PubMed  Google Scholar 

  • Frost PGH (2012) The responses and survival of organisms in fire-prone environments. In: Booysen PDV, Tainton NM (eds) Ecological effects of fire in South African ecosystems, vol 48. Springer, Berlin

    Google Scholar 

  • Gignoux J, Lahoreau G, Julliard R, Barot S (2009) Establishment and early persistence of tree seedlings in an annually burned savanna. J Ecol 97:484–495

    Article  Google Scholar 

  • He T, Lamont BB, Downes KS (2011) Banksia born to burn. New Phytol 191:184–196

    Article  PubMed  Google Scholar 

  • He T, Lamont BB, Manning J (2016) A Cretaceous origin for fire adaptations in the Cape flora. Sci Rep 6:34880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoetzel S, Dupont L, Schefuss E, Rommerskirchen F, Wefer G (2013) The role of fire in Miocene to Pliocene C4 grassland and ecosystem evolution. Nat Geosci 6:1027–1030

    Article  CAS  Google Scholar 

  • Hoffmann WA, Solbrig OT (2003) The role of topkill in the differential response of savanna woody species to fire. For Ecol Manag 180:273–286

    Article  Google Scholar 

  • Holdo RM (2005) Stem mortality following fire in Kalahari sand vegetation: effects of frost, prior damage, and tree neighbourhoods. Plant Ecol 180:77–86

    Article  Google Scholar 

  • Hyde MA, Wursten BT, Ballings P, Coates Palgrave M (2016) Flora of Zimbabwe: records of Protea welwitschii. http://www.zimbabweflora.co.zw/speciesdata/species-display.php?speciesid=120800. Retrieved 6 Oct 2016

  • Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2012) Fire in Mediterranean ecosystems: ecology, evolution and management. Cambridge University Press, Cambridge

    Google Scholar 

  • Kennedy AD, Potgieter ALF (2003) Fire season affects size and architecture of Colophospermum mopane in southern African savannas. Plant Ecol 167:179–192

    Article  Google Scholar 

  • Lamont BB, Downes KS (2011) Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa. Plant Ecol 212:2111–2125

    Article  Google Scholar 

  • Lamont BB, Enright NJ (2000) Adaptive advantages of aerial seed banks. Plant Species Biol 15:157–166

    Article  Google Scholar 

  • Lamont BB, He T (2012) Fire-adapted Gondwanan Angiosperm floras arose in the Cretaceous. BMC Evol Biol 12:223

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamont BB, Keith D (2017) Heathlands and associated shrublands. In: Keith D (ed) Vegetation of Australia, 3rd edn. Cambridge University Press, Cambridge, pp 339–368

    Google Scholar 

  • Lamont BB, He T, Downes KS (2013) Adaptive responses to directional trait selection in the Miocene enabled Cape proteas to colonize the savanna grasslands. Evol Ecol 27:1099–1115

    Article  Google Scholar 

  • Lindman CAM (1900) Vegetationen i Rio Grande do Sul (Sydobrasilien). Nordin and Josephson, Stockholm

    Google Scholar 

  • Manry DE, Knight RS (1986) Lightning density and burning frequency in South African vegetation. Vegetatio 66:67–76

    Google Scholar 

  • Maurin O, Davies TJ, Burrows JE, Daru BH, Yessoufou K, Muasya AM, van der Bank M, Bond WJ (2014) Savanna fire and the origins of the ‘underground forests’ of Africa. New Phytol 204:201–214

    Article  PubMed  Google Scholar 

  • Medwecka Kornas A (1980) Gardenia subacaulis a pyrophytic suffrutex of the African savanna. Acta Botanica Acad Sci Hung 26:131–138

    Google Scholar 

  • Mucina L, Rutherford MC (2006) The vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute, Pretoria

    Google Scholar 

  • Muir RA, Bordy EM, Prevec R (2015) Lower Cretaceous deposit reveals first evidence of a post-wildfire debris flow in the Kirkwood Formation, Algoa Basin, Eastern Cape, South Africa. Cretac Res 56:161–179

    Article  Google Scholar 

  • Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump markov chain monte carlo. Am Nat 167:808–825

    PubMed  Google Scholar 

  • Platt WJ, Evans GW, Davis MM (1988) Effects of fire season on flowering of forbs and shrubs in longleaf pine forests. Oecologia 76:353–363

    Article  PubMed  Google Scholar 

  • Prunier R, Holsinger KE, Carlson JE (2012) The effect of historical legacy on adaptation: do closely related species respond to the environment in the same way? J Evol Biol 25:1636–1649

    Article  CAS  PubMed  Google Scholar 

  • Rebelo AG (2001) A field guide to the Proteas of Southern Africa. Fernwood Press, Nova Scotia

    Google Scholar 

  • Rebelo AG. 2009. Protea Atlas Project. South African National Biodiversity Institute, Kirstenbosch, South Africa. http://www.proteaatlas.org.za. Retrieved 26 Aug 2009

  • Ristic Z, Ashworth EN. 1997. Mechanisms of freezing resistance of wood tissues: recent advancements. In Basra AS, Basra RK. (Eds) Mechanisms of environmental stress resistance in plants. Amsterdam, the Netherlands. pp. 123–136

  • Rizzini C, Heringer E (1961) Underground organs of plants from southern Brazilian savannas, with special reference to the xylopodium. Phyton 17:105–124

    Google Scholar 

  • Roberts DL, Neumann FH, Cawthra HC, Carr AS, Scott L, Durugbo EU, Humphries MS, Cowling RM, Bamford MK, Musekiwa C, MacHutchon M (2017) Palaeoenvironments during a terminal Oligocene or early Miocene transgression in a fluvial system at the southwestern tip of Africa. Glob Planet Change 150:1–23

    Article  Google Scholar 

  • Roques KG, O’Connor TG, Watkinson AR (2001) Dynamics of shrub encroachment in an African savanna: relative influences of fire, herbivory, rainfall and density dependence. J Appl Ecol 38:268–280

    Article  Google Scholar 

  • Rundel PW, Arroyo MTK, Cowling RM, Keeley JE, Lamont BB, Vargas P (2016) Mediterranean biomes: evolution of their vegetation, floras and climate. Ann Rev Ecol Evol Syst 47:383–407

    Article  Google Scholar 

  • Scheiter S, Higgins SI, Osborne CP, Bradshaw C, Lunt D, Ripley BS et al (2012) Fire and fire-adapted vegetation promoted C4 expansion in the Late Miocene. New Phytol 195:653–666

    Article  PubMed  Google Scholar 

  • Sciscio L, Tsikos H, Roberts DL, Scott L, van Breugel Y, Damste JS, Schouten DR, Grocke DR (2016) Miocene climate and vegetation changes in the Cape Peninsula, South Africa: evidence from biogeochemistry and palynology. Palaeogeogr Palaeoclimatol Palaeoecol 445:124–137

    Article  Google Scholar 

  • Simon MF, Grether R, de Queiroz LP, Skema C, Pennington RT, Hughes CE (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proc Natl Acad Sci 106:20359–20364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith FR, Granger JE (2017) Survival and life expectancy of the tree Protea roupelliae subsp. roupelliae in a montane grassland savanna: effects of fire regime and plant structure. Aust Ecol. doi:10.1111/aec.12459

    Google Scholar 

  • Utescher T, Mosbrugger V, Ivanov D, Dilcher DL (2009) Present-day climatic equivalents of European Cenozoic climates. Earth Planet Sci Lett 284:544–552

    Article  CAS  Google Scholar 

  • Valente LM, Reeves G, Schnitzler J, Mason IP, Fay MF, Rebelo TG, Chase MW, Barraclough TG (2010) Diversification of the African genus Protea (Proteaceae) in the Cape biodiversity hotspot and beyond: equal rates in different biomes. Evolution 64:745–760

    Article  CAS  PubMed  Google Scholar 

  • Vrba ES (1985) Early hominids in southern Africa: updated observations on chronological and ecological background. In: Tobias PV (ed) Hominid Evolution. Alan R Liss, New York, pp 195–200

    Google Scholar 

  • Wakeling JL, Cramer MD, Bond WJ (2012) The savannah-grassland ‘treeline’: why don’t savanna trees occur in upland grasslands? J Ecol 100:381–391

    Article  Google Scholar 

  • Weiersbye IM, Witkowski ETF (2002). Seed fate and practical germination methods for 46 perennial species that colonize gold mine tailings and acid mine drainage-polluted soils in the grassland biome. In: Seydack AHW Vorster T, Vermeulen WJ, van der Merwe IJ (Eds). Multiple use management of natural forests and woodlands: policy refinements and scientific progress. Proceedings of the Natural Forests and Savanna Woodlands Symposium III, KNP, Department of Water Affairs and Forestry Indigenous Forest Management, Pretoria. pp. 221–255

  • White F (1977) The underground forests of Africa: a preliminary review. Gard Bull 29:57–71 (Singapore)

    Google Scholar 

  • Witkowski ETF, Lamont BB (1997) Does the rare Banksia goodii have different vegetative, reproductive or ecological attributes from its widespread co-occurring relative B. gardneri? J Biogeogr 24:469–482

    Article  Google Scholar 

  • Zachos JC, Dickens GR, Zeebe RE (2008) An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451:279–283

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Richard Cowling, Tony Rebelo, David Ackerly and three other reviewers for comments on the manuscript. This work was supported by the Australian Research Council (DP120103389 and DP130013029).

Author information

Authors and Affiliations

  1. Department of Environment and Agriculture, Curtin University, PO Box U1987, Perth, WA, 6845, Australia

    Byron B. Lamont & Tianhua He

  2. CIDE-CSIC, Ctra. Naquera km 4.5, 46113, Montcada, Valencia, Spain

    Juli G. Pausas

Authors
  1. Byron B. Lamont
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tianhua He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juli G. Pausas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tianhua He.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 481 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lamont, B.B., He, T. & Pausas, J.G. African geoxyles evolved in response to fire; frost came later. Evol Ecol 31, 603–617 (2017). https://doi.org/10.1007/s10682-017-9905-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-017-9905-4

Keywords

Search

Navigation