Savanna fire and the origins of the 'underground forests' of Africa

New Phytologist

Volumn 204, Issue 1, 2014, Pages 201-214

  Maurin, Olivier ^a   Davies, T Jonathan ^a,b   Burrows, John E ^c,d   Daru, Barnabas H ^a   Yessoufou, Kowiyou ^a,e   Muasya, A Muthama ^f   van der Bank, Michelle ^a   Bond, William J ^f,g  

^a UNIVERSITY OF JOHANNESBURG   (South Africa)

^b MCGILL UNIVERSITY   (Canada)

^c Buffelskloof Herbarium   (South Africa)

^d UNIVERSITY OF PRETORIA   (South Africa)

^e UNIVERSITY OF SOUTH AFRICA   (South Africa)

^f UNIVERSITY OF CAPE TOWN   (South Africa)

^g SOUTH AFRICAN ENVIRONMENTAL OBSERVATION NETWORK   (South Africa)

Author keywords

Fire adaptation; Geoxylic suffrutex; Phylogeny; Pliocene; Savanna; Trees of southern africa; Underground forests

Indexed keywords

CERRADO; DIVERGENCE; FIRE BEHAVIOR; PHYLOGENETICS; PHYLOGENY; PHYLOGEOGRAPHY; PLIOCENE; SAVANNA;

AFRICA;

ADAPTATION; AFRICA; BIODIVERSITY; BRAZIL; ECOSYSTEM; EVOLUTION; FIRE; FOREST; GRASSLAND; PHYLOGENY;

ADAPTATION, BIOLOGICAL; AFRICA; BIODIVERSITY; BIOLOGICAL EVOLUTION; BRAZIL; ECOSYSTEM; FIRES; FORESTS; GRASSLAND; PHYLOGENY;

EID: 84906519040     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12936     Document Type: Article

References (110)

1. Angiosperm Phylogeny Group. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105-121.
2. Appezzato-da-Glória B, Cury G, Kasue Misaki Soares M, Rocha R, Hissae Hayashi A. 2008. Underground systems of Asteraceae species from the Brazilian Cerrado 1. The Journal of the Torrey Botanical Society 135: 103-113.
3. Arakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences, USA 108: 8379-8384.
4. Archibald S, Lehmann CE, Gómez-Dans JL, Bradstock RA. 2013. Defining pyromes and global syndromes of fire regimes. Proceedings of the National Academy of Sciences, USA 110: 6442-6447.
5. Archibald S, Scholes RJ, Roy DP, Roberts G, Boschetti L. 2010. Southern African fire regimes as revealed by remote sensing. International Journal of Wildland Fire 19: 861-878.
6. Barraclough TG, Nee S, Harvey PH. 1998. Sister-group analysis in identifying correlates of diversification - comment. Evolutionary Ecology 12: 751-754.
7. Beerling DJ, Osborne CP. 2006. The origin of the savanna biome. Global Change Biology 12: 2023-2031.
8. 2 history by proxy. Nature Geoscience 4: 418-420.
9. Bell CD, Soltis DE, Soltis PS. 2010. The age and diversification of the angiosperms re-revisited. American Journal of Botany 97: 1296-1303.
10. Bininda-Emonds O. 2005. TransAlign: using amino acids to facilitate the multiple alignment of protein-coding DNA sequences. BMC Bioinformatics 6: 156.
11. 4 grasslands and savannas? Annual Review of Ecology, Evolution and Systematics 39: 641-659.
12. Bond WJ, Cook G, Williams RJ. 2012. Which trees dominate in savannas? The escape hypothesis and eucalypts in northern Australia. Austral Ecology 37: 678-685.
13. 2-controlled mechanism of woody plant invasion in grasslands and savannas. Global Change Biology 6: 865-870.
14. 2 and the uneasy interactions of trees and savanna grasses. Philosophical Transactions of the Royal Society of London Series B 367: 601-612.
15. Bond WJ, Midgley GF, Woodward FI. 2003. What controls South African vegetation - climate or fire? South African Journal of Botany 69: 79-91.
16. Bond WJ, Woodward FI, Midgley GF. 2005. The global distribution of ecosystems in a world without fire. New Phytologist 165: 525-538.
17. Boon D. 2010. Pooley's trees of Eastern South Africa - a complete guide. Durban, South Africa: Flora and Fauna Publication Trust.
18. Bouchenak-Khelladi Y, Muasya AM, Linder HP. 2014. A revised evolutionary history of Poales: origins and diversification. Botanical Journal of the Linnean Society 175: 4-16.
19. Britton T, Anderson CL, Jacquet D, Lundqvist S, Bremer K. 2007. Estimating divergence times in large phylogenetic trees. Systematic Biology 56: 741-752.
20. Bryant JB, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL. 2008. Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proceedings of the National Academy of Sciences, USA 105: 11505-11511.
21. Burtt Davy J. 1922. The suffrutescent habit as an adaptation to environment. Journal of Ecology 10: 211-219.
22. 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. Proceedings of the Royal Society Series B 278: 188-195.
23. Cantino PD, Doyle JA, Graham SW, Judd WS, Olmstead RG, Soltis DE, Soltis PS, Donoghue MJ. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56: 822-846.
24. CBOL Plant Working Group. 2009. A DNA barcode for land plants. Proceedings of the National Academy of Sciences, USA 106: 12794-12797.
25. Cerling TE, Harris JM, McFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR. 1997. Global vegetation change through the Miocene/Pliocene boundary. Nature 389: 153-158.
26. 4 photosynthesis in grasses. Current Biology 18: 37-43.
27. Christin PA, Spriggs E, Osborne CP, Strömberg CAE, Salamin N, Edwards EJ. 2014. Molecular dating, evolutionary rates, and the age of the grasses. Systematic Biology 63: 153-165.
28. Chuvieco E, Giglio L, Justice C. 2008. Global characterization of fire activity: toward defining fire regimes from Earth observation data. Global Change Biology 14: 1488-1502.
29. rd edn. Cape Town, South Africa: Struik.
30. Cole M. 1986. Savannas: biogeography and geobotany. London, UK: Academic Press.
31. nd edn. London, UK: Unwin Hyman Ltd.
32. Coutinho LM. 1982. Ecological effects of fire in Brazilian cerrado. In: Huntley BJ, Walker BH, eds. Ecology of tropical savannas. Berlin, Germany: Springer, 273-291.
33. Coutinho LM. 1990. Fire in the ecology of the Brazilian cerrado. In: Goldamer JG, ed. Fire in the tropical biota - ecosystem process and global challenges. Berlin, Germany: Springer, 82-105.
34. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
35. 4 grasslands: integrating evolutionary and ecosystem science. Science 328: 587-591.
36. 4 grasses. Oecologia 31: 255-267.
37. 2, and climate. Oecologia 112: 285-299.
38. Felsenstein J. 1985. Phylogenies and the comparative method. The American Naturalist 125: 1-15.
39. Frost P. 1996. The ecology of miombo woodlands. In: Campbell B, ed. The miombo in transition: woodlands and welfare in Africa. Bogor, Indonesia: Centre for International Forestry Research, 11-55.
40. Germishuizen G, Meyer NL. 2013. Plants of southern Africa: an annotated checklist. Strelitzia, vol. 14. Pretoria, South Africa: National Botanical Institute.
41. Hajibabaei M, De Waard JR, Ivanova NV, Ratnasingham S, Dooh RT, Kirk SL, Mackie PM, Hebert PDN. 2005. Critical factors for assembling a high volume of DNA barcodes. Philosophical Transactions of the Royal Society London Series B 360: 1959-1967.
42. He T, Lamont BB, Downes KS. 2011. Banksia born to burn. New Phytologist 191: 184-196.
43. 2: natural variations Archaean to present. Washington DC, USA: American Geophysical Union, 32, 419-422.
44. Higgins SI, Bond WJ, February EC, Bronn A, Euston-Brown DIW, Enslin B, Govender N, Rademan L, O'Regan S, Potgieter ALF et al. 2007. Effects of four decades of fire manipulation on woody vegetation structure in savanna. Ecology 88: 1119-1125.
45. Higgins SI, Bond WJ, Trollope WSW. 2000. Fire, resprouting and variability: a recipe for tree-grass coexistence in savanna. Journal of Ecology 88: 213-229.
46. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
47. Hirota M, Holmgren M, Van Nes EH, Scheffer M. 2011. Global resilience of tropical forest and savanna to critical transitions. Science 334: 232-235.
48. 4 grassland and ecosystem evolution. Nature Geoscience 6: 1027-1030.
49. Hoffmann WA, Adasme R, Haridasan M, Carvalho M, Geiger EL, Pereira MAB, Gotsch SG, Franco AC. 2009. Tree topkill, not mortality, governs the dynamics of alternate stable states at savanna forest boundaries under frequent fire in central Brazil. Ecology 90: 1326-1337.
50. Hoffmann WA, Geiger EL, Gotsch SG, Rossatto DR, Silva LCR, Lau OL, Haridasan M, Franco AC. 2012. Ecological thresholds at the savanna-forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes. Ecology Letters 15: 759-768.
51. Hoffmann WA, Orthen B, Franco AC. 2004. Constraints to seedling success of savanna and forest trees across the savanna-forest boundary. Oecologia 140: 252-260.
52. Hoffmann WA, Orthen B, Nascimento PKV. 2003. Comparative fire ecology of tropical savanna and forest trees. Functional Ecology 17: 720-726.
53. Ivanova NV, Fazekas AJ, Hebert PDN. 2008. Semi-automated membrane based protocol for DNA isolation from plants. Plant Molecular Biology Reporter 26: 186-198.
54. Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW. 2012. Fire in Mediterranean ecosystems: ecology, evolution and management. Cambridge, UK: Cambridge University Press.
55. 4 grasslands. Ecological Letters 8: 683-690.
56. Kellman M. 1984. Synergistic relationships between fire and low soil fertility in neotropical savannas: a hypothesis. Biotropica 16: 158-160.
57. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26: 1463-1464.
58. 2 as a driver of past and current changes in savanna tree cover. Austral Ecology 35: 451-463.
59. Lehmann CER, Archibald SA, Hoffmann WA, Bond WJ. 2011. Deciphering the distribution of the savanna biome. New Phytologist 191: 197-209.
60. Li P, Johnston MO. 2000. Heterochrony in plant evolutionary studies through the twentieth century. The Botanical Review 66: 57-88.
61. Lock JM. 1998. Aspects of fire in tropical African vegetation. In: Huxley CR, Lock JM, Cutler DF, eds. Chorology, taxonomy and ecology of the floras of Africa and Madagascar. Kew, UK: Royal Botanic Gardens, 181-189.
62. Lock JM. 2006. The seasonally dry vegetation of Africa: parallels and comparisons with the neotropics. In: Pennington RT, Lewis GP, Ratter JA, eds. Neotropical savannas and seasonally dry forests: plant diversity, biogeography and conservation. London, UK: CRC Press, 450-465.
63. Matthews WS, van Wyk AE, van Rooyen N. 1999. Vegetation of the Sileza Nature Reserve and neighbouring areas, South Africa, and its importance in conserving woody grasslands of the Maputaland Centre of Endemism. Bothalia 29: 151-167.
64. Midgley J, Bond WJ. 2011. Pushing back in time: the role of fire in plant evolution. New Phytologist 191: 5-7.
65. Miller MA, Holder MT, Vos R, Midford PE, Liebowitz T, Chan L, Hoover P, Warnow T. 2009. The CIPRES portals. [WWW document] URL http://www.phylo.org/sub_sections/portal [accessed November 2012].
66. Morley RJ, Richards K. 1993. Gramineae cuticle: a key indicator of Late Cenozoic climatic change in the Niger Delta. Review of Palaeobotany and Palynology 77: 119-127.
67. Mucina L, Rutherford MC. 2006. The vegetation of South Africa, Lesotho and Swaziland. Pretoria, South Africa: South African National Biodiversity Institute.
68. Murphy BP, Bowman DMJS. 2012. What controls the distribution of tropical forest and savanna? Ecology Letters 15: 748-758.
69. Noss RF. 2012. Forgotten grasslands of the South: natural history and conservation. Washington, DC, USA: Island Press.
70. Nylander JAA. 2004. Modeltest v2. Program distributed by the author. Uppsala, Sweden: Evolutionary Biology Centre, Uppsala University.
71. Oliveira-Filho AT, Cardoso D, Schrire BD, Lewis GP, Pennington RT, Brummer TJ, Rotella J, Lavin M. 2013. Stability structures tropical woody plant diversity more than seasonality: insights into the ecology of high legume-succulent-plant biodiversity. South African Journal of Botany 89: 42-57.
72. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W. 2012. caper: comparative analyses of phylogenetics and evolution in R. R package version 0.5. [WWW document] URL http://CRAN.R-project.org/package=caper [accessed November 2012].
73. 4 grasslands? Journal of Ecology 96: 35-45.
74. 2 proxy. Paleoceanography 17: 21-1-21-12.
75. Pennington RT, Richardson JE, Lavin M. 2006. Insights into the historical construction of species-rich biomes from dated plant phylogenies, neutral ecological theory and phylogenetic community structure. New Phytologist 172: 605-616.
76. Plants of Southern Africa. 2012. Native plants of southern Africa. South African National Biodiversity Institute. [WWW document] URL www.plantzafrica.com [accessed November 2012].
77. Prior LD, Murphy BP, Russell-Smith J. 2009. Environmental and demographic correlates of tree recruitment and mortality in north Australian savannas. Forest Ecology and Management 257: 66-74.
78. Ratnam J, Bond WJ, Fensham RJ, Hoffmann WA, Archibald S, Lehmann CE, Sankaran M. 2011. When is a 'forest' a savanna, and why does it matter? Global Ecology and Biogeography 20: 653-660.
79. Ratter JA, Bridgewater S, Ribeiro JF, Fonsêca-Filho J, Rodrigues da Silva M, Milliken W, Pullan M, Pott A, Oliveira-Filho A, Durigan G et al. 2012. Analysis of the floristic composition of the Brazilian cerrado vegetation IV. Presentation of a Revised Data-Base of 367 Areas. [WWW document] URL http://www.cerrado.rbge.org.uk [accessed 20 November 2012].
80. Rodgers A, Salehe J, Howard G. 1996. The biodiversity of miombo woodlands. In: Campbell B, ed. The miombo in transition: woodlands and welfare in Africa. Bogor, Indonesia: Centre for International Forestry Research, 12.
81. 4 photosynthetic syndrome. Plant Biology 3: 202-213.
82. 4 photosynthesis. New Phytologist 161: 341-370.
83. 4 expansion in the late Miocene. New Phytologist 195: 653-666.
84. Schmidt E, Lotter M, McCleland W. 2007. Trees and shrubs of Mpumalanga and Kruger National Park. Johannesburg, South Africa: Jacana Education.
85. Scholes RJ, Archer SR. 1997. Tree-grass interactions in savannas. Annual Review of Ecology and Systematics 28: 517-544.
86. 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. Proceedings of the National Academy of Sciences, USA 106: 20359-20364.
87. Simon MF, Pennington T. 2012. Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. International Journal of Plant Sciences 173: 711-723.
88. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockinton SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS et al. 2011. Angiosperm phylogeny: 17 genes, 640 taxa. American Journal of Botany 98: 704-730.
89. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid Bootstrap Algorithm for the RAxML Web-Servers. Systematic Biology 75: 758-771.
90. Staver AC, Archibald S, Levin SA. 2011a. The global extent and determinants of savanna and forest as alternative biome states. Science 334: 230-232.
91. Staver AC, Archibald S, Levin SA. 2011b. Tree cover in sub-Saharan Africa: rainfall and fire constrain forest and savanna as alternative stable states. Ecology 92: 1063-1072.
92. Steenkamp Y, Kellerman MJS, van Wyk AE. 2001. Fire, frost, waterlogged soil or something else: what selected for the geoxylic suffrutex form in Africa? PlantLife 25: 4-6.
93. Strömberg CAE. 2005. Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proceedings of the National Academy of Sciences, USA 102: 11980-11984.
94. Strömberg CAE. 2011. Evolution of grass and grassland ecosystems. Annual Review of Earth and Planetary Sciences 39: 517-544.
95. Trollope WSW. 1984. Fire in savanna. In: Booysen PV, Tainton NM, eds. Ecological effects of fire in South African ecosystems. Berlin, Germany: Springer-Verlag, 149-176.
96. st edn. Pretoria, South Africa: Briza.
97. Vollesen K. 1981. Catunaregam pygmaea (Rubiaceae) - a new geoxylic suffrutex from the woodlands of SE Tanzania. Nordic Journal of Botany 1: 735-740.
98. Webb CO, Ackerly DD, Kembel SW. 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 18: 2098-2100.
99. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33: 475-505.
100. Webb CO, Donoghue MJ. 2005. Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 5: 181-183.
101. van der Werf GR, Randerson JT, Giglio L, Collatz GJ, Mu M, Kasibhatla PS, Morton DC, DeFries RS, Jin Y, van Leeuwen TT. 2010. Global fire emissions and the contribution of deforestation, savanna, forest, agricultural, and peat fires (1997-2009). Atmospheric Chemistry and Physics 10: 11707-11735.
102. Werner PA, Cowie ID, Cusack JS. 2006. Juvenile tree growth and demography in response to feral water buffalo in savannas of northern Australia: an experimental field study in Kakadu National Park. Australian Journal of Botany 54: 283-296.
103. Werner PA, Franklin DC. 2010. Resprouting and mortality of juvenile eucalypts in an Australian savanna: impacts of fire season and annual sorghum. Australian Journal of Botany 58: 619-628.
104. Werner PA, Prior LD. 2013. Demography and growth of subadult savanna trees: interactions of life history, size, fire season, and grassy understory. Ecological Monographs 83: 67-93.
105. White F. 1976. The underground forests of Africa: a preliminary review. The Gardens' Bulletin, Singapore 24: 57-71.
106. White F. 1979. The Guineo-Congolian Region and its relationship to other phytochoria. Bulletin Jardin Botanique National de Belgique 49: 11-55.
107. White F. 1983. The vegetation of Africa. A descriptive memoir to accompany the Unesco/AETFAT/UNSO vegetation map of Africa. Paris, France: Unesco.
108. Wikström N, Savolainen V, Chase MW. 2001. Evolution of the angiosperms: calibrating the family tree. Proceedings of the Royal Society Series B 268: 2211-2220.
109. Wilcoxon F. 1945. Individual comparisons by ranking methods. Biometrics Bulletin 1: 80-83.
110. Williams RJ, Cook GD, Gill AM, Moore PHR. 1999. Fire regime, fire intensity and tree survival in a tropical savanna in Northern Australia. Australian Journal of Ecology 24: 50-59.