Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
REVIEW

Buds, bushfires and resprouting in the eucalypts

G. E. Burrows
+ Author Affiliations
- Author Affiliations

Graham Centre for Agricultural Innovation, School of Agricultural and Wine Sciences, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia. Email: gburrows@csu.edu.au

Australian Journal of Botany 61(5) 331-349 https://doi.org/10.1071/BT13072
Submitted: 18 March 2013  Accepted: 13 May 2013   Published: 27 June 2013

Abstract

Eucalypts encounter a wide range of severe disturbances such as extensive defoliation by insects, major structural damage from cyclonic winds, as well as foliage and bark loss during drought and fire. Most healthy, mature eucalypts are not killed by these events, but regenerate vegetatively. With increasing intensity of disturbance, resprouting first occurs from the accessory buds in the small-diameter branchlets of the crown, followed by the epicormic buds in the medium- and large-diameter branches and stems, and then from the buds of the lignotuber. All these modes of regeneration are ultimately dependent on preventitious buds and, thus, the present review concentrates on axillary buds, their subsequent development into epicormic or lignotuber buds and their degree of protection from fire. The eucalypts have remarkably abundant, well protected and anatomically distinctive bud-forming structures in their leaf axils, branches, stems and lignotubers. These structures are quite consistent across this large genus, but are generally different from resprouting structures in many other plants. From an anatomical perspective, these structures seem best adapted to regeneration after fire, rather than damage from insects, storms or drought and this also correlates with ecological observations. On a worldwide basis, the eucalypts are some of the most successful post-fire resprouters, especially epicormic resprouting after medium- and high-intensity fires. Given the apparent ecological advantages of epicormic resprouting (the rapid reestablishment of extensive leaf area while simultaneously shading basal resprouters and seedlings) this could be an important factor in the success of eucalypts in Australia. Recent phylogenetic analysis has indicated a long relationship between eucalypts, fire and bud structures that facilitate resprouting.

Additional keywords: accessory, axillary, epicormic, Eucalyptus, fire, lignotuber, meristems.


References

Ashton DH (1975) The root and shoot development in Eucalyptus regnans F. Muell. Australian Journal of Botany 23, 867–887.
The root and shoot development in Eucalyptus regnans F. Muell.Crossref | GoogleScholarGoogle Scholar |

Bachelard EP (1969) Studies on the formation of epicormic shoots on eucalypt stem segments. Australian Journal of Biological Sciences 22, 1291–1296.

Bamber RK, Mullette KJ (1978) Studies of the lignotubers of Eucalyptus gummifera (Gaertn. & Hochr.). II. Anatomy. Australian Journal of Botany 26, 15–22.
Studies of the lignotubers of Eucalyptus gummifera (Gaertn. & Hochr.). II. Anatomy.Crossref | GoogleScholarGoogle Scholar |

Banks JCG, Paton DM (1993) Low temperature as an ecological factor in the cool-climate eucalypt forests. Studia Forestalia Suecica 191, 25–32.

Baranova EA (1960) Formation and development of axillary and dormant buds in Eucalyptus. Botanicheskii Zhurnal SSSR 45, 1169–1175.

Bell AD (1991) ‘Plant form. An illustrated guide to flowering plant morphology.’ (Oxford University Press: Oxford, UK)

Bell AD, Bell A, Dines TD (1999) Branch construction and bud defence status at the canopy surface of a West African rainforest. Biological Journal of the Linnean Society 66, 481–499.
Branch construction and bud defence status at the canopy surface of a West African rainforest.Crossref | GoogleScholarGoogle Scholar |

Benson D, McDougall L (1995) Ecology of Sydney plant species. Part 3. Dicotyledon families Cabombaceae to Eupomatiaceae. Cunninghamia 4, 217–431.

Benson D, McDougall L (1998) Ecology of Sydney plant species. Part 6. Dicotyledon family Myrtaceae. Cunninghamia 5, 808–987.

Benson D, McDougall L (2000) Ecology of Sydney plant species: Part 7b. Dicotyledon families Proteaceae to Rubiaceae. Cunninghamia 6, 1016–1202.

Bohte A, Drinnan A (2005) Floral development and systematic position of Arillastrum, Allosyncarpia, Stockwellia and Eucalyptopsis (Myrtaceae). Plant Systematics and Evolution 251, 53–70.
Floral development and systematic position of Arillastrum, Allosyncarpia, Stockwellia and Eucalyptopsis (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |

Bond WJ, Midgley JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends in Ecology & Evolution 16, 45–51.
Ecology of sprouting in woody plants: the persistence niche.Crossref | GoogleScholarGoogle Scholar |

Bond WJ, Midgley JJ (2003) The evolutionary ecology of sprouting in woody plants. International Journal of Plant Sciences 164, S103–S114.
The evolutionary ecology of sprouting in woody plants.Crossref | GoogleScholarGoogle Scholar |

Bond WJ, Midgley JJ (2012) Fire and the angiosperm revolutions. International Journal of Plant Sciences 173, 569–583.
Fire and the angiosperm revolutions.Crossref | GoogleScholarGoogle Scholar |

Bond WJ, Scott AC (2010) Fire and the spread of flowering plants in the Cretaceous. New Phytologist 188, 1137–1150.
Fire and the spread of flowering plants in the Cretaceous.Crossref | GoogleScholarGoogle Scholar | 20819174PubMed |

Bond WJ, Cook GD, Williams RJ (2012) Which trees dominate in savannas? The escape hypothesis and eucalypts in northern Australia. Austral Ecology 37, 678–685.
Which trees dominate in savannas? The escape hypothesis and eucalypts in northern Australia.Crossref | GoogleScholarGoogle Scholar |

Bowman DMJS (2000) ‘Australian rainforests: islands of green in a land of fire.’ (Cambridge University Press: Cambridge, UK)

Bradshaw SD, Dixon KW, Hopper SD, Lambers H, Turner SR (2011) Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends in Plant Science 16, 69–76.
Little evidence for fire-adapted plant traits in Mediterranean climate regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFKit78%3D&md5=278a955747f50a389fd901cc68168654CAS | 21095155PubMed |

Bradstock RA, Auld TD (1995) Soil temperatures during experimental bushfires in relation to fire intensity: consequences for legume germination and fire management in south-eastern Australia. Journal of Applied Ecology 32, 76–84.
Soil temperatures during experimental bushfires in relation to fire intensity: consequences for legume germination and fire management in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Bradstock RA, Gill AM, Williams RJ (2012) ‘Flammable Australia: fire regimes, biodiversity and ecosystems in a changing world.’ (CSIRO Publishing: Melbourne)

Brown SAE, Scott AC, Glasspool IJ, Collinson ME (2012) Cretaceous wildfires and their impact on the Earth system. Cretaceous Research 36, 162–190.
Cretaceous wildfires and their impact on the Earth system.Crossref | GoogleScholarGoogle Scholar |

Buckeridge JS (2010) Some biological consequences of environmental change: a study using barnacles (Cirripedia: Balanomorpha) and gum trees (Angiospermae: Myrtaceae). Integrative Zoology 5, 122–131.
Some biological consequences of environmental change: a study using barnacles (Cirripedia: Balanomorpha) and gum trees (Angiospermae: Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 21392330PubMed |

Burrows GE (1987) Leaf axil anatomy in the Araucariaceae. Australian Journal of Botany 35, 631–640.
Leaf axil anatomy in the Araucariaceae.Crossref | GoogleScholarGoogle Scholar |

Burrows GE (1990) The role of axillary meristems in coppice and epicormic bud initiation in Araucaria cunninghamii. Botanical Gazette 151, 293–301.
The role of axillary meristems in coppice and epicormic bud initiation in Araucaria cunninghamii.Crossref | GoogleScholarGoogle Scholar |

Burrows GE (1999) Wollemi pine (Wollemia nobilis, Araucariaceae) possesses the same unusual leaf axil anatomy as the other investigated members of the family. Australian Journal of Botany 47, 61–68.
Wollemi pine (Wollemia nobilis, Araucariaceae) possesses the same unusual leaf axil anatomy as the other investigated members of the family.Crossref | GoogleScholarGoogle Scholar |

Burrows GE (2000) An anatomical study of epicormic bud strand structure in Eucalyptus cladocalyx (Myrtaceae). Australian Journal of Botany 48, 233–245.
An anatomical study of epicormic bud strand structure in Eucalyptus cladocalyx (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |

Burrows GE (2002) Epicormic strand structure in Angophora, Eucalyptus and Lophostemon (Myrtaceae) – implications for fire resistance and recovery. New Phytologist 153, 111–131.
Epicormic strand structure in Angophora, Eucalyptus and Lophostemon (Myrtaceae) – implications for fire resistance and recovery.Crossref | GoogleScholarGoogle Scholar |

Burrows GE (2008) Syncarpia and Tristaniopsis (Myrtaceae) possess specialised fire-resistant epicormic structures. Australian Journal of Botany 56, 254–264.
Syncarpia and Tristaniopsis (Myrtaceae) possess specialised fire-resistant epicormic structures.Crossref | GoogleScholarGoogle Scholar |

Burrows N, Wardell-Johnson G (2003) Fire and plant interactions in forested ecosystems of south-west Western Australia. In ‘Fire in ecosystems of south-west Western Australia: impacts and management’. (Eds I Abbott, N Burrows) pp. 225–268. (Backhuys Publishers: Leiden, The Netherlands)

Burrows GE, Offord CA, Meagher PF, Ashton K (2003) Axillary meristems and the development of epicormic buds in wollemi pine (Wollemia nobilis). Annals of Botany 92, 835–844.
Axillary meristems and the development of epicormic buds in wollemi pine (Wollemia nobilis).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srjtlWmuw%3D%3D&md5=a072a01796063a8630bb848fd59a7423CAS | 14612379PubMed |

Burrows GE, Hornby SK, Waters DA, Bellairs SM, Prior LD, Bowman DMJS (2008a) Leaf axil anatomy and bud reserves in 21 Myrtaceae species from northern Australia. International Journal of Plant Sciences 169, 1174–1186.
Leaf axil anatomy and bud reserves in 21 Myrtaceae species from northern Australia.Crossref | GoogleScholarGoogle Scholar |

Burrows ND, Wardell-Johnson G, Ward B (2008b) Post-fire juvenile period of plants in south-west Australia forests and implications for fire management. Journal of the Royal Society of Western Australia 91, 163–174.

Burrows GE, Hornby SK, Waters DA, Bellairs SM, Prior LD, Bowman DMJS (2010) A wide diversity of epicormic structures is present in Myrtaceae species in the northern Australian savanna biome – implications for adaptation to fire. Australian Journal of Botany 58, 493–507.
A wide diversity of epicormic structures is present in Myrtaceae species in the northern Australian savanna biome – implications for adaptation to fire.Crossref | GoogleScholarGoogle 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. Proceedings of the Royal Society B Biological Sciences 278, 188–195.
Estimating the age of fire in the Cape flora of South Africa from an orchid phylogeny.Crossref | GoogleScholarGoogle Scholar |

Carey G (1930) The leaf-buds of some woody perennials in the New South Wales flora. Proceedings of the Linnean Society of New South Wales 55, 708–737.

Carey G (1931) A note on the leaf buds of angophoras. Proceedings of the Linnean Society of New South Wales 56, 455–457.

Carey A, Evans M, Hann P, Lintermans M, MacDonald T, Ormay P, Sharp S, Shorthouse D, Webb N (2003) ‘Wildfires in the ACT 2003: report on initial impacts on natural ecosystems.’ (Environment ACT: Canberra)

Carr DJ, Jahnke R, Carr SGM (1983) Development of the lignotuber and plant form in Lehmannianae. Australian Journal of Botany 31, 629–643.
Development of the lignotuber and plant form in Lehmannianae.Crossref | GoogleScholarGoogle Scholar |

Carr DJ, Jahnke R, Carr SGM (1984) Initiation, development and anatomy of lignotubers in some species of Eucalyptus. Australian Journal of Botany 32, 415–437.
Initiation, development and anatomy of lignotubers in some species of Eucalyptus.Crossref | GoogleScholarGoogle Scholar |

Carrodus BB, Blake TJ (1970) Studies on the lignotubers of Eucalyptus obliqua L’Heri. I. The nature of the lignotuber. New Phytologist 69, 1069–1072.
Studies on the lignotubers of Eucalyptus obliqua L’Heri. I. The nature of the lignotuber.Crossref | GoogleScholarGoogle Scholar |

Catry FX, Rego FC, Bugalho MN, Lopes T, Silva JS, Moreira F (2006) Effects of fire on tree survival and regeneration in a Mediterranean ecosystem. Forest Ecology and Management 234, S197
Effects of fire on tree survival and regeneration in a Mediterranean ecosystem.Crossref | GoogleScholarGoogle Scholar |

Chattaway MM (1958) Bud development and lignotuber formation in eucalypts. Australian Journal of Botany 6, 103–115.
Bud development and lignotuber formation in eucalypts.Crossref | GoogleScholarGoogle Scholar |

Choczynska J, Johnson EA (2009) A soil heat and water transfer model to predict belowground grass rhizome bud death in a grass fire. Journal of Vegetation Science 20, 277–287.
A soil heat and water transfer model to predict belowground grass rhizome bud death in a grass fire.Crossref | GoogleScholarGoogle Scholar |

Chong C, Edwards W, Waycott M (2007) Differences in resprouting ability are not related to seed size or seedling growth in four riparian woody species. Journal of Ecology 95, 840–850.
Differences in resprouting ability are not related to seed size or seedling growth in four riparian woody species.Crossref | GoogleScholarGoogle Scholar |

Chudnoff M (1971) Tissue regeneration of debarked eucalypts. Forest Science 17, 300–305.

Clarke PJ (2002) Habitat insularity and fire response traits: evidence from a sclerophyll archipelago. Oecologia 132, 582–591.
Habitat insularity and fire response traits: evidence from a sclerophyll archipelago.Crossref | GoogleScholarGoogle Scholar |

Clarke PJ, Knox KJE, Campbell ML, Copeland LM (2009) Post-fire recovery of woody plants in the New England Tableland Bioregion. Cunninghamia 11, 221–239.

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 resources drive persistence after fire. New Phytologist 197, 19–35.
Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s%2FptlGmsw%3D%3D&md5=4fd5ff13474096d4181cdb6a0794da66CAS | 23110592PubMed |

Colin F, Mothe F, Freyburger C, Morisset JB, Leban JM, Fontaine F (2010) Tracking rameal traces in sessile oak trunks with X-ray computer tomography: biological bases, preliminary results and perspectives. Trees Structure and Function 24, 953–967.
Tracking rameal traces in sessile oak trunks with X-ray computer tomography: biological bases, preliminary results and perspectives.Crossref | GoogleScholarGoogle Scholar |

Colin F, Sanjines A, Fortin M, Bontemps JD, Nicolini E (2012) Fagus sylvatica trunk epicormics in relation to primary and secondary growth. Annals of Botany 110, 995–1005.
Fagus sylvatica trunk epicormics in relation to primary and secondary growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38fnsV2ktA%3D%3D&md5=3bbc5cca857f9a6fae49d526f2de8767CAS | 22887022PubMed |

Collett NG, Fagg PC (2010) Insect defoliation of mixed-species eucalypts in East Gippsland. Australian Forestry 73, 81–90.
Insect defoliation of mixed-species eucalypts in East Gippsland.Crossref | GoogleScholarGoogle Scholar |

Commonwealth Government of Australia (1999) ‘Comprehensive regional assessment. World heritage sub-theme: eucalypt-dominated vegetation.’ (Government Printer: Canberra)

Cremer KW (1972) Morphology and development of the primary and accessory buds of Eucalyptus regnans. Australian Journal of Botany 20, 175–195.
Morphology and development of the primary and accessory buds of Eucalyptus regnans.Crossref | GoogleScholarGoogle Scholar |

Crisp MD, Burrows GE, Cook LG, Thornhill AH, Bowman DMJS (2011) Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary. Nature Communications 2, 193
Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary.Crossref | GoogleScholarGoogle Scholar | 21326225PubMed |

Croft P, Hunter JT, Reid N (2007) Depletion of regenerative bud resources during cyclic drought: what are the implications for fire management? Ecological Management & Restoration 8, 187–192.
Depletion of regenerative bud resources during cyclic drought: what are the implications for fire management?Crossref | GoogleScholarGoogle Scholar |

Davidson NJ, Reid JB (1989) Response of eucalypt species to drought. Australian Journal of Ecology 14, 139–156.
Response of eucalypt species to drought.Crossref | GoogleScholarGoogle Scholar |

Falster DS, Westoby M (2005) Tradeoffs between height growth rate, stem persistence and maximum height among plant species in a post-fire succession. Oikos 111, 57–66.
Tradeoffs between height growth rate, stem persistence and maximum height among plant species in a post-fire succession.Crossref | GoogleScholarGoogle Scholar |

Fernandes PM, Vega JA, Jiménez E, Rigolot E (2008) Fire resistance of European pines. Forest Ecology and Management 256, 246–255.
Fire resistance of European pines.Crossref | GoogleScholarGoogle Scholar |

Fink S (1980) Anatomische untersuchungen über das vorkommen von spross- und wurzelanlagen im stammbereich von laub- und nadelbäumen. I. Proventive anlagen. Allgemeine Forst- und Jagdzeitung 151, 160–180.

Fink S (1983) The occurrence of adventitious and preventitious buds within the bark of some temperate and tropical trees. American Journal of Botany 70, 532–542.
The occurrence of adventitious and preventitious buds within the bark of some temperate and tropical trees.Crossref | GoogleScholarGoogle Scholar |

Fink S (1999) ‘Pathological and regenerative plant anatomy.’ (Gebrüder Borntraeger: Berlin)

Florence RG (1996) ‘Ecology and silviculture of eucalypt forests.’ (CSIRO Publishing: Melbourne)

Franklin DC, Gunton RM, Schatz J, Lawes MJ (2010) Resprouting responses of trees in a fire-prone tropical savanna following severe tornado damage. Austral Ecology 35, 685–694.
Resprouting responses of trees in a fire-prone tropical savanna following severe tornado damage.Crossref | GoogleScholarGoogle Scholar |

Gandolfo MA, Hermsen EJ, Zamaloa MC, Nixon KC, González CC, Wilf P, Cúneo NR, Johnson KR (2011) Oldest known Eucalyptus macrofossils are from South America. PLoS One 6, e21084
Oldest known Eucalyptus macrofossils are from South America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1yqtLg%3D&md5=38da3e7c6f40e64de8375167f9d99889CAS | 21738605PubMed |

Gill AM (1978) Crown recovery of Eucalyptus dives following wildfire. Australian Forestry 41, 207–214.
Crown recovery of Eucalyptus dives following wildfire.Crossref | GoogleScholarGoogle Scholar |

Gill AM (1980) Restoration of bark thickness after fire and mechanical injury in a smooth-barked eucalypt. Australian Forest Research 10, 311–319.

Gill AM, Cheney NP, Walker J, Tunstall BR (1986) Bark losses from two eucalypt species following fires of different intensities. Australian Forest Research 16, 1–7.

Gillison AN, Lacey CJ, Bennett RH (1980) Rhizo-stolons in Eucalyptus. Australian Journal of Botany 28, 299–304.
Rhizo-stolons in Eucalyptus.Crossref | GoogleScholarGoogle Scholar |

Glasby P, Selkirk PM, Adamson D, Downing AJ, Selkirk DR (1988) Blue mountains ash (Eucalyptus oreades R. T. Baker) in the western Blue Mountains. Proceedings of the Linnean Society of New South Wales 110, 141–158.

Gosper CR, Prober SM, Yates CJ (2010) Chaining and burning modifies vegetation structure, fuel, and post-disturbance sprouting capacity. Rangeland Ecology and Management 63, 588–592.
Chaining and burning modifies vegetation structure, fuel, and post-disturbance sprouting capacity.Crossref | GoogleScholarGoogle Scholar |

Grady JM, Hoffmann WA (2012) Caught in a fire trap: recurring fire creates stable size equilibria in woody resprouters. Ecology 93, 2052–2060.
Caught in a fire trap: recurring fire creates stable size equilibria in woody resprouters.Crossref | GoogleScholarGoogle Scholar | 23094377PubMed |

Graham AW, Wallwork MA, Sedgley M (1998) Lignotuber bud development in Eucalyptus cinerea (F.Muell. ex Benth.). International Journal of Plant Sciences 159, 979–988.

Grant CD, Koch JM, Bell DT, Loneragan WA (1997) Tree species response to prescribed burns in rehabilitated bauxite mines in Western Australia. Australian Forestry 60, 84–89.
Tree species response to prescribed burns in rehabilitated bauxite mines in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Grattapaglia D, Vaillancourt RE, Shepherd M, Thumma BR, Foley W, Külheim C, Potts BM, Myburg AA (2012) Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus. Tree Genetics & Genomes 8, 463–508.
Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus.Crossref | GoogleScholarGoogle Scholar |

He T, Lamont BB, Downes KS (2011) Banksia born to burn. New Phytologist 191, 184–196.
Banksia born to burn.Crossref | GoogleScholarGoogle Scholar | 21388378PubMed |

He T, Pausas JG, Belcher CM, Schwilk DW, Lamont BB (2012) Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytologist 194, 751–759.
Fire-adapted traits of Pinus arose in the fiery Cretaceous.Crossref | GoogleScholarGoogle Scholar | 22348443PubMed |

Hermsen EJ, Gandolfo MA, Zamaloa MC (2012) The fossil record of Eucalyptus in Patagonia. American Journal of Botany 99, 1356–1374.
The fossil record of Eucalyptus in Patagonia.Crossref | GoogleScholarGoogle Scholar | 22859652PubMed |

Hervé P, Jauneau A, Pâques M, Marien JN, Boudet AM, Teulières C (2001) A procedure for shoot organogenesis in vitro from leaves and nodes of an elite Eucalyptus gunnii clone: comparative histology. Plant Science 161, 645–653.
A procedure for shoot organogenesis in vitro from leaves and nodes of an elite Eucalyptus gunnii clone: comparative histology.Crossref | GoogleScholarGoogle Scholar |

Higgins SI, Bond WJ, Combrink H, Craine JM, February EC, Govender N, Lannas K, Moncreiff G, Trollope WSW (2012) Which traits determine shifts in the abundance of tree species in a fire-prone savanna? Journal of Ecology 100, 1400–1410.
Which traits determine shifts in the abundance of tree species in a fire-prone savanna?Crossref | GoogleScholarGoogle Scholar |

Hodgkinson KC (1998) Sprouting success of shrubs after fire: height-dependent relationships for different strategies. Oecologia 115, 64–72.
Sprouting success of shrubs after fire: height-dependent relationships for different strategies.Crossref | GoogleScholarGoogle Scholar |

Hoffmann WA, Adasme R, Haridasan M, de Carvalho MT, Geiger EL, Pereira MAB, Gotsch SG, Franco AC (2009) Tree topkill, not mortality, governs the dynamics of savanna–forest boundaries under frequent fire in central Brazil. Ecology 90, 1326–1337.
Tree topkill, not mortality, governs the dynamics of savanna–forest boundaries under frequent fire in central Brazil.Crossref | GoogleScholarGoogle Scholar | 19537552PubMed |

Horton BM, Close DC, Wardlaw TJ, Davidson NJ (2011) Crown condition assessment: an accurate, precise and efficient method with broad applicability to Eucalyptus. Austral Ecology 36, 709–721.

Jacobs MR (1955) ‘Growth habits of the eucalypts.’ (Forestry and Timber Bureau: Canberra)

James S (1984) Lignotubers and burls – their structure, function and ecological significance in Mediterranean ecosystems. Botanical Review 50, 225–266.
Lignotubers and burls – their structure, function and ecological significance in Mediterranean ecosystems.Crossref | GoogleScholarGoogle Scholar |

Kauffman JB (1991) Survival by sprouting following fire in tropical forests of the eastern Amazon. Biotropica 23, 219–224.
Survival by sprouting following fire in tropical forests of the eastern Amazon.Crossref | GoogleScholarGoogle Scholar |

Kauffman JB, Uhl C (1990) Interactions of anthropogenic activities, fire, and rain forests in the Amazon basin. In ‘Fire in the tropical biota’. (Ed. JG Goldammer) pp. 117–134. (Springer-Verlag: Berlin)

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

Keith H, Mackey B, Berry S, Lindenmayer D, Gibbons P (2010) Estimating carbon carrying capacity in natural forest ecosystems across heterogeneous landscapes: addressing sources of error. Global Change Biology 16, 2971–2989.

Kerr LR (1925) The lignotubers of eucalypt seedlings. Proceedings of the Royal Society of Victoria 37, 79–97.

Lacey CJ (1974) Rhizomes in tropical eucalypts and their role in recovery from fire damage. Australian Journal of Botany 22, 29–38.
Rhizomes in tropical eucalypts and their role in recovery from fire damage.Crossref | GoogleScholarGoogle Scholar |

Lacey CJ, Johnston RD (1990) Woody clumps and clumpwoods. Australian Journal of Botany 38, 299–334.
Woody clumps and clumpwoods.Crossref | GoogleScholarGoogle Scholar |

Lacey CJ, Whelan PI (1976) Observations on the ecological significance of vegetative reproduction in the Katherine–Darwin region of the Northern Territory. Australian Forestry 39, 131–139.
Observations on the ecological significance of vegetative reproduction in the Katherine–Darwin region of the Northern Territory.Crossref | GoogleScholarGoogle Scholar |

Lamont BB, Downes KS (2011) Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa. Plant Ecology 212, 2111–2125.
Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa.Crossref | GoogleScholarGoogle Scholar |

Lamont BB, He T (2012) Fire-adapted Gondwanan angiosperm floras evolved in the Cretaceous. BMC Evolutionary Biology 12, 223
Fire-adapted Gondwanan angiosperm floras evolved in the Cretaceous.Crossref | GoogleScholarGoogle Scholar | 23171161PubMed |

Lamont BB, Markey A (1995) Biogeography of fire-killed and resprouting Banksia species in south-western Australia. Australian Journal of Botany 43, 283–303.
Biogeography of fire-killed and resprouting Banksia species in south-western Australia.Crossref | GoogleScholarGoogle Scholar |

Lawes MJ, Adie H, Russell-Smith J, Murphy B, Midgley JJ (2011a) How do small savanna trees avoid stem mortality by fire? The roles of stem diameter, height and bark thickness. Ecosphere 2, art42
How do small savanna trees avoid stem mortality by fire? The roles of stem diameter, height and bark thickness.Crossref | GoogleScholarGoogle Scholar |

Lawes MJ, Richards A, Dathe J, Midgley JJ (2011b) Bark thickness determines fire resistance of selected tree species from fire-prone tropical savanna in north Australia. Plant Ecology 212, 2057–2069.
Bark thickness determines fire resistance of selected tree species from fire-prone tropical savanna in north Australia.Crossref | GoogleScholarGoogle Scholar |

Lawes MJ, Midgley JJ, Clarke PJ (2013) Costs and benefits of relative bark thickness in relation to fire damage: a savanna/forest contrast. Journal of Ecology 101, 517–524.
Costs and benefits of relative bark thickness in relation to fire damage: a savanna/forest contrast.Crossref | GoogleScholarGoogle Scholar |

Lee SK, Rao AN (1984) Axillary buds of some tropical trees. Gardens’ Bulletin Singapore 37, 65–79.

Lev-Yadun S, Aloni R (1993) Bark structure and mode of canopy regeneration in trees of Melia azedarach L. Trees Structure and Function 7, 144–147.

Matthews A, Lunney D, Gresser S, Maitz W (2007) Tree use by koalas (Phascolarctos cinereus) after fire in remnant coastal forest. Wildlife Research 34, 84–93.
Tree use by koalas (Phascolarctos cinereus) after fire in remnant coastal forest.Crossref | GoogleScholarGoogle Scholar |

McArthur AG (1968) The fire resistance of eucalypts. Proceedings of the Ecological Society of Australia 3, 83–90.

McCaw WL, Smith RH, Neal JE (1994) Stem damage and crown recovery following high intensity fire in a 16-year-old stand of Eucalyptus diversicolour and Eucalyptus muellerana. Australian Forestry 57, 76–81.
Stem damage and crown recovery following high intensity fire in a 16-year-old stand of Eucalyptus diversicolour and Eucalyptus muellerana.Crossref | GoogleScholarGoogle Scholar |

McCaw WL, Smith RH, Neal JE (1997) Prescribed burning of thinning slash in regrowth stands of karri (Eucalyptus diversicolor) 1. Fire characteristics, fuel consumption and tree damage. International Journal of Wildland Fire 7, 29–40.
Prescribed burning of thinning slash in regrowth stands of karri (Eucalyptus diversicolor) 1. Fire characteristics, fuel consumption and tree damage.Crossref | GoogleScholarGoogle Scholar |

Medeiros MB, Miranda HS (2008) Post-fire resprouting and mortality in cerrado woody plant species over a three-year period. Edinburgh Journal of Botany 65, 53–68.
Post-fire resprouting and mortality in cerrado woody plant species over a three-year period.Crossref | GoogleScholarGoogle Scholar |

Meier AR, Saunders MR, Michler CH (2012) Epicormic buds in trees: a review of bud establishment, development and dormancy release. Tree Physiology 32, 565–584.
Epicormic buds in trees: a review of bud establishment, development and dormancy release.Crossref | GoogleScholarGoogle Scholar | 22555307PubMed |

Michaletz ST, Johnson EA (2007) How forest fires kill trees: a review of the fundamental biophysical processes. Scandinavian Journal of Forest Research 22, 500–515.
How forest fires kill trees: a review of the fundamental biophysical processes.Crossref | GoogleScholarGoogle Scholar |

Michaletz ST, Johnson EA (2008) A biophysical process model of tree mortality in surface fires. Canadian Journal of Forest Research 38, 2013–2029.
A biophysical process model of tree mortality in surface fires.Crossref | GoogleScholarGoogle Scholar |

Michaletz ST, Johnson EA, Tyree MT (2012) Moving beyond the cambium necrosis hypothesis of post-fire tree mortality: cavitation and deformation of xylem in forest fires. New Phytologist 194, 254–263.
Moving beyond the cambium necrosis hypothesis of post-fire tree mortality: cavitation and deformation of xylem in forest fires.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383mt12gtA%3D%3D&md5=dc6b0f5b0aeb451d2846b8a8af64c345CAS | 22276783PubMed |

Midgley JJ (1996) Why the world’s vegetation is not totally dominated by resprouting plants; because resprouters are shorter than reseeders. Ecography 19, 92–95.
Why the world’s vegetation is not totally dominated by resprouting plants; because resprouters are shorter than reseeders.Crossref | GoogleScholarGoogle Scholar |

Midgley JJ, Bond WJ (2011) Pushing back in time: the role of fire in plant evolution. New Phytologist 191, 5–7.
Pushing back in time: the role of fire in plant evolution.Crossref | GoogleScholarGoogle Scholar |

Midgley JJ, Kruger LM, Skelton R (2011) How do fires kill plants? The hydraulic death hypothesis and Cape Proteaceae ‘fire-resisters’. South African Journal of Botany 77, 381–386.
How do fires kill plants? The hydraulic death hypothesis and Cape Proteaceae ‘fire-resisters’.Crossref | GoogleScholarGoogle Scholar |

Montenegro G, Ginocchio R, Segura A, Keely JE, Gómez M (2004) Fire regimes and vegetation responses in two Mediterranean-climate regions. Revista Chilena de Historia Natural 77, 455–464.
Fire regimes and vegetation responses in two Mediterranean-climate regions.Crossref | GoogleScholarGoogle Scholar |

Moreira B, Tormo J, Pausas JG (2012) To resprout or not to resprout: factors driving intraspecific variability in resprouting. Oikos 121, 1577–1584.
To resprout or not to resprout: factors driving intraspecific variability in resprouting.Crossref | GoogleScholarGoogle Scholar |

Morisset JB, Mothe F, Colin F (2012) Observation of Quercus petraea epicormics with X-ray CT reveals strong pith-to-bark correlations: silvicultural and ecological implications. Forest Ecology and Management 278, 127–137.
Observation of Quercus petraea epicormics with X-ray CT reveals strong pith-to-bark correlations: silvicultural and ecological implications.Crossref | GoogleScholarGoogle Scholar |

Morrison DA, Renwick JA (2000) Effects of variation in fire intensity on regeneration of co-occurring species of small trees in the Sydney region. Australian Journal of Botany 48, 71–79.
Effects of variation in fire intensity on regeneration of co-occurring species of small trees in the Sydney region.Crossref | GoogleScholarGoogle Scholar |

Nicolle D (2006) A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus-Myrtaceae), with special reference to the obligate seeders. Australian Journal of Botany 54, 391–407.
A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus-Myrtaceae), with special reference to the obligate seeders.Crossref | GoogleScholarGoogle Scholar |

Noble JC (2001) Lignotubers and meristem dependence in mallee (Eucalyptus spp.) coppicing after fire. Australian Journal of Botany 49, 31–41.
Lignotubers and meristem dependence in mallee (Eucalyptus spp.) coppicing after fire.Crossref | GoogleScholarGoogle Scholar |

North MP, Hurteau MD (2011) High-severity wildfire effects on carbon stocks and emissions in fuels treated and untreated forest. Forest Ecology and Management 261, 1115–1120.
High-severity wildfire effects on carbon stocks and emissions in fuels treated and untreated forest.Crossref | GoogleScholarGoogle Scholar |

O’Gara E, Howard K, Colquhoun IJ, Dell B, McComb J, Hardy GESJ (2009) The development and characteristics of periderm and rhytidome in Eucalyptus marginata. Australian Journal of Botany 57, 221–228.
The development and characteristics of periderm and rhytidome in Eucalyptus marginata.Crossref | GoogleScholarGoogle Scholar |

Ogden J, Basher L, McGlone M (1998) Fire, forest regeneration and links with early human habitation: evidence from New Zealand. Annals of Botany 81, 687–696.
Fire, forest regeneration and links with early human habitation: evidence from New Zealand.Crossref | GoogleScholarGoogle Scholar |

Ohmart CP, Edwards PB (1991) Insect herbivory on Eucalyptus. Annual Review of Entomology 36, 637–657.
Insect herbivory on Eucalyptus.Crossref | GoogleScholarGoogle Scholar |

Paula S, Arianoutsou M, Kazanis D, Tavsanoglu Ç, Lloret F, Buhk C, Ojeda F, Luna B, Moreno JM, Rodrigo A, Espelta JM, Palacio S, Fernández-Santos B, Fernandes PM, Pausas JG (2009) Fire-related traits for plant species of the Mediterranean Basin. Ecology 90, 1420
Fire-related traits for plant species of the Mediterranean Basin.Crossref | GoogleScholarGoogle Scholar |

Pausas JG (1997) Resprouting of Quercus suber in NE Spain after fire. Journal of Vegetation Science 8, 703–706.
Resprouting of Quercus suber in NE Spain after fire.Crossref | GoogleScholarGoogle Scholar |

Pausas JG, Keeley JE (2009) A burning story: the role of fire in the history of life. Bioscience 59, 593–601.
A burning story: the role of fire in the history of life.Crossref | GoogleScholarGoogle Scholar |

Pausas JG, Schwilk DW (2012) Fire and plant evolution. New Phytologist 193, 301–303.
Fire and plant evolution.Crossref | GoogleScholarGoogle Scholar | 22221150PubMed |

Peter DH, Agee JK, Sprugel DG (2009) Bud damage from controlled heat treatments in Quercus garryana. Trees Structure and Function 23, 381–390.
Bud damage from controlled heat treatments in Quercus garryana.Crossref | GoogleScholarGoogle Scholar |

Putz FE, Brokaw NVL (1989) Sprouting of broken trees on Barro Colorado Island, Panama. Ecology 70, 508–512.
Sprouting of broken trees on Barro Colorado Island, Panama.Crossref | GoogleScholarGoogle Scholar |

Schweingruber FH, Börner A, Schulze E-D (2006) ‘Atlas of woody plant stems. Evolution, structure, and environmental modifications.’ (Springer: Heidelberg, Germany)

Setterfield SA, Rossiter-Rachor NA, Hutley LB, Douglas MM, Williams RJ (2010) Turning up the heat: the impacts of Andropogon gayanus (gamba grass) invasion on fire behaviour in northern Australian savannas. Diversity & Distributions 16, 854–861.
Turning up the heat: the impacts of Andropogon gayanus (gamba grass) invasion on fire behaviour in northern Australian savannas.Crossref | GoogleScholarGoogle Scholar |

Shukla A, Mehrotra RC, Tyagi A (2012) The oldest fossil of Eucalyptus from the Late Maastrichtian–Danian of India and the theory of its Gondwanic origin. Current Science 103, 74–80.

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.
Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian cerrado.Crossref | GoogleScholarGoogle 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. Proceedings of the National Academy of Sciences, USA 106, 20 359–20 364.
Recent assembly of the cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFSqtQ%3D%3D&md5=5f9e2fa4529062b0a8c5ecc628fa2dfaCAS |

Tozer MG, Auld TD (2006) Soil heating and germination: investigations using leaf scorch on graminoids and experimental seed burial. International Journal of Wildland Fire 15, 509–516.
Soil heating and germination: investigations using leaf scorch on graminoids and experimental seed burial.Crossref | GoogleScholarGoogle Scholar |

Verdaguer D, Ojeda F (2005) Evolutionary transition from resprouter to seeder life history in two Erica (Ericaceae) species: insights from seedling axillary buds. Annals of Botany 95, 593–599.
Evolutionary transition from resprouter to seeder life history in two Erica (Ericaceae) species: insights from seedling axillary buds.Crossref | GoogleScholarGoogle Scholar | 15661748PubMed |

Vesk PA (2006) Plant size and resprouting ability: trading tolerance and avoidance of damage? Journal of Ecology 94, 1027–1034.
Plant size and resprouting ability: trading tolerance and avoidance of damage?Crossref | GoogleScholarGoogle Scholar |

Vesk PA, Westoby M (2003) Drought damage and recovery – a conceptual model. New Phytologist 160, 7–14.
Drought damage and recovery – a conceptual model.Crossref | GoogleScholarGoogle Scholar |

Vesk PA, Westoby M (2004) Funding the bud bank: a review of the costs of buds. Oikos 106, 200–208.
Funding the bud bank: a review of the costs of buds.Crossref | GoogleScholarGoogle Scholar |

Vines RG (1968) Heat transfer through bark, and the resistance of trees to fire. Australian Journal of Botany 16, 499–514.
Heat transfer through bark, and the resistance of trees to fire.Crossref | GoogleScholarGoogle Scholar |

Wardell-Johnson GW (2000) Responses of forest eucalypts to moderate and high intensity fire in the Tingle Mosaic, south-western Australia: comparisons between locally endemic and regionally distributed species. Austral Ecology 25, 409–421.
Responses of forest eucalypts to moderate and high intensity fire in the Tingle Mosaic, south-western Australia: comparisons between locally endemic and regionally distributed species.Crossref | GoogleScholarGoogle Scholar |

Waters DA, Burrows GE, Harper JDI (2010) Eucalyptus regnans (Myrtaceae): a fire-sensitive eucalypt with a resprouter epicormic structure. American Journal of Botany 97, 545–556.
Eucalyptus regnans (Myrtaceae): a fire-sensitive eucalypt with a resprouter epicormic structure.Crossref | GoogleScholarGoogle Scholar | 21622417PubMed |

Werner PA, Murphy PG (2001) Size-specific biomass allocation and water content of above- and below-ground components of three Eucalyptus species in a northern Australian savanna. Australian Journal of Botany 49, 155–167.
Size-specific biomass allocation and water content of above- and below-ground components of three Eucalyptus species in a northern Australian savanna.Crossref | GoogleScholarGoogle Scholar |

Wildy DT, Pate JS (2002) Quantifying above- and below-ground growth responses of the western Australian oil mallee, Eucalyptus kochii subsp. plenissima, to contrasting decapitation regimes. Annals of Botany 90, 185–197.
Quantifying above- and below-ground growth responses of the western Australian oil mallee, Eucalyptus kochii subsp. plenissima, to contrasting decapitation regimes.Crossref | GoogleScholarGoogle Scholar | 12197516PubMed |

Wilkinson G, Jennings S (1993) Survival and recovery of Eucalyptus obliqua regeneration following wildfire. Tasforests 5, 1–11.

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.
Fire regime, fire intensity and tree survival in a tropical savanna in northern Australia.Crossref | GoogleScholarGoogle Scholar |

Williams PR, Congdon RA, Grice AC, Clarke PJ (2004) Soil temperature and depth of legume germination during early and late dry season fires in a tropical eucalypt savanna of north-eastern Australia. Austral Ecology 29, 258–263.
Soil temperature and depth of legume germination during early and late dry season fires in a tropical eucalypt savanna of north-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Williams PR, Parsons M, Jensen R, Tran C (2012a) Mechanisms of rainforest persistence and recruitment in frequently burnt wet tropical eucalypt forests. Austral Ecology 37, 268–275.
Mechanisms of rainforest persistence and recruitment in frequently burnt wet tropical eucalypt forests.Crossref | GoogleScholarGoogle Scholar |

Williams RJ, Bradstock RA, Barrett D, Beringer J, Boer MM, Cary GJ, Cook GD, Gill AM, Hutley LB, Keith H, Maier SW, Meyer CP, Price O, Roxburgh SH, Russell-Smith J (2012b) Fire regimes and carbon in Australian vegetation. In ‘Flammable Australia. Fire regimes, biodiversity and ecosystems in a changing world’. (Eds RA Bradstock, AM Gill, RJ Williams) pp. 273–291. (CSIRO Publishing: Melbourne)

Wright BR, Clarke PJ (2007) Resprouting responses of Acacia shrubs in the Western Desert of Australia – fire severity, interval and season influence survival. International Journal of Wildland Fire 16, 317–323.
Resprouting responses of Acacia shrubs in the Western Desert of Australia – fire severity, interval and season influence survival.Crossref | GoogleScholarGoogle Scholar |

Wrigley J, Fagg M (2010) ‘Eucalypts a celebration.’ (Allen and Unwin: Sydney)