Unearthing belowground bud banks in fire-prone ecosystems.

Despite long-time awareness of the importance of the location of buds in plant biology, research on belowground bud banks has been scant. Terms such as lignotuber, xylopodium and sobole, all referring to belowground bud-bearing structures, are used inconsistently in the literature. Because soil efficiently insulates meristems from the heat of fire, concealing buds below ground provides fitness benefits in fire-prone ecosystems. Thus, in these ecosystems, there is a remarkable diversity of bud-bearing structures. There are at least six locations where belowground buds are stored: roots, root crown, rhizomes, woody burls, fleshy swellings and belowground caudexes. These support many morphologically distinct organs. Given their history and function, these organs may be divided into three groups: those that originated in the early history of plants and that currently are widespread (bud-bearing roots and root crowns); those that also originated early and have spread mainly among ferns and monocots (nonwoody rhizomes and a wide range of fleshy underground swellings); and those that originated later in history and are strictly tied to fire-prone ecosystems (woody rhizomes, lignotubers and xylopodia). Recognizing the diversity of belowground bud banks is the starting point for understanding the many evolutionary pathways available for responding to severe recurrent disturbances.

[1]  S. Little,et al.  Buds Enable Pitch and Shortleaf Pines to Recover From Injury , 2019 .

[2]  S. Arndt,et al.  Whole-tree distribution and temporal variation of non-structural carbohydrates in broadleaf evergreen trees , 2018, Tree physiology.

[3]  J. Keeley,et al.  Epicormic Resprouting in Fire-Prone Ecosystems. , 2017, Trends in plant science.

[4]  J. Pausas,et al.  African geoxyles evolved in response to fire; frost came later , 2017, Evolutionary Ecology.

[5]  B. Lamont,et al.  Fire-Proneness as a Prerequisite for the Evolution of Fire-Adapted Traits. , 2017, Trends in plant science.

[6]  Isabelle Mougenot,et al.  Towards a thesaurus of plant characteristics: an ecological contribution , 2017 .

[7]  E. Laliberté Below-ground frontiers in trait-based plant ecology. , 2017, The New phytologist.

[8]  J. Pausas Bark thickness and fire regime : another twist AcommentonRosell ( , 2016 .

[9]  T. Herben,et al.  Disturbance is an important factor in the evolution and distribution of root-sprouting species , 2017, Evolutionary Ecology.

[10]  J. Manning,et al.  A Cretaceous origin for fire adaptations in the Cape flora , 2016, Scientific Reports.

[11]  B. Lamont,et al.  Pre-Gondwanan-breakup origin of Beauprea (Proteaceae) explains its historical presence in New Caledonia and New Zealand , 2016, Science Advances.

[12]  B. Lamont,et al.  A 350‐million‐year legacy of fire adaptation among conifers , 2016 .

[13]  Susana Paula,et al.  Towards understanding resprouting at the global scale. , 2016, The New phytologist.

[14]  J. Pausas,et al.  Lignotubers in Mediterranean basin plants , 2015, Plant Ecology.

[15]  J. Pausas Bark thickness and fire regime , 2015 .

[16]  H. Peter Linder,et al.  Do Mediterranean‐type ecosystems have a common history?—Insights from the Buckthorn family (Rhamnaceae) , 2015, Evolution; international journal of organic evolution.

[17]  W. Bond Fires in the Cenozoic: a late flowering of flammable ecosystems , 2015, Front. Plant Sci..

[18]  M. Crisp,et al.  Clock model makes a large difference to age estimates of long-stemmed clades with no internal calibration: a test using Australian grasstrees , 2014, BMC Evolutionary Biology.

[19]  L. Mommer,et al.  Going underground: root traits as drivers of ecosystem processes. , 2014, Trends in ecology & evolution.

[20]  R. Pennington,et al.  The remarkable congruence of New and Old World savanna origins. , 2014, The New phytologist.

[21]  Juli G Pausas,et al.  Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. , 2014, The New phytologist.

[22]  W. Bond,et al.  Savanna fire and the origins of the 'underground forests' of Africa. , 2014, The New phytologist.

[23]  B. Appezzato‐da‐Glória,et al.  Anatomy of vegetative organs in Aldama tenuifolia and A. kunthiana (Asteraceae: Heliantheae) , 2014, Brazilian Journal of Botany.

[24]  Richard D. Hayes,et al.  The genome of Eucalyptus grandis , 2014, Nature.

[25]  V. Pillar,et al.  Does disturbance affect bud bank size and belowground structures diversity in Brazilian subtropical grasslands , 2014 .

[26]  W. Jepson Regeneration in Manzanita , 2013 .

[27]  G. Burrows Buds, bushfires and resprouting in the eucalypts , 2013 .

[28]  A. A. Soares,et al.  Underground system of Mandevilla atroviolacea (Stadelm.) Woodson (Apocynaceae, Apocynoideae) from the Brazilian high-altitude grassland , 2013 .

[29]  B. Lamont,et al.  Adaptive responses to directional trait selection in the Miocene enabled Cape proteas to colonize the savanna grasslands , 2013, Evolutionary Ecology.

[30]  R. Alves,et al.  Longevity of the Brazilian underground tree Jacaranda decurrens Cham. , 2013, Anais da Academia Brasileira de Ciencias.

[31]  M. Lawes,et al.  Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. , 2013, The New phytologist.

[32]  B. Lamont,et al.  Low Rate of Between-Population Seed Dispersal Restricts Genetic Connectivity and Metapopulation Dynamics in a Clonal Shrub , 2012, PloS one.

[33]  R. Srivastava,et al.  Revision of Early Cretaceous angiosperm remains from the Rajmahal Basin, India, with notes on the palaeoecology of the Pentoxylon plant , 2012 .

[34]  R. Will,et al.  Factors affecting the sprouting of shortleaf pine rootstock following prescribed fire , 2012 .

[35]  H. S. Rai,et al.  Recent Synchronous Radiation of a Living Fossil , 2011, Science.

[36]  B. Lamont,et al.  Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa , 2011, Plant Ecology.

[37]  N. Enright,et al.  Ecology of fire-tolerant podocarps in temperate Australian forests , 2011 .

[38]  B. Lamont,et al.  Fitness and evolution of resprouters in relation to fire , 2011, Plant Ecology.

[39]  Juli G Pausas,et al.  Fire as an evolutionary pressure shaping plant traits. , 2011, Trends in plant science.

[40]  B. Appezzato‐da‐Glória,et al.  Morpho-anatomical features of underground systems in six Asteraceae species from the Brazilian Cerrado. , 2011, Anais da Academia Brasileira de Ciencias.

[41]  T. Taylor,et al.  Root suckering in a Triassic conifer from Antarctica: paleoecological and evolutionary implications. , 2011, American journal of botany.

[42]  Tianhua He,et al.  Banksia born to burn. , 2011, The New phytologist.

[43]  N. Pütz,et al.  Seed germination and seedling morphology of Smilax polyantha (Smilacaceae) , 2011 .

[44]  H. Linder,et al.  Estimating the age of fire in the Cape flora of South Africa from an orchid phylogeny , 2011, Proceedings of the Royal Society B: Biological Sciences.

[45]  W. Bond,et al.  Fire and the spread of flowering plants in the Cretaceous. , 2010, The New phytologist.

[46]  V. Pillar,et al.  Population biology and regeneration of forbs and shrubs after fire in Brazilian Campos grasslands , 2010, Plant Ecology.

[47]  R. Pennington,et al.  Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire , 2009, Proceedings of the National Academy of Sciences.

[48]  J. Keeley,et al.  A Burning Story: The Role of Fire in the History of Life , 2009 .

[49]  N. Thevs,et al.  Root suckering patterns in Populus euphratica (Euphrates poplar, Salicaceae) , 2009, Trees.

[50]  B. Appezzato‐da‐Glória,et al.  Resprouting from roots in four Brazilian tree species. , 2007, Revista de biologia tropical.

[51]  J. Fisher Anatomy of axis contraction in seedlings from a fire prone habitat. , 2008, American journal of botany.

[52]  Paul J. Constantino,et al.  Mechanical Properties of Plant Underground Storage Organs and Implications for Dietary Models of Early Hominins , 2008, Evolutionary Biology.

[53]  Peter Del Tredici,et al.  Sprouting in temperate trees: A morphological and ecological review , 2001, The Botanical Review.

[54]  S. James Lignotubers and burls— their structure, function and ecological significance in Mediterranean ecosystems , 1984, The Botanical Review.

[55]  V. Krassilov,et al.  Weedy Albian angiosperms , 2008 .

[56]  B. Appezzato‐da‐Glória,et al.  Underground systems of Asteraceae species from the Brazilian Cerrado1 , 2008 .

[57]  S. Machado,et al.  Morphological and developmental investigations of the underground system of Erythroxylum species from Brazilian cerrado , 2007 .

[58]  L. Klimeš,et al.  Bud banks and their role in vegetative regeneration – A literature review and proposal for simple classification and assessment , 2007 .

[59]  G. Overbeck,et al.  Adaptive strategies in burned subtropical grassland in southern Brazil , 2007 .

[60]  V. Lieffers,et al.  Effects of soil temperature and time of decapitation on sucker initiation of intact Populus tremuloides root systems , 2006 .

[61]  N. L. Menezes Rhizophores in Rhizophora mangle L: an alternative interpretation of so-called ''aerial roots''. , 2006, Anais da Academia Brasileira de Ciencias.

[62]  R. Cowling,et al.  An overview of the Cape geophytes , 2006 .

[63]  B. Appezzato‐da‐Glória,et al.  The origin and anatomy of rhizophores in Vernonia herbacea and V. platensis (Asteraceae) from the Brazilian Cerrado , 2005 .

[64]  T. Feild,et al.  Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils. , 2005, The New phytologist.

[65]  F. Ojeda,et al.  Evolutionary transition from resprouter to seeder life history in two Erica (Ericaceae) species: insights from seedling axillary buds. , 2005, Annals of botany.

[66]  D. Ackerly,et al.  Is there a cost to resprouting? Seedling growth rate and drought tolerance in sprouting and nonsprouting Ceanothus (Rhamnaceae). , 2005, American journal of botany.

[67]  Beatriz Appezzato-da-Gl The origin and anatomy of rhizophores in Vernonia herbacea and V. platensis (Asteraceae) from the Brazilian Cerrado , 2005 .

[68]  M. Westoby,et al.  Sprouting by semi‐arid plants: testing a dichotomy and predictive traits , 2004 .

[69]  H. Schneider,et al.  Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. , 2004, American journal of botany.

[70]  R. R. Rodrigues,et al.  Tree species sprouting from root buds in a semideciduous forest affected by fires , 2004 .

[71]  M. Spetich Upland oak ecology symposium: history, current conditions, and sustainability , 2004 .

[72]  D. V. Lear,et al.  Survival of Hardwood Regeneration During Prescribed Fires: The Importance of Root Development and Root Collar Location , 2004 .

[73]  L. Klimeš,et al.  Resprouting of herbs in disturbed habitats: is it adequately described by Bellingham–Sparrow's model? , 2003 .

[74]  O. Solbrig,et al.  The role of topkill in the differential response of savanna woody species to fire , 2003 .

[75]  S. Hopper,et al.  Monocotyledonous geophytes: comparison of south-western Australia with other areas of mediterranean climate , 2003 .

[76]  William J. Bond,et al.  The Evolutionary Ecology of Sprouting in Woody Plants , 2003, International Journal of Plant Sciences.

[77]  J. Pate,et al.  Quantifying above- and below-ground growth responses of the western Australian oil mallee, Eucalyptus kochii subsp. plenissima, to contrasting decapitation regimes. , 2002, Annals of botany.

[78]  F. Putz,et al.  Effect of disturbance intensity on regeneration mechanisms in a tropical dry forest , 2002 .

[79]  M. Molinas,et al.  Comparative anatomical analysis of the cotyledonary region in three Mediterranean Basin Quercus (Fagaceae). , 2002, American journal of botany.

[80]  R. R. Rodrigues,et al.  Anatomical studies of shoot bud-forming roots of Brazilian tree species , 2001 .

[81]  M. Sedgley,et al.  Early Lignotuber Formation in Banksia—Investigations into the Anatomy of the Cotyledonary Node of TwoBanksia (Proteaceae) Species , 2000 .

[82]  G. Retallack Carboniferous fossil plants and soils of an early tundra ecosystem , 1999 .

[83]  M. Sedgley,et al.  Lignotuber Bud Development in Eucalyptus cinerea (F. Muell. ex Benth) , 1998, International Journal of Plant Sciences.

[84]  N. Pütz Underground Plant Movement. V. Contractile Root Tubers and Their Importance to the Mobility of Hemerocallis fulva L. (Hemerocallidaceae) , 1998, International Journal of Plant Sciences.

[85]  M. Riba Effects of intensity and frequency of crown damage on resprouting of Erica arborea L. (Ericaceae) , 1998 .

[86]  F. Ewers,et al.  The mode of origin of root buds and root sprouts in the clonal tree Sassafras albidum (Lauraceae). , 1997, American journal of botany.

[87]  D. C. Rocha,et al.  O Sistema Subterrâneo de Dioscorea kunthiana Uline Ex R. Knuth (Dioscoreaceae) , 1997 .

[88]  A. Granström,et al.  Fire Severity and Vegetation Response in the Boreal Swedish Forest , 1996 .

[89]  T. Auld,et al.  Soil temperatures after the passage of a fire : Do they influence the germination of buried seeds ? , 1996 .

[90]  P. Lu,et al.  Rhizophore and Root Development in Selaginella martensii: Meristem Transitions and Identity , 1996, International Journal of Plant Sciences.

[91]  J. Arroyo,et al.  Postfire Regeneration of a Mediterranean Heathland in Southern Spain , 1996 .

[92]  M. C. Grant,et al.  Genetic variation and the natural history of quaking aspen , 1996 .

[93]  A. Markey,et al.  Biogeography of Fire-Killed and Resprouting Banksia Species in South-Western Australia , 1995 .

[94]  J. Keeley Smoke-induced flowering in the fire-lily Cyrtanthus ventricosus , 1993 .

[95]  J. Pate,et al.  The Significance of Root Starch in Post-fire Shoot Recovery of the Resprouter Stirlingia latifolia R. Br. (Proteaceae) , 1993 .

[96]  M. Molinas,et al.  Lignotuber ontogeny in the cork-oak (Quercus suber; Fagaceae). I. Late embryo , 1993 .

[97]  D. Maitre,et al.  Life Cycles and Fire-Stimulated Flowering in Geophytes , 1992 .

[98]  C. Lacey,et al.  Woody Clumps and Clumpwoods , 1990 .

[99]  B. Lamont Sexual Versus Vegetative Reproduction in Banksia elegans , 1988, Botanical Gazette.

[100]  George P. Malanson,et al.  Vigour of post-fire resprouting by Quercus coccifera L. , 1988 .

[101]  R. Barbour,et al.  Underground systems of gambel oak (Quercus gambelii) in central Utah , 1987 .

[102]  P. Rinne,et al.  Initiation, Structure and Sprouting of Dormant Basal Buds in Betula pubescens , 1987 .

[103]  D. Raynal,et al.  Spatial distribution and development of root sprouts in Fagus grandifolia (Fagaceae). , 1986 .

[104]  K. Niklas,et al.  Clonal growth in land plants: a paleobotanical perspective , 1985 .

[105]  I. Abbott,et al.  Growth Rate and Long-term Population Dynamics of Jarrah (Eucalyptus marginata Donn ex Sm.) Regeneration in Western Australian Forest , 1984 .

[106]  D. Stevenson Observations on root and stem contraction in cycads (Cycadales) with special reference to Zamia pumila L. , 1980 .

[107]  B. Lamont,et al.  THE LONGEVITY, FLOWERING AND FIRE HISTORY OF THE GRASSTREES XANTHORRHOEA PREISSH AND KINGIA AUSTRALIS , 1979 .

[108]  R. Wein,et al.  Depth of underground plant organs and theoretical survival during fire , 1977 .

[109]  J. Doyle Fossil Evidence on Early Evolution of the Monocotyledons , 1973, The Quarterly Review of Biology.

[110]  G. A. Schier,et al.  Role of Carbohydrate Reserves in the Development of Root Suckers in Populustremuloides , 1973 .

[111]  M. Chattaway Bud development and lignotuber formation in eucalypts , 1958 .

[112]  N. Beadle Soil temperatures during forest fires and their effect on the survival of vegetation. , 1940 .

[113]  D. Rietz,et al.  Life-forms of terrestrial flowering plants, 1 , 1931 .

[114]  T. Holm The application of the term "rhizome. " , 1929 .

[115]  J. Davy The Suffrutescent Habit as an Adaptation to Environment , 1922 .