Plant Ecology

, Volume 217, Issue 6, pp 661–676 | Cite as

Lignotubers in Mediterranean basin plants

  • Susana Paula
  • Paulette I. Naulin
  • Cristian Arce
  • Consttanza Galaz
  • Juli G. Pausas
Article

Abstract

Lignotubers are swollen woody structures located at the root-shoot transition zone and contain numerous dormant buds and starch reserves. This structure enables the plant to resprout prolifically after severe disturbances that remove the aboveground biomass. These are considered adaptive traits in ecosystems with highly frequent and severe disturbances—such as fire-prone ecosystems. In this paper, we aim to contribute to the knowledge of lignotubers in the Mediterranean basin and highlight the evolutionary implications. We first summarise existing knowledge on lignotuber species in the Mediterranean basin. We then provide a detailed morpho-anatomical description of early lignotubers in two common woody species (Arbutus unedo L. and Phillyrea angustifolia L.). Finally, we compare our anatomical results with those obtained in studies conducted with other lignotuberous species from different Mediterranean regions. Lignotubers were verified in 14 species in the Mediterranean basin; all being from lineages with origins dating to the Tertiary and thus pre-dating the Mediterranean climate. In A. unedo and P. angustifolia, lignotubers are macroscopically discernible in 4- and 2-year-old saplings, respectively. In these two species, the lignotubers have numerous buds protected by hypertrophied scales, and have a contorted xylem containing abundant starch. Our results challenge the traditional idea that pre-Mediterranean lineages suffered evolutionary inertia; instead, lignotuberous species may be considered examples of plants that adapted to the increased fire activity that occurred throughout the Tertiary and Quaternary. We also highlight the use of morpho-anatomical traits to unambiguously distinguish between lignotuberous and non-lignotuberous resprouting species.

Keywords

Morpho-anatomy Bud bank Fire adaptations Fire regime Resprouting Tertiary Madrean–Tethyan vegetation 

Supplementary material

11258_2015_538_MOESM1_ESM.pdf (9.5 mb)
Supplementary material 1 (PDF 9687 kb)

References

  1. Axelrod DI (1975) Evolution and biogeography of Madrean-Tethyan sclerophyll vegetation. Ann Mo Bot Gard 62:280–334CrossRefGoogle Scholar
  2. Bamber RK, Mullette KJ (1978) Studies of lignotubers of Eucalyptus gummifera (Gaertn. and Hochr.). II anatomy. Aust J Bot 26:15–22CrossRefGoogle Scholar
  3. Bellingham PJ, Sparrow AD (2000) Resprouting as a life history strategy in woody plant communities. Oikos 89:409–416CrossRefGoogle Scholar
  4. Bernays EA, Cooper-Driver GA, Bilgener M (1989) Herbivores and plant tannins. In: Begon M, Fitter AH, Ford ED, MacFadyen A (eds) Advances in ecological research, vol 19. Academic Press Ltd, London, pp 263–302Google Scholar
  5. Burrows GE, Chisnall LK (2015) Buds buried in bark: the reason why Quercus suber (cork oak) is an excellent post-fire epicormic resprouter. Trees 1–14Google Scholar
  6. Burrows N, Wardell-Johnson G (2003) Fire and plant interactions in forested ecosystems of south-west Western Australia. In: Abbott I, Burrows N (eds) Fire in ecosystems of south-west Western Australia: impacts and management. Backhuys Publishers, Leiden, pp 225–268Google Scholar
  7. Canadell J, López-Soria L (1998) Lignotuber reserves support regrowth following clipping of two mediterranean shrubs. Funct Ecol 12:31–38CrossRefGoogle Scholar
  8. Canadell J, Zedler PH (1995) Underground structures of woody plants in Mediterranean Ecosystems of Australia, California, and Chile. In: Arroyo MTK, Zedler PH, Fox MD (eds) Ecology and biogeography of Mediterranean ecosystems in Chile, California, and Australia. Springer, New York, pp 177–210CrossRefGoogle Scholar
  9. Canadell J, Lloret F, López-Soria L (1991) Resprouting vigour of two Mediterranean shrub species after experimental fire treatments. Vegetatio 95:119–126Google Scholar
  10. Carr DJ, Jahnke R, Carr SGM (1983) Development of the lignotuber and plant form in Lehmannianae. Aust J Bot 31:629–643CrossRefGoogle Scholar
  11. Carrodus BB, Blake TJ (1970) Studies on lignotubers of Eucalyptus obliqua L’Heri. I. Nature of lignotuber. New Phytol 69:1069–1072CrossRefGoogle Scholar
  12. Catry F, Rego F, Moreira F, Fernandes P, Pausas JG (2010) Post-fire tree mortality in mixed forests of central Portugal. For Ecol Manage 260:1184–1192CrossRefGoogle Scholar
  13. Charco J (1999) El bosque mediterráneo en el norte de África. Agencia Española de Cooperación Internacional, MadridGoogle Scholar
  14. Chattaway MM (1958) Bud development and lignotuber formation in eucalypts. Aust J Bot 6:103–115CrossRefGoogle Scholar
  15. Clarke PJ, Lawes M, Midgley J, Lamont B, Ojeda F, Burrows G, Enright N, Knox K (2013) Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytol 197:19–35CrossRefPubMedGoogle Scholar
  16. Çolak AH, Rotherham ID, Spethmann W (2009) The Importance of lignotubers in arid-zone and humid-zone ecosystems with particular reference to Rhododendron ponticum L. Arboric J 32:67–82CrossRefGoogle Scholar
  17. Cruz A, Pérez B, Moreno JM (2003) Resprouting of the mediterranean-type shrub Erica australis with modified lignotuber carbohydrate content. J Ecol 91:348–356CrossRefGoogle Scholar
  18. Del Tredici P (1999) Redwood burls: immortality underground. Arnoldia 59:14–22Google Scholar
  19. Field J, Lettinga G (1992) Toxicity of tannic compounds to microorganisms. In: Hemingway RW, Laks PE (eds) Plant polyphenols. Synthesis, properties, significance. Plenum Press, New York, pp 673–692Google Scholar
  20. Graham AW, Wallwork M, Sedgley M (1998) Lignotuber bud development in Eucalyptus cinerea (F. Muell. ex Benth). Int J Plant Sci 159:979–988CrossRefGoogle Scholar
  21. Herrera CM (1992) Historical effects and sorting processes as explanations for contemporary ecological patterns—character syndromes in Mediterranean woody-plants. Am Nat 140:421–446CrossRefGoogle Scholar
  22. James S (1984) Lignotubers and burls—their structure, function and ecological significance in mediterranean ecosystems. Bot Rev 50:225–266CrossRefGoogle Scholar
  23. Johansen D (1940) Plant microtechnique. McGraw-Hill, New YorkGoogle Scholar
  24. Keeley JE (2012) Fire in Mediterranean climate ecosystems—a comparative overview. Israel J Ecol Evol 58:123–135Google Scholar
  25. Keeley JE, Pausas JG, Rundel PW, Bond WJ, Bradstock RA (2011) Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci 16:406–411CrossRefPubMedGoogle Scholar
  26. Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2012) Fire in mediterranean ecosystems: ecology, evolution and management. Cambridge University Press, CambridgeGoogle Scholar
  27. Kerr LR (1925) The lignotubers of eucalypt seedlings. Proceedings of the Royal Society of Victoria 37Google Scholar
  28. Knox KJ, Clarke PJ (2004) Fire response syndromes of shrubs in grassy woodlands in the New England Tableland Bioregion. Cunninghamia 8:348–353Google Scholar
  29. Kummerow J (1989) Structural aspects of shrubs in Mediterranean-type plant communities. Optiòns Méditerranéennes 3:5–11Google Scholar
  30. Ladd PG, Crosti R, Pignatti S (2005) Vegetative and seedling regeneration after fire in planted Sardinian pinewood compared with that in other areas of Mediterranean-type climate. J Biogeogr 32:85–98CrossRefGoogle Scholar
  31. Lloret F, López-Soria L (1993) Resprouting of Erica multiflora after experimental fire treatments. J Veg Sci 4:367–374CrossRefGoogle Scholar
  32. Lloret F, Verdú M, Flores-Hernández N, Valiente-Banuet A (1999) Fire and resprouting in Mediterranean ecosystems: insights from an external biogeographical region, the mexical shrubland. Am J Bot 86:1655–1661CrossRefPubMedGoogle Scholar
  33. Mibus R, Sedgley M (2000) Early lignotuber formation in Banksia—Investigations into the anatomy of the cotyledonary node of two Banksia (Proteaceae) species. Ann Bot 86:575–587CrossRefGoogle Scholar
  34. Molinas ML, Verdaguer D (1993a) Lignotuber ontogeny in the cork oak (Quercus suber, Fagaceae). 2. Germination and young seedling. Am J Bot 80:182–191CrossRefGoogle Scholar
  35. Molinas ML, Verdaguer D (1993b) Lignotuber ontogeny in the cork oak (Quercus suber, Fagaceae). 1. Late embryo. Am J Bot 80:172–181CrossRefGoogle Scholar
  36. Montenegro G, Avila G, Schatte P (1983) Presence and development of lignotubers in shrubs of the Chilean matorral. Can J Bot 61:1804–1808CrossRefGoogle Scholar
  37. Montenegro G, Gómez M, Díaz F, Ginocchio R (2003) Regeneration potential of Chilean matorral after fire: an updated view. In: Veblen TT, Baker WL, Montenegro G, Swetnam TW (eds) Fire and climatic change in temperate ecosystems of the Western Americas. Springer, New York, pp 375–403Google Scholar
  38. Mullette K, Bamber R (1978) Studies of the lignotubers of Eucalyptus gummifera (Gaertn. and Hochr.). III. Inheritance and chemical composition. Aust J Bot 26:23–28CrossRefGoogle Scholar
  39. Nitta I, Ohsawa M (1998) Bud structure and shoot architecture of canopy and understorey evergreen broad-leaved trees at their northern limit in East Asia. Ann Bot 81:115–129CrossRefGoogle Scholar
  40. Pascual G, Molinas M, Verdaguer D (2002) Comparative anatomical analysis of the cotyledonary region in three Mediterranean Basin Quercus (Fagaceae). Am J Bot 89:383–392CrossRefPubMedGoogle Scholar
  41. Paula S, Ojeda F (2006) Resistance of three co-occurring resprouter Erica species to highly frequent disturbance. Plant Ecol 183:329–336CrossRefGoogle Scholar
  42. Paula S, Ojeda F (2009) Belowground starch consumption after recurrent severe disturbance in three resprouter species of the genus Erica. Botany 87:253–259CrossRefGoogle Scholar
  43. Paula S., Pausas JG (2013) BROT: a plant trait database for Mediterranean Basin species. Version 2013.06. http://www.uv.es/jgpausas/brot.htm
  44. 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 90:1420CrossRefGoogle Scholar
  45. Pausas JG (1997) Resprouting of Quercus suber in NE. Spain after fire. J Veg Sci 8:703–706CrossRefGoogle Scholar
  46. Pausas JG (2015) Bark thickness and fire regime. Funct Ecol 29:317–327CrossRefGoogle Scholar
  47. Pausas JG, Keeley JE (2014) Evolutionary ecology of resprouting and seeding in fireprone ecosystems. New Phytol 204:55–65CrossRefPubMedGoogle Scholar
  48. Pausas JG, Verdú M (2005) Plant persistence traits in fire-prone ecosystems of the Mediterranean basin: a phylogenetic approach. Oikos 109:196–202CrossRefGoogle Scholar
  49. Pausas JG, Pratt RB, Keeley JE, Jacobsen AL, Ramirez AR, Vilagrosa A, Paula S, Kanekua-Pia IN, Davis SD (2015) Towards understanding resprouting at the global scale. New Phytol. doi:10.1111/nph.13644 PubMedGoogle Scholar
  50. Pryor L, Byrne O (1969) Variation and taxonomy in Eucalyptus camaldulensis. Silvae Genetica 18:64–71Google Scholar
  51. Quevedo L, Rodrigo A, Espelta JM (2007) Post-fire resprouting ability of 15 non-dominant shrub and tree species in Mediterranean areas of NE Spain. Ann Forest Sci 64:883–890CrossRefGoogle Scholar
  52. Rundel PW, Baker GA, Parsons DJ, Stohlgren TJ (1987) Postfire demography of resprouting and seedling establishment by Adenostoma fasciculatum in the California chaparral. In: Tenhunen JD, Catarino FM, Lange OL, Oechel WC (eds) Plant response to stress. Springer, Berlin, pp 575–596CrossRefGoogle Scholar
  53. Sealy JR (1949a) Arbutus unedo. J Ecol 37:365–388CrossRefGoogle Scholar
  54. Sealy JR (1949b) The swollen stem-base in Arbutus unedo. Kew Bull 4:241–251Google Scholar
  55. Shepherd M, Kasem S, Lee DJ, Henry R (2008) Mapping species differences for adventitious rooting in a Corymbia torelliana × Corymbia citriodora subspecies variegata hybrid. Tree Genet Genomes 4:715–725CrossRefGoogle Scholar
  56. Silva JS, Rego FC, Martins-Loução MA (2002) Belowground traits of mediterranean woody plants in a portuguese shrubland. Ecol Mediter 28:5–13Google Scholar
  57. Valdés B, Talavera S, Galiano EF (1987) Flora Vascular de Andalucía Occidental. Ketres, BarcelonaGoogle Scholar
  58. Valiente-Banuet A, Rumebe AV, Verdú M, Callaway RM (2006) Modern quaternary plant lineages promote diversity through facilitation of ancient tertiary lineages. Proc Natl Acad Sci USA 103:16812–16817CrossRefPubMedPubMedCentralGoogle Scholar
  59. Van Groenendael J, Klimes L, Klimesova J, Hendriks R (1996) Comparative ecology of clonal plants. Philos Trans Royal Soc London B 351:1331–1339CrossRefGoogle Scholar
  60. Verdaguer D, Ojeda F (2005) Evolutionary transition from resprouter to seeder life history in two Erica (Ericaceae) species: insights from seedling axillary buds. Ann Bot 95:593–599CrossRefPubMedPubMedCentralGoogle Scholar
  61. Verdaguer D, García-Berthou E, Pascual G, Puigderrajols P (2001) Sprouting of seedlings of three Quercus species in relation to repeated pruning and the cotyledonary node. Aust J Bot 49:67–74CrossRefGoogle Scholar
  62. Verdú M, Pausas JG (2013) Syndrome-driven diversification in a Mediterranean ecosystem. Evolution 67:1756–1766CrossRefPubMedGoogle Scholar
  63. Vesk PA, Westoby M (2004a) Sprouting ability across diverse disturbances and vegetation types worldwide. J Ecol 92:310–320CrossRefGoogle Scholar
  64. Vesk PA, Westoby M (2004b) Funding the bud bank: a review of the costs of buds. Oikos 106:200–208CrossRefGoogle Scholar
  65. 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. Ann Bot 90:185–197CrossRefPubMedPubMedCentralGoogle Scholar
  66. Zammit C (1988) Dynamics of resprouting in the lignotuberous shrub Banksia oblongifolia. Austral Ecol 13:311–320CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Instituto de Ciencias Ambientales y EvolutivasUniversidad Austral de ChileValdiviaChile
  2. 2.Laboratorio de Biología de Plantas, Departamento de Silvicultura y Conservación de la NaturalezaUniversidad de ChileSantiagoChile
  3. 3.CIDE-CSICMontcadaSpain

Personalised recommendations