Abstract
The presence of belowground organs with buds and carbohydrate storage is typical of perennial plants in fire-prone ecosystems. The bud-bearing storage organs allow regeneration after fire, and they may lose their regeneration capacity if the disturbance is excluded, because of the depletion in the bud bank. We assessed the morphology, anatomy, and storage of carbohydrates in the belowground organs of eight perennial species from open savannas and analyzed their bud banks at different fire frequencies (annual, biennial, and exclusion). Xylopodium was found in all the study species as bud-bearing organ, associated with proliferated storage parenchyma tissue, often in the tuberous roots. We found that bud bank size varied according to different fire frequencies for only half of the studied species (most forbs), and a tendency for lower bud bank sizes in fire-excluded areas was found for all shrub species. Our study highlights the significance of bud-bearing storage organs, particularly xylopodium, and that the species-specific responses of bud bank size to different fire frequencies underscore the need to consider individual plant strategies when analysing fire effects, emphasizing the critical role of belowground organs in sustaining these ecosystems.
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Data Availability
The dataset analysed during the current study is available in the Zenodo repository, https://zenodo.org/record/8373051. Bombo et al. 2023.
References
Ahmed MA, Kroener E, Holz M, et al (2014) Mucilage exudation facilitates root water uptake in dry soils. Functional Plant Biology 41:1129–1137. https://doi.org/10.1071/FP13330
Antonelli-Filho R (2011) Plano de Manejo da Reserva Natural Serra do Tombador, Cavalcante - Goiás. Curitiba, Fundação Grupo O Boticário de Proteção à Natureza. 217 p.
Appezzato-da-Glória B (2015) Morfologia de sistemas subterrâneos de plantas. 3i
Appezzato-da-Glória B, Curry G, Soares MKM, et al (2008) Underground Systems of Asteraceae Species from the Brazilian Cerrado. J Torrey Bot Soc 135:103–113
Appezzato-da-Glória B, Cury G (2011) Morpho-anatomical features of underground systems in six Asteraceae species from the Brazilian Cerrado. An Acad Bras Cienc 83:981–992. https://doi.org/10.1590/S0001-37652011005000018
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bewley JD (2002) Root storage proteins, with particular reference to taproots. Canadian Journal of Botany 80:321–329. https://doi.org/10.1139/b02-025
Bombo AB, De Oliveira TS, Da Silva Santos De Oliveira A, et al (2014) Anatomy and essential oil composition of the underground systems of three species of Aldama la Llave (Asteraceae). Journal of the Torrey Botanical Society 141:115–125.https://doi.org/10.3159/TORREY-D-12-00053.1
Bombo A, Siebert F, Fidelis A (2021) Fire and herbivory shape belowground bud banks in a semi-arid African savanna. African Journal of Range & Forage Science ISSN: 1–11. https://doi.org/10.2989/10220119.2021.1982004
Bombo AB, Appezzato-da-Glória B, Fidelis A (2022a) Fire exclusion changes belowground bud bank and bud-bearing organ composition jeopardizing open savanna resilience. Oecologia. https://doi.org/10.1007/S00442-022-05172-1
Bombo AB, Siebert F, Fidelis A (2022b) Fire and herbivory shape belowground bud banks in a semi-arid African savanna. Afr J Range Forage Sci 39:16–26. https://doi.org/10.2989/10220119.2021.1982004
Bond WJ (2019) Open Ecosystems, 1st edn. Oxford University Press
Bond WJ, Woodward FI, Midgley GF (2005) The global distribution of ecosystems in a world without fire. New Phytologist 165:525–538. https://doi.org/10.1111/j.1469-8137.2004.01252.x
Braga MR, Carpita NC, Dietrich SMC, Figueiredo-Ribeiro RDCL (2006) Changes in pectins of the Xylopodium of Ocimum nudicaule from dormancy to sprouting. Brazilian Journal of Plant Physiology 18:325–331. https://doi.org/10.1590/S1677-04202006000200009
Buisson E, Le Stradic S, Silveira FAO, et al (2019) Resilience and restoration of tropical and subtropical grasslands, savannas, and grassy woodlands. Biological Reviews 94:590–609. https://doi.org/10.1111/brv.12470
Bukatsch F (1972) Bemerkungen zur doppelfärbung Astrablau-Safranin. Microkosmos 61:255
Chapin FS, Schulze E, Mooney HA (1990) The Ecology and Economics of Storage in Plants. Annu Rev Ecol Syst 21:423–447. https://doi.org/10.1146/annurev.es.21.110190.002231
Chiminazzo MA, Bombo AB, Charles-Dominique T, Fidelis A (2021) Your best buds are worth protecting: Variation in bud protection in a fire-prone Cerrado system. Funct Ecol 35:2424–2434. https://doi.org/10.1111/1365-2435.13907/SUPPINFO
Clarke PJ, Lawes MJ, Midgley JJ, et al (2013) Resprouting as a key functional trait: How buds, protection and resources drive persistence after fire. New Phytologist 197:19–35. https://doi.org/10.1111/nph.12001
Daldegan GA, de Carvalho Júnior OA, Guimarães RF, et al (2014) Spatial patterns of fire recurrence using remote sensing and GIS in the Brazilian savanna: Serra do Tombador Nature Reserve, Brazil. Remote Sens (Basel) 6:9873–9894. https://doi.org/10.3390/rs6109873
Dalgleish HJ, Hartnett DC (2009) The effects of fire frequency and grazing on tallgrass prairie productivity and plant composition are mediated through bud bank demography. Plant Ecol 201:411–420. https://doi.org/10.1007/s11258-008-9562-3
Dalgleish HJ, Ott JP, Setshogo MP, Hartnett DC (2012) Inter-specific variation in bud banks and flowering effort among semi-arid African savanna grasses. South African Journal of Botany 83:127–133. https://doi.org/10.1016/J.SAJB.2012.08.010
Diaz-Toribio MH, Putz FE (2021) Underground carbohydrate stores and storage organs in fire-maintained longleaf pine savannas in Florida, USA. Am J Bot 108:432–442. https://doi.org/10.1002/ajb2.1620
Esau K (1953) Plant Anatomy, Wiley. John Wiley, New York
Faleiro R, da Silva GS, Pilon NAL, et al (2022) Attributes that ensure Cerrado shrub layer resilience after afforestation: The case of Psidium grandifolium. South African Journal of Botany 149:6–18. https://doi.org/10.1016/J.SAJB.2022.05.040
Ferraro A, da Silva GS, de Aguiar CL, Appezzato-da-Glória B (2021a) Evaluating belowground bud banks of native species from Cerrado: Structural, chemical, and ecological approaches. Flora 281:151852. https://doi.org/10.1016/J.FLORA.2021.151852
Ferraro A, da Silva GS, de Aguiar CL, Appezzato-da-Glória B (2021b) Evaluating belowground bud banks of native species from Cerrado: structural, chemical, and ecological approaches. Flora 151852. https://doi.org/10.1016/j.flora.2021.151852
Fidelis A, Appezzato-da-Glória B, Pillar VD, Pfadenhauer J (2014) Does disturbance affect bud bank size and belowground structures diversity in Brazilian subtropical grasslands? Flora 209:110–116. https://doi.org/10.1016/j.flora.2013.12.003
Fidelis A, Müller SC, Pillar VD, Pfadenhauer J (2010) Population biology and regeneration of forbs and shrubs after fire in Brazilian Campos grasslands. Plant Ecol 211:107–117. https://doi.org/10.1007/s11258-010-9776-z
Filartiga AL, Bombo AB, Garcia VL, Appezzato-da-Glória B (2017) Belowground organs of four Brazilian Aldama (Asteraceae) species: Morphoanatomical traits and essential oil profile. South African Journal of Botany 113. https://doi.org/10.1016/j.sajb.2017.08.008
Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Israel Journal of Botany 38:125–174. https://doi.org/10.1080/0021213X.1989.10677119
Hartnett DC, Setshogo MP, Dalgleish HJ (2006) Bud banks of perennial savanna grasses in Botswana. Afr J Ecol 44:256–263. https://doi.org/10.1111/j.1365-2028.2006.00646.x
Hiers QA, Treadwell ML, Dickinson MB, et al (2021) Grass bud responses to fire in a semiarid savanna system. Ecol Evol 11:6620–6633. https://doi.org/10.1002/ECE3.7516
Janeček Š, Bartušková A, Bartoš M, et al (2015) Effects of disturbance regime on carbohydrate reserves in meadow plants. AoB Plants 7:plv123. https://doi.org/10.1093/AOBPLA/PLV123
Jensen WA (1962) Botanical Histochemistry. Principles and practices. Freeman, San Francisco
Joaquim E deO., Silva TM, Figueiredo-Ribeiro R deC. L, et al (2018) Diversity of reserve carbohydrates in herbaceous species from Brazilian campo rupestre reveals similar functional traits to endure environmental stresses. Flora 238:201–209.https://doi.org/10.1016/J.FLORA.2017.01.001
Johansen DA (1940) Plant Microtechnique. McGraw-Hill Book Co., New York
Keeley JE, Pausas JG, Rundel PW, et al (2011) Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci 16:406–411. https://doi.org/10.1016/j.tplants.2011.04.002
Klimešová J, Klimeš L (2007) Bud banks and their role in vegetative regeneration - A literature review and proposal for simple classification and assessment. Perspect Plant Ecol Evol Syst 8:115–129. https://doi.org/10.1016/j.ppees.2006.10.002
Klimešová J, Martínková J, Ottaviani G (2018) Belowground plant functional ecology: Towards an integrated perspective. Funct Ecol 32:2115–2126. https://doi.org/10.1111/1365-2435.13145
Klimešová J, Martínková J, Pausas JG, et al (2019) Handbook of standardized protocols for collecting plant modularity traits. Perspect Plant Ecol Evol Syst 40:125485. https://doi.org/10.1016/j.ppees.2019.125485
Lenth R V. (2016) Least-Squares Means: The R Package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/JSS.V069.I01
Lopes-Mattos KLB, Azevedo AA, Soares AA, Meira RMSA (2013) Underground system of Mandevilla atroviolacea (Stadelm.) Woodson (Apocynaceae, Apocynoideae) from the Brazilian high-altitude grassland. S Afr J Bot 87: 27-33. https://doi.org/10.1016/j.sajb.2013.03.007
Lubbe FC, Klimeš A, Doležal J, et al (2021) Carbohydrate storage in herbs: the forgotten functional dimension of the plant economic spectrum. Ann Bot 127:813–825. https://doi.org/https://doi.org/10.1093/aob/mcab014
McManus JFA (1948) Histological and Histochemical Uses of Periodic Acid. Stain Technol 23:99–108. https://doi.org/10.3109/10520294809106232
Melo-De-Pinna GFA, Bruno Edson-Chaves ·, Menezes-E-Vasconcelos K, et al (2022) Underground system of geoxylic species of Homalolepis Turcz. (Simaroubaceae, Sapindales) from the Brazilian Cerrado. Brazilian Journal of Botany 2021 1–11.https://doi.org/10.1007/S40415-021-00761-5
Moraes M, Carvalho MAM de., Franco AC, et al (2016) Fire and Drought: soluble carbohydrate storage and survival mechanisms in herbaceous plants from the Cerrado. Bioscience 66:107–117. https://doi.org/10.1093/biosci/biv178
Nazari M, Riebeling S, Banfield CC, et al (2020) Mucilage Polysaccharide Composition and Exudation in Maize From Contrasting Climatic Regions. Front Plant Sci 11:1968. https://doi.org/10.3389/FPLS.2020.587610/BIBTEX
O’Brien TP, McCully ME (1981) The study ofplant structure principles and select methods. Blackwell Scientific Publications, Oxford
Ott JP, Klimešová J, Hartnett DC (2019) The ecology and significance of below-ground bud banks in plants. Ann Bot 123:1099–1118. https://doi.org/10.1093/aob/mcz051
Ottaviani G, Martínková J, Herben T, et al (2017) On Plant Modularity Traits: Functions and Challenges. Trends Plant Sci 22:648–651. https://doi.org/10.1016/j.tplants.2017.05.010
Palhares D, De Paula JE, Pereira LAR, Silveira CEDS (2007) Comparative Wood Anatomy of Stem, Root and Xylopodium of Brosimum Gaudichaudii (Moraceae). IAWA J 28:83–94. https://doi.org/10.1163/22941932-90001621
Pausas JG, Lamont BB, Paula S, et al (2018) Unearthing belowground bud banks in fire-prone ecosystems. New Phytologist 217:1435–1448. https://doi.org/10.1111/nph.14982
Pearse AGE (1985) Histochemistry: Theoretical and Applied, 4th Editio. Churchill Livingstone, Edinburgh, London, Melbourne and New York
Pilon NAL, Cava MGB, Hoffmann WA, et al (2021) The diversity of post‐fire regeneration strategies in the cerrado ground layer. Journal of Ecology 109:154–166. https://doi.org/10.1111/1365-2745.13456
Plavcová L, Hoch G, Morris H, et al (2016) The amount of parenchyma and living fibers affects storage of nonstructural carbohydrates in young stems and roots of temperate trees. Am J Bot 103:603–612. https://doi.org/10.3732/AJB.1500489
Qian J, Wang Z, Liu Z, Busso CA (2017) Belowground Bud Bank Responses to Grazing Intensity in the Inner-Mongolia Steppe, China. Land Degrad Dev 28:822–832. https://doi.org/10.1002/ldr.2300
R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org/. Accessed 10 Oct 2022.
Rasheed F, Markgren J, Hedenqvist M, Johansson E (2020) Modeling to Understand Plant Protein Structure-Function Relationships—Implications for Seed Storage Proteins. Molecules 2020, Vol 25, Page 873 25:873.https://doi.org/10.3390/MOLECULES25040873
Rawitscher FK, Rachid M (1946) Troncos subterrâneos de plantas brasileiras. An Acad Bras Cienc 18:261–280
Ribeiro JF, Walter BMT (2008) As principais Fitofisionomias do Bioma Cerrado. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: ecologia e flora. Embrapa.
Rizzini CT, Heringer EP (1961) Underground organs of plants from some southern Brazilian savannas, with special reference to the xylopodium. Phyton (B Aires) 17:105–124
Rodrigues CA, Fidelis A (2022) Should we burn the Cerrado? Effects of fire frequency on open savanna plant communities. Journal of Vegetation Science. https://doi.org/10.1111/JVS.13159
Rodrigues CA, Zirondi HL, Fidelis A (2021) Fire frequency affects fire behavior in open savannas of the Cerrado. For Ecol Manage 482:118850. https://doi.org/10.1016/j.foreco.2020.118850
Rossatto DR, da Silveira Lobo Sternberg L, Franco AC (2013) The partitioning of water uptake between growth forms in a Neotropical savanna: do herbs exploit a third water source niche? Plant Biol 15:84–92.https://doi.org/10.1111/J.1438-8677.2012.00618.X
Silva BHP, Rossatto DR (2019) Are underground organs able to store water and nutrients? A study case in non-arboreal species from the Brazilian Cerrado. Theor Exp Plant Physiol 1–9. https://doi.org/10.1007/s40626-019-00155-9
Silva GS, Ferraro A, Lima de Aguiar C, Appezzato-da-Glória B (2021) Resprouting strategies of three native shrub Cerrado species from a morphoanatomical and chemical perspective. Aust J Bot. https://doi.org/10.1071/bt21039
Simon MF, Pennington T (2012) Evidence for Adaptation to Fire Regimes in the Tropical Savannas of the Brazilian Cerrado. Int J Plant Sci 173:711–723. https://doi.org/10.1086/665973
Strasburger E (1913) Handbook os pratical botany. George Allen & Company Ltda, London
Tripathi YC, Rathore M (2001) Role of Lipids in Natural Defense and Plant Protection. Indian Journal of Forestry 24:448–455
Voragen AGJ, Coenen GJ, Verhoef RP, Schols HA (2009) Pectin, a versatile polysaccharide present in plant cell walls. Struct Chem 20:263–275. https://doi.org/10.1007/S11224-009-9442-Z/TABLES/1
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis, 2nd edn. Springer-Verlag New York, Texas
Zdunek A, Pieczywek PM, Cybulska J (2021) The primary, secondary, and structures of higher levels of pectin polysaccharides. Compr Rev Food Sci Food Saf 20:1101–1117. https://doi.org/10.1111/1541-4337.12689
Zirondi H, Ooi MKJ, Fidelis A (2021) Fire-triggered flowering is the dominant post-fire strategy in a tropical savanna. Journal of Vegetation Science 32:e12995. https://doi.org/10.1111/JVS.12995
Zupo T, Daibes LF, Pausas JG, Fidelis A (2021) Post‐fire regeneration strategies in a frequently burned Cerrado community. Journal of Vegetation Science 32:jvs.12968. https://doi.org/10.1111/jvs.12968
Zuur AF, Ieno EN, Walker NJ, et al (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New York
Acknowledgments
The authors thank the staff of the Reserva Natural Serra do Tombador for their support during the fieldwork. We also thank Vagner Zanzarini, Gabriela Damasceno, and Nubia Vilela for their help digging the plants. This work was funded by the National Council for Scientific and Technological Development (CNPq, 406505/2018-7), São Paulo Research Foundation (FAPESP 2015/06743-0), National Geographic Society (NGS-51903C-18), and National Centre for Scientific Research (CNRS PICS 2018-2020 RESIGRASS] for financial support. ABB received postdoctoral support via a grant from the São Paulo Research Foundation (2017/02934-1), and AF and BAG received productivity grants from the National Council for Scientific and Technological Development (312689/2021-7 and 311721/2018-4, respectively).
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Aline Bombo and Alessandra Fidelis contributed to the study's conception and design. Raquel Martins and Aline Bombo collected and analyzed the data. Aline Bombo and Alessandra Fidelis wrote the first draft of the manuscript, and Beatriz Appezzato-da-Glória commented on previous versions. Aline Bombo and Alessandra Fidelis revised the manuscript and prepared the updated version. All authors have read and approved the final manuscript.
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Bombo, A.B., Appezzato-da-Glória, B., Martins, R. et al. Belowground organs and bud bank: Insights on morphoanatomical functional traits related to fire. Folia Geobot 58, 259–273 (2024). https://doi.org/10.1007/s12224-023-09437-2
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DOI: https://doi.org/10.1007/s12224-023-09437-2