Abstract
Aims
Banksia attenuata is a resprouting species growing in deep sand, while B. sessilis is a fire-killed species occurring in shallow sand over laterite or limestone. We aimed to discover the ecophysiological basis for their different distributions by exploring their investment in deep non-cluster roots and shallow cluster roots, and their cluster-root functioning.
Methods
Deep-pot (1 m), shallow-pot (400 mm), hydroponic experiments and phosphorus (P)-extraction experiment were carried out. Biomass allocation, cluster-root exudation, plant P and leaf manganese (Mn) concentrations were measured.
Results
Banksia attenuata allocated more biomass to deep roots and less biomass to cluster roots than B. sessilis did in deep pots. The two Banksias released similar carboxylates in all experiments, with similar carboxylate-exudation rates in hydroponics. The carboxylate amount per unit cluster root of B. sessilis grown in shallow pots was greater than that of B. attenuata, and B, sessilis acquired more P than B. attenuata did in limestone substrate.
Conclusions
Greater investment in deep roots for water uptake accounts for the presence of B. attenuata in deep sand, and vice versa for the absence of B. sessilis. A larger investment in cluster roots, which released greater amounts of carboxylates, likely accounts for B. sessilis occurring over limestone. Trade-offs in investment and cluster-root functioning support the species’ distribution patterns and life histories. Leaf Mn concentration was a good proxy for the plant capacity to acquire P.
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References
Bell DT (2001) Ecological response syndromes in the flora of southwestern Western Australia: fire resprouters versus reseeders. Bot Rev 67:417–440
Bowen BJ, Pate JS (2017) Patterns of storage tissue and starch distribution in the young taproot of obligate seeders and resprouters of Australian Proteaceae (Juss.): possible evidence of homoplastic evolution. Austral Ecol 42:617–629
Buri A, Cianfrani C, Pinto-Figueroa E, Yashiro E, Spangenberg JE, Adatte T, Verrecchia E, Guisan A, Pradervand J-N (2017) Soil factors improve predictions of plant species distribution in a mountain environment. Prog Phys Geog 41:703–722
Canham CA, Froend RH (2015) Rapid root elongation by phreatophyte seedlings does not imply tolerance of water table decline. Trees 29:815–824
Causley CL, Fowler WM, Lamont BB, He T (2016) Fitness benefits of serotiny in fire- and drought-prone environments. Plant Ecol 217:773–779
Cawthray GR (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J Chromatogr 1011:233–240
Clark DB, Clark DA, Read JM (1998) Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. J Ecol 86:101–112
Clark DB, Palmer MW, Clark DA (1999) Edaphic factors and the landscape-scale distributions of tropical rain forest trees. Ecology 80:2662–2675
Clarke PJ, Knox KJE (2009) Trade-offs in resource allocation that favour resprouting affect the competitive ability of woody seedlings in grassy communities. J Ecol 97:1374–1382
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 Phytol 197:19–35
Delgado M, Suriyagoda L, Zúñiga-Feest A, Borie F, Lambers H (2014) Divergent functioning of Proteaceae species: the south American Embothrium coccineum displays a combination of adaptive traits to survive in high-phosphorus soils. Funct Ecol 28:1356–1366
Denton MD, Veneklaas EJ, Lambers H (2007) Does phenotypic plasticity in carboxylate exudation differ among rare and widespread Banksia species (Proteaceae)? New Phytol 173:592–599
Frazer JM, Davis SD (1988) Differential survival of chaparral seedlings during the first summer drought after wildfire. Oecologia 76:215–221
Gardner WK, Boundy KA (1983) The acquisition of phosphorus by Lupinus albus L. IV. The effect of interplanting wheat and white lupin on the growth and mineral composition of the two species. Plant Soil 70:391–402
Groom PK, Lamont BB (2011) Regional and local effects on reproductive allocation in epicormic and lignotuberous populations of Banksia menziesii. Plant Ecol 212:2003–2011
Hansen A, Pate JS, Hansen AP (1991) Growth and reproductive performance of a seeder and a resprouter species of Bossiaea as a function of plant age after fire. Ann Bot 67:497–509
Hayes PE, Guilherme Pereira C, Clode PL, Lambers H (2019) Calcium-enhanced phosphorus toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence. New Phytol 221:764–777
Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86
Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44
Kidd DR, Ryan MH, Hahne D, Haling RE, Lambers H, Sandral GA, Simpson RJ, Cawthray GR (2018) The carboxylate composition of rhizosheath and root exudates from twelve species of grassland and crop legumes with special reference to the occurrence of citramalate. Plant Soil 424:389–403
Knox KJE, Clarke PJ (2005) Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs. Funct Ecol 19:690–698
Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martínez-Ferri E (2002) The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant Soil 238:111–122
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713
Lambers H, Finnegan PM, Laliberté E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156:1058–1066
Lambers H, Clode PL, Hawkins H-J, Laliberté E, Oliveira RS, Reddell P, Shane MW, Stitt M, Weston P (2015) Metabolic adaptations of the non-mycotrophic Proteaceae to soil with a low phosphorus availability. In: Plaxton WC, Lambers H eds. Annual Plant Reviews, Volume 48, Phosphorus Metabolism in Plants. Chicester: John Wiley & Sons, 289–366
Lambers H, Albornoz F, Kotula L, Laliberté E, Ranathunge K, Teste FP, Zemunik G (2018) How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil 424:11–34
Lamont BB, Connell SW (1996) Biogeography of Banksia in southwestern Australia. J Biogeogr 23:295–309
Lamont BB, Markey A (1995) Biogeography of fire-killed and resprouting Banksia species in South-Western Australia. Aust J Bot 43:283–303
Markesteijn L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. J Ecol 97:311–325
Motomizu S, Wakimoto T, Toei K (1983) Spectrophotometric determination of phosphate in river waters with molybdate blue and malachite green. Analyst 108:361–367
Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KHM (2018) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529
Pate JS, Bell TL (1999) Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia. Agrofor Syst 45:303–341
Pate JS, Froend RH, Bowen BJ, Hansen A, Kuo J (1990) Seedling growth and storage characteristics of seeder and resprouter species of Mediterranean-type ecosystems of S.W. Australia. Ann Bot 65:585–601
Pate J, Meney K, Dixon K (1991) Contrasting growth and morphological characteristics of fire-sensitive (obligate seeder) and fire-resistant (resprouter) species of Restionaceae (S hemisphere restiads) from South-Western Western-Australia. Aust J Bot 39:505–525
Paula S, Pausas JG (2011) Root traits explain different foraging strategies between resprouting life histories. Oecologia 165:321–331
Pausas JG, Keeley JE (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytol 204:55–65
Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MD, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species’ ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173:181–190
Poot P, Lambers H (2003) Are trade-offs in allocation pattern and root morphology related to species abundance? A congeneric comparison between rare and common species in the south-western Australian flora. J Ecol 91:58–67
Poot P, Lambers H (2008) Shallow-soil endemics: adaptive advantages and constraints of a specialized root-system morphology. New Phytol 178:371–381
Power SC, Cramer MD, Verboom GA, Chimphango SBM (2011) Legume seeders of the cape floristic region inhabit more fertile soils than congeneric resprouters—sometimes. Plant Ecol 212:1979–1989
Rellán-Álvarez R, Lobet G, Dinneny JR (2016) Environmental control of root system biology. Annu Rev Plant Biol 67:619–642
Richards MB, Groom PL, Lamont BB (1997) A trade-off between fecundity and drought susceptibility in adults and seedlings of Hakea species as influenced by leaf morphology. Aust J Bot 45:301–309
Shane MW, Lambers H (2005) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–450
Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135:549–560
Ström L, Olsson T, Tyler G (1994) Differences between calcifuge and acidifuge plants in root exudation of low-molecular organic acids. Plant Soil 167:239–245
Sultan SE (1995) Phenotypic plasticity and plant adaptation. Plant Biol 44:363–383
Suriyagoda LD, Lambers H, Renton M, Ryan MH (2012) Growth, carboxylate exudates and nutrient dynamics in three herbaceous perennial plant species under low, moderate and high phosphorus supply. Plant Soil 358:105–117
Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197
Witkowski ETF, Lamont BB (1996) Disproportionate allocation of mineral nutrients and carbon between vegetative and reproductive structures in Banksia hookeriana. Oecologia 105:38–42
Acknowledgements
We thank Caio Guilherme Pereira, Kenny Png, Kelsie Lambert, Azrul Azmi and Li Yan for help with plant harvesting and sample processing, Jiayin Pang, Wenli Ding, Patrick E. Hayes, Hongtao Zhong, Daniel Beeck for helpful advice on the experiments, and Rob Creasy and Bill Piasini for help with maintaining the plants in the glasshouse. We are grateful to Greg Cawthray for help with HPLC analyses, to Elizabeth Halladin for help with plant digestion, and to Michael Smirk for help with ICP-OES. Dr. Jianmin Shi was supported by the China Scholarship Council.
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Shi, J., Strack, D., Albornoz, F.E. et al. Differences in investment and functioning of cluster roots account for different distributions of Banksia attenuata and B. sessilis, with contrasting life history. Plant Soil 447, 85–98 (2020). https://doi.org/10.1007/s11104-019-03982-6
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DOI: https://doi.org/10.1007/s11104-019-03982-6