Abstract
Background and aims
Root-released carboxylates enhance the availability of manganese (Mn), which enters roots through transporters with low substrate specificity. Leaf Mn concentration ([Mn]) has been proposed as a signature for phosphorus (P)-mobilising carboxylates in the rhizosphere. Here we test whether leaf [Mn] provides a signature for root functional types related to P acquisition.
Methods
Across 727 species at 66 sites in Australia and New Zealand, we measured leaf [Mn] as related to root functional type, while also considering soil and climate variables. To further assess the specific situations under which leaf [Mn] is a suitable proxy for rhizosphere carboxylate concentration, we studied leaf [Mn] along a strong gradient in water availability on one representative site. In addition, we focused on two systems where a species produced unexpected results.
Results
Controlling for background site-specific variation in leaf [Mn] with soil pH and mean annual precipitation, we established that mycorrhizal species have significantly lower leaf [Mn] than non-mycorrhizal species with carboxylate-releasing root structures, e.g., cluster roots. In exception to the general tendency, leaf [Mn] did not provide information about root functional types under seasonally waterlogged conditions, which increase iron availability and thereby interfere with Mn-uptake capacity. Two further exceptions were scrutinised, leading to the conclusion that they were ‘anomalous’ in not functioning like typical species in their families, as expected according to the literature.
Conclusions
Leaf [Mn] variation provides considerable insights on differences in belowground functioning among co-occurring species. Using this approach, we concluded that, within typical mycorrhizal families, some species actually depend on a carboxylate-releasing P-mobilising strategy. Likewise, within families that are known to produce carboxylate-releasing cluster roots, some do not produce functional cluster roots when mature. An analysis of leaf [Mn] can alert us to such ‘anomalous’ species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated and analysed during this study will be available in the AEKOS data repository (http://aekos.org.au/home).
References
Abrahão A, Ryan MH, Laliberté E, Oliveira RS, Lambers H (2018) Phosphorus- and nitrogen-acquisition strategies in two Bossiaea species (Fabaceae) along retrogressive soil chronosequences in South-Western Australia. Physiol Plant 163:323–343. https://doi.org/10.1111/ppl.12704
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
Baxter IR, Vitek O, Lahner B, Muthukumar B, Borghi M, Morrissey J, Guerinot ML, Salt DE (2008) The leaf ionome as a multivariable system to detect a plant's physiological status. Proc Natl Acad Sci U S A 105:12081–12086. https://doi.org/10.1073/pnas.0804175105
Beadle NCW (1953) The edaphic factor in plant ecology with a special note on soil phosphates. Ecology 34:426–428. https://doi.org/10.2307/1930910
Bethlenfalvay GJ, Franson RL (1989) Manganese toxicity alleviated by mycorrhizae in soybean. J Plant Nutr 12:953–970. https://doi.org/10.1080/01904168909364006
Bouwens L, Longin J (1979) Le du manganèse foliaire dans les strates herbacées en rapport avec l'écophysiologie des plantes calcicoles et calcifuges. Bull SocR Bot Belg / Bull Koninkl Belg Bot Ver 112:243–251
Bowen BJ, Pate JS (1993) The significance of root starch in post-fire shoot recovery of the resprouter Stirlingia latifolia R. Br. (Proteaceae). Ann Bot 72:7–16. https://doi.org/10.1006/anbo.1993.1075
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. https://doi.org/10.1007/s11104-008-9877-9
Brundrett MC (2017) Global diversity and importance of mycorrhizal and nonmycorrhizal plants. In: Tedersoo L (ed) Biogeography of Mycorrhizal Symbiosis. Springer International Publishing, Cham, pp 533–556. https://doi.org/10.1007/978-3-319-56363-3_21
Brundrett MC, Abbott LK (1991) Roots of jarrah forest plants. I. Mycorrhizal associations of shrubs and herbaceous plants. Aust J Bot 39:445–457. https://doi.org/10.1071/BT9910445
Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976
Canton GC, Bertolazi AA, Cogo AJD, Eutrópio FJ, Melo J, de Souza SB, A. Krohling C, Campostrini E, da Silva AG, Façanha AR, Sepúlveda N, Cruz C, Ramos AC (2016) Biochemical and ecophysiological responses to manganese stress by ectomycorrhizal fungus Pisolithus tinctorius and in association with Eucalyptus grandis. Mycorrhiza 26:475–487. https://doi.org/10.1007/s00572-016-0686-3
Cawthray GR (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J Chromotog A 1011:233–240. https://doi.org/10.1016/S0021-9673(03)01129-4
De Long JR, Jackson BG, Wilkinson A, Pritchard WJ, Oakley S, Mason KE et al (2019) Relationships between plant traits, soil properties and carbon fluxes differ between monocultures and mixed communities in temperate grassland. J Ecol 107:1704–1719. https://doi.org/10.1111/1365-2745.13160
DeGroote KV, McCartha GL, Pollard AJ (2018) Interactions of the manganese hyperaccumulator Phytolacca americana L. with soil pH and phosphate. Ecol Res 33:749–755. https://doi.org/10.1007/s11284-017-1547-z
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. https://doi.org/10.1007/BF02374894
Gardner WK, Parbery DG, Barber DA (1982) The acquisition of phosphorus by Lupinus albus L. I. some characteristics of the soil/root interface. Plant Soil 68:19–32. https://doi.org/10.1007/bf02374724
Gettier SW, Martens DC, Brumback TB Jr (1985) Timing of foliar manganese application for correction of manganese deficiency in soybean. Agron J 77:627–630. https://doi.org/10.2134/agronj1985.00021962007700040026x
Gray EF, Wright IJ, Falster DS, Eller ASD, Lehmann CER, Bradford MG, Cernusak LA (2019) Leaf:wood allometry and functional traits together explain substantial growth rate variation in rainforest trees. AoB Plants 11:plz024. https://doi.org/10.1093/aobpla/plz024
Hashem AR (1995) The role of mycorrhizal infection in the resistance of Vaccinium macrocarpon to manganese. Mycorrhiza 5:289–291. https://doi.org/10.1007/BF00204964
Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410. https://doi.org/10.1111/1365-2745.12196
Hayes PE, Clode PL, Guilherme Pereira C, Lambers H (2019) Calcium modulates leaf cell-specific phosphorus allocation in Proteaceae from South-Western Australia. J Exp Bot 70:3995–4009. https://doi.org/10.1093/jxb/erz156
Hill J, Attiwill PM, Uren NC, O'Brien ND (2001) Does manganese play a role in the distribution of the eucalypts? Aust J Bot 49:1–8. https://doi.org/10.1071/BT00012
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. https://doi.org/10.1007/s11104-009-0068-0
Huang G, Hayes PE, Ryan MH, Pang J, Lambers H (2017) Peppermint trees shift their phosphorus-acquisition strategy along a strong gradient of plant-available phosphorus by increasing their transpiration. Oecologia 185:487–400. https://doi.org/10.1007/s00442-017-3961-x
Ji W, LaZerte SE, Waterway MJ, Lechowicz MJ (2020) Functional ecology of congeneric variation in the leaf economics spectrum. New Phytol 225:196–208. https://doi.org/10.1111/nph.16109
Kirk GJD, Greenway H, Atwell BJ, Ismail AM, Colmer TD (2014) Adaptation of rice to flooded soils. Progr Bot 75:215–253. https://doi.org/10.1007/978-3-642-38797-5_8
Kohout P (2017) Biogeography of ericoid mycorrhiza. In: Tedersoo L (ed) Biogeography of Mycorrhizal Symbiosis. Springer International Publishing, Cham, pp 179–193. https://doi.org/10.1007/978-3-319-56363-3_9
Kooyman RM, Laffan SW, Westoby M (2017) The incidence of low phosphorus soils in Australia. Plant Soil 412:143–150. https://doi.org/10.1007/s11104-016-3057-0
Korcak RF (1989) Variation in nutrient requirements of blueberries and other calcifuges. HortSci 24:573–578
Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44. https://doi.org/10.1023/a:1026438615520
Kothari SK, Marschner H, Römheld V (1991) Effect of a vesicular–arbuscular mycorrhizal fungus and rhizosphere micro-organisms on manganese reduction in the rhizosphere and manganese concentrations in maize (Zea mays L.). New Phytol 117:649–655. https://doi.org/10.1111/j.1469-8137.1991.tb00969.x
Kula E, Wildová E, Hrdlička P (2018) Accumulation and dynamics of manganese content in bilberry (Vaccinium myrtillus L.). Environ Monit Assess 190:224. https://doi.org/10.1007/s10661-018-6604-8
Lambers H, Oliveira RS (2019) Plant physiological ecology, 3rd edn. Springer, Cham. https://doi.org/10.1007/978-3-030-29639-1
Lambers H, Teste FP (2013) Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do non-mycorrhizal species at both extremes of nutrient-availability play the same game? Plant Cell Environ 36:1911–1915. https://doi.org/10.1111/pce.12117
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. https://doi.org/10.1023/A:1014289121672
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. https://doi.org/10.1016/j.tree.2007.10.008
Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31. https://doi.org/10.1007/s11104-010-0444-9
Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90. https://doi.org/10.1016/j.tplants.2014.10.007
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. https://doi.org/10.1007/s11104-017-3427-2
Lambers H, Albornoz FE, Arruda AJ, Barker T, Finnegan PM, Gille C et al (2019) Nutrient-acquisition strategies. In: Lambers H (ed) A Jewel in the crown of a global biodiversity hotspot. Kwongan Foundation and the Western Australian Naturalists' Club Inc, Perth, pp 227–248
Lamont B (1972) The morphology and anatomy of proteoid roots in the genus Hakea. Aust J Bot 20:155–174. https://doi.org/10.1071/BT9720155
Leake JR, Read DJ (1989) The biology of mycorrhiza in the Ericaceae. New Phytol 113:535–544. https://doi.org/10.1111/j.1469-8137.1989.tb00366.x
Leopold M, Zhong H (2019) The soils of the Alison Baird reserve. In: Lambers H (ed) A Jewel in the crown of a global biodiversity hotspot. Kwongan Foundation and the Western Australian Naturalists' Club Inc, Perth, pp 49–57
Long L, Persson DP, Duan F, Jørgensen K, Yuan L, Schjoerring JK, Pedas PR (2018) The iron-regulated transporter 1 plays an essential role in uptake, translocation and grain-loading of manganese, but not iron, in barley. New Phytol 217:1640–1653. https://doi.org/10.1111/nph.14930
Losfeld G, L’Huillier L, Fogliani B, Coy SM, Grison C, Jaffré T (2014) Leaf-age and soil-plant relationships: key factors for reporting trace-elements hyperaccumulation by plants and design applications. Environ Sci Pollut Res 22:5620–5632. https://doi.org/10.1007/s11356-014-3445-z
Luteyn JL (2002) Diversity, adaptation, and endemism in neotropical Ericaceae: biogeographical patterns in the Vaccinieae. Bot Rev 68:55–87. https://doi.org/10.1663/0006-8101(2002)068[0055:DAAEIN]2.0.CO;2
Ma JF (2005) Plant root responses to three abundant soil minerals: silicon, aluminum and iron. Crit Rev Plant Sci 24:267–281. https://doi.org/10.1080/07352680500196017
Mansfeldt T (2004) Redox potential of bulk soil and soil solution concentration of nitrate, manganese, iron, and sulfate in two Gleysols. J Plant Nutr Soil Sci 167:7–16. https://doi.org/10.1002/jpln.200321204
Martin FM, Uroz S, Barker DG (2017) Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356:eaad4501. https://doi.org/10.1126/science.aad4501
McCormack ML, Iversen CM (2019) Physical and functional constraints on viable belowground acquisition strategies. Front Plant Sci 10:1215. https://doi.org/10.3389/fpls.2019.01215
McCulloch CE, Neuhaus JM (2005) Generalized linear mixed models. In: Armitage P, Colton T (eds) Encyclopedia of biostatistics. Wiley, New York, pp 2085–2089
Millaleo R, Alvear M, Aguilera P, González-Villagra J, de la Luz MM, Alberdi M, Reyes-Díaz M (2020) Mn toxicity differentially affects physiological and biochemical features in highbush blueberry (Vaccinium corymbosum L.) cultivars. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-019-00166-0
Muler AL, Oliveira RS, Lambers H, Veneklaas EJ (2014) Does cluster-root activity of Banksia attenuata (Proteaceae) benefit phosphorus or micronutrient uptake and growth of neighbouring shrubs? Oecologia 174:23–31. https://doi.org/10.1007/s00442-013-2747-z
Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205:1183–1194. https://doi.org/10.1111/nph.13175
Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioSci 51:933–938. https://doi.org/10.1641/0006-3568(2001)051[0933:Teotwa]2.0.Co;2
Page ER (1962) Studies in soil and plant manganese. Plant Soil 16:247–257. https://doi.org/10.1007/BF01377220
Pang J, Ruchi B, Zhao H, Bansal R, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KMH (2018) The carboxylate-releasing phosphorus-mobilising strategy could be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529. https://doi.org/10.1111/nph.15200
Papadakis IE, Sotiropoulos TE, Therios IN (2007) Mobility of iron and manganese within two citrus genotypes after foliar applications of iron sulfate and manganese sulfate. J Plant Nutr 30:1385–1396. https://doi.org/10.1080/01904160701555754
Pierce S, Negreiros D, Cerabolini BEL, Kattge J, Díaz S, Kleyer M, Shipley B, Wright SJ, Soudzilovskaia NA, Onipchenko VG, van Bodegom PM, Frenette-Dussault C, Weiher E, Pinho BX, Cornelissen JHC, Grime JP, Thompson K, Hunt R, Wilson PJ, Buffa G, Nyakunga OC, Reich PB, Caccianiga M, Mangili F, Ceriani RM, Luzzaro A, Brusa G, Siefert A, Barbosa NPU, Chapin FS III, Cornwell WK, Fang J, Fernandes GW, Garnier E, le Stradic S, Peñuelas J, Melo FPL, Slaviero A, Tabarelli M, Tampucci D (2017) A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct Ecol 31:444–457. https://doi.org/10.1111/1365-2435.12722
Pii Y, Cesco S, Mimmo T (2015) Shoot ionome to predict the synergism and antagonism between nutrients as affected by substrate and physiological status. Plant Physiol Bochem 94:48–56. https://doi.org/10.1016/j.plaphy.2015.05.002
Pillon Y, Petit D, Gady C, Soubrand M, Joussein E, Saladin G (2018) Ionomics suggests niche differences between sympatric heathers (Ericaceae). Plant Soil 434:481–489. https://doi.org/10.1007/s11104-018-3870-8
Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167:733–742. https://doi.org/10.1111/j.1469-8137.2005.01453.x
Poot P, Lambers H (2008) Shallow-soil endemics: adaptive advantages and constraints of a specialized root-system morphology. New Phytol 178:371–381. https://doi.org/10.1111/j.1469-8137.2007.02370.x
Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124. https://doi.org/10.1007/BF00202343
R_Development_Core_Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Römheld V (1987) Different strategies for iron acquisition in higher plants. Physiol Plant 70:231–234. https://doi.org/10.1111/j.1399-3054.1987.tb06137.x
Saatkamp A, Cochrane A, Commander L, Guja Lydia K, Jimenez-Alfaro B, Larson J et al (2019) A research agenda for seed-trait functional ecology. New Phytol 221:1764–1775. https://doi.org/10.1111/nph.15502
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167. https://doi.org/10.1105/tpc.112.096925
Schwery O, Onstein RE, Bouchenak-Khelladi Y, Xing Y, Carter RJ, Linder HP (2015) As old as the mountains: the radiations of the Ericaceae. New Phytol 207:355–367. https://doi.org/10.1111/nph.13234
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. https://doi.org/10.1111/j.1399-3054.2005.00527.x
Shane MW, De Vos M, De Roock S, Cawthray GR, Lambers H (2003) Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata r.Br. Plant Soil 248:209–219. https://doi.org/10.1023/A:1022320416038
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. https://doi.org/10.1104/pp.103.035659
Silveira FO, Negreiros D, Barbosa NU, Buisson E, Carmo F, Carstensen D et al (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152. https://doi.org/10.1007/s11104-015-2637-8
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London
Socha AL, Guerinot ML (2014) Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci 5:106. https://doi.org/10.3389/fpls.2014.00106
Sousa MF, Façanha AR, Tavares RM, Lino-Neto T, Gerós H (2007) Phosphate transport by proteoid roots of Hakea sericea. Plant Sci 173:550–558
Suresh R, Foy CD, Weidner JR (1987) Effects of excess soil manganese on stomatal function in two soybean cultivars. J Plant Nutr 10:749–760. https://doi.org/10.1080/01904168709363606
Tauss C, Keighery GJ, Keighery BJ, Cloran PM, Genovese SD (2019) A new look at the flora and the vegetation patterns of the greater Brixton street wetlands and Yule brook. In: Lambers H (ed) A Jewel in the crown of a global biodiversity hotspot. Kwongan Foundation and the Western Australian Naturalists' Club Inc, Perth, pp 69–207
Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367:eaba1223. https://doi.org/10.1126/science.aba1223
Turner BL, Blackwell MSA (2013) Isolating the influence of pH on the amounts and forms of soil organic phosphorus. Eur J Soil Sci 64:249–259. https://doi.org/10.1111/ejss.12026
Turner BL, Laliberté E, Hayes PE (2018) A climosequence of chronosequences in southwestern Australia. Eur J Soil Sci 69:69–85. https://doi.org/10.1111/ejss.12507
Viscarra Rossel RA, Bui EN (2016) A new detailed map of total phosphorus stocks in Australian soil. Sci Total Environ 542:1040–1049. https://doi.org/10.1016/j.scitotenv.2015.09.119
von Humboldt A (1807, translated 1826) Personal narrative of travels to the equinoctial regions of the new continent during the years 1799–1804 by Alexandre de Humboldt and Aimé Bonpland. Longman, Rees, Orme, Brown & Green, London
Warming E (1909) Oecology of plants. Clarendon Press, Oxford
Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227. https://doi.org/10.1023/A:1004327224729
Wojtuń B, Samecka-Cymerman A, Żołnierz L, Rajsz A, Kempers AJ (2017) Vascular plants as ecological indicators of metals in alpine vegetation (Karkonosze, SW Poland). Environ Sci Pollut Res 24:20093–20103. https://doi.org/10.1007/s11356-017-9608-y
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr 14:411–421. https://doi.org/10.1111/j.1466-822x.2005.00172.x
Wright IJ, Cooke J, Cernusak LA, Hutley LB, Scalon MC, Tozer WC, Lehmann CER (2019) Stem diameter growth rates in a fire-prone savanna correlate with photosynthetic rate and branch-scale biomass allocation, but not specific leaf area. Aust Ecol 44:339–350. https://doi.org/10.1111/aec.12678
Yu R-P, Li X-X, Xiao Z-H, Lambers H, Li L (2020a) Phosphorus facilitation and covariation of root traits in steppe species. New Phytol 226:1285–1298. https://doi.org/10.1111/nph.16499
Yu R-P, Zhang W, Yu Y, Yu S, Lambers H, Li L (2020b) Linking shifts in species composition induced by grazing with root traits for phosphorus acquisition in a typical steppe in Inner Mongolia. Sci Total Environ 712:136495. https://doi.org/10.1016/j.scitotenv.2020.136495
Zemunik G (2019) Diversity of the Yule brook region in context. In: Lambers H (ed) A Jewel in the crown of a global biodiversity hotspot. Kwongan Foundation and the Western Australian Naturalists' Club Inc, Perth, pp 59–68
Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050. https://doi.org/10.1038/nplants.2015.50
Zemunik G, Davies SJ, Turner BL (2018) Soil drivers of local-scale tree growth in a lowland tropical forest. Ecology 99:2844–2852. https://doi.org/10.1002/ecy.2532
Zhong H, Zhou J, Arruda AJ, Doolette AL, Smernik RJ, Lambers H (2020) Xylomelum occidentale (Proteaceae) accesses relatively mobile soil organic phosphorus without releasing carboxylates. J Ecol in press. https://doi.org/10.1111/1365-2745.13468
Zhou J, Zúñiga-Feest A, Lambers H (2020) In the beginning, there was only bare regolith - then some plants arrived and changed the regolith. J Plant Ecol 13:511–516 (in press). https://doi.org/10.1093/jpe/rtaa030
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer-Verlag, New York
Acknowledgements
This research was supported by an ARC-funded Discovery Project grant (DP130100005) awarded to HL and supporting CGP and PEH, and by ARC DP120103284 (awarded to IJW and LAC, also supporting EFG). PJB and SJR were funded by the Strategic Science Investment Fund of the NZ Ministry of Business, Innovation and Employment’s Science and Innovation Group. CS was funded by the FWF Erwin-Schrödinger Fellowship (J4127).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Tim S. George.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Hans Lambers, Ian J. Wright and Caio Guilherme Pereira are joint first authors
William Foulds and Michael W. Shane are Deceased
Electronic supplementary material
ESM 1
(DOCX 486 kb)
Rights and permissions
About this article
Cite this article
Lambers, H., Wright, I.J., Guilherme Pereira, C. et al. Leaf manganese concentrations as a tool to assess belowground plant functioning in phosphorus-impoverished environments. Plant Soil 461, 43–61 (2021). https://doi.org/10.1007/s11104-020-04690-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04690-2