Abstract
Tropical forests play an enormously important role in the global cycling of carbon. However, the extent to which nutrients limit the potential for tropical trees to increase carbon gain as atmospheric carbon dioxide rises, a phenomenon known as the carbon-concentration feedback, is uncertain. This chapter addresses our current state of knowledge on nutrient limitation of photosynthesis in tropical trees, summarizing and synthesizing the results of over 20 studies on photosynthetic responses to nutrient manipulation experiments. Our results indicate that nutrient limitation of photosynthesis is widespread, but that contrasting species and ecosystems vary in their responses, with savannah trees showing the least response at the leaf scale. Second, although photosynthesis is strongly limited by N in particular species, N limitation of photosynthesis is modest compared to P limitation of photosynthesis when considering all of the available literature. Finally, alleviation of nutrient limitation through addition of combined nutrient treatments produces the strongest photosynthetic responses, highlighting the potentially complex stroichiometric interactions among elements. The authors discuss several ways forward for resolving questions regarding the potential and limits of tropical trees to influence key carbon cycling processes and thus improve our ability to forecast global responses and feedbacks to climate change .
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–66
Ali AA, Xu C, Rogers A, McDowell NG, E. MB, Fisher R, Wullschleger SD, Reich PB, Vrugt JA, Baurle WL, Santiago LS, Wilson CJ (2015) Global scale environmental control of plant photosynthetic capacity. Ecol Appl 25:2349–2365
Álvarez-Clare S, Mack MC, Brooks M (2013) A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94:1540–1551
Andersen KM, Corre MD, Turner BL, Dalling JW (2010) Plant-soil associations in a lower montane tropical forest: physiological acclimation and herbivore-mediated responses to nitrogen addition. Funct Ecol 24:1171–1180
Baltzer JL, Davies SJ, Bunyavejchewin S, Noor NSM (2008) The role of desiccation tolerance in determining tree species distributions along the Malay-Thai Peninsula. Funct Ecol 22:221–231
Barberis IM, Tanner EVJ (2005) Gaps and root trenching increase tree seedling growth in Panamanian semi-evergreen forest. Ecology 86:667–674
Beer C, Reichstein M, Tomelleri E, Ciais P, Jung M, Carvalhais N, Rodenbeck C, Arain MA, Baldocchi D, Bonan GB, Bondeau A, Cescatti A, Lasslop G, Lindroth A, Lomas M, Luyssaert S, Margolis H, Oleson KW, Roupsard O, Veenendaal E, Viovy N, Williams C, Woodward FI, Papale D (2010) Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329:834–838
Bloom AJ, Chapin FS III, Mooney HA (1985) Resource limitation in plants-an economic analogy. Annu Rev Ecol Syst 16:363–392
Bloomfield KJ, Farquhar GD, Lloyd J (2014) Photosynthesis-nitrogen relationships in tropical forest tree species as affected by soil phosphorus availability: a controlled environment study. Funct Plant Biol 41:820–832
Bonan GB, Levis S (2010) Quantifying carbon-nitrogen feedbacks in the Community Land Model (CLM4). Geophys Res Lett 37(7):L07401
Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Campanello PI, Villalobos-Vega R, Bustamante M, Miralles-Wilhelm F (2006) Nutrient availability constrains the hydraulic architecture and water relations of savannah trees. Plant Cell Environ 29:2153–2167
Bungard RA, Zipperlen SA, Press MC, Scholes JD (2002) The influence of nutrients on growth and photosynthesis of seedlings of two rainforest dipterocarp species. Funct Plant Biol 29:505–515
Burslem DFRP (1996) Differential responses to nutrients, shade and drought among tree seedlings of lowland tropical forest in Singapore. In: Swaine MD (ed) The ecology of tropical forest tree seedlings. UNESCO, Paris, pp 211–244
Cai ZQ, Poorter L, Han Q, Bongers F (2008) Effects of light and nutrients on seedlings of tropical Bauhinia lianas and trees. Tree Physiol 28:1277–1285
Campo J, Dirzo R (2003) Leaf quality and herbivory responses to soil nutrient addition in secondary tropical dry forests of Yucatan, Mexico. J Trop Ecol 19:525–530
Campo J, Vázquez-Yanes C (2004) Effects of nutrient limitation on aboveground carbon dynamics during tropical dry forest regeneration in Yucatán, Mexico. Ecosystems 7:311–319
Carswell FE, Grace J, Lucas ME, Jarvis PG (2000) Interaction of nutrient limitation and elevated CO2 concentration on carbon assimilation of a tropical tree seedling (Cedrela odorata). Tree Physiol 20:977–986
Cernusak LA, Aranda J, Marshall JD, Winter K (2007a) Large variation in whole-plant water-use efficiency among tropical tree species. New Phytol 173:294–305
Cernusak LA, Winter K, Aranda J, Turner BL, Marshall JD (2007b) Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility. J Exp Bot 58:3549–3566
Cernusak LA, Winter K, Turner BL (2009) Physiological and isotopic (δ13C and δ18O) responses of three tropical tree species to water and nutrient availability. Plant Cell Environ 32:1441–1455
Cernusak LA, Winter K, Dalling JW, Holtum JAM, Jaramillo C, Korner C, Leakey ADB, Norby RJ, Poulter B, Turner BL, Wright SJ (2013) Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. Funct Plant Biol 40:531–551
Cordell S, Goldstein G, Meinzer FC, Vitousek PM (2001) Regulation of leaf life-span and nutrient-use efficiency of Metrosideros polymorpha trees at two extremes of a long chronosequence in Hawaii. Oecologia 127:198–206
Cramer MD, Hoffmann V, Verboom GA (2008) Nutrient availability moderates transpiration in Ehrharta calycina. New Phytol 179:1048–1057
Cramer MD, Hawkins HJ, Verboom GA (2009) The importance of nutritional regulation of plant water flux. Oecologia 161:15–24
Davidson EA, de Carvalho CJR, Vieira ICG, Figueiredo RD, Moutinho P, Ishida FY, dos Santos MTP, Guerrero JB, Kalif K, Saba RT (2004) Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol Appl 14:S150–S163
de Oliveira EAD, Approbato AU, Legracie JR, Martinez CA (2012) Soil-nutrient availability modifies the response of young pioneer and late successional trees to elevated carbon dioxide in a Brazilian tropical environment. Environ Exp Bot 77:53–62
Delucia EH, Sasek TW, Strain BR (1985) Photosynthetic inhibition after long-term exposure to elevated levels of atmospheric carbon dioxide. Photosynth Res 7:175–184
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19
Evans HJ, Sorger GJ (1966) Role of mineral elements with emphasis on the univalent cations. Ann Rev Plant Physiol 17:47–76
Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11:539–552
Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. University Press, Cambridge, pp 25–55
Fisher JB, Malhi Y, Torres IC, Metcalfe DB, van de Weg MJ, Meir P, Silva-Espejo JE, Huasco WH (2013) Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes. Oecologia 172:889–902
Friedlingstein P, Cox P, Betts R, Bopp L, Von Bloh W, Brovkin V, Cadule P, Doney S, Eby M, Fung I, Bala G, John J, Jones C, Joos F, Kato T, Kawamiya M, Knorr W, Lindsay K, Matthews HD, Raddatz T, Rayner P, Reick C, Roeckner E, Schnitzler KG, Schnur R, Strassmann K, Weaver AJ, Yoshikawa C, Zeng N (2006) Climate-carbon cycle feedback analysis: results from the C4MIP model intercomparison. J Clim 19:3337–3353
Furley PA, Ratter JA (1988) Soil resources and plant communities of the Central Brazilian cerrado and their development. J Biogeogr 15:97–108
Fyllas NM, Patiño S, Baker TR, Nardoto GB, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jiménez EM, Luizão FJ, Neill DA, Silva N, Prieto A, Rudas A, Silviera M, Vieira ICG, Lopez-Gonzalez G, Malhi Y, Phillips OL, Lloyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6:2677–2708
Gunatilleke CVS, Gunatilleke IAUN, Perera GAD, Burslem DFRP, Ashton PMS, Ashton PS (1997) Responses to nutrient addition among seedlings of eight closely related species of Shorea in Sri Lanka. J Ecol 85:301–311
Haridasan M (1992) Observations on soils, foliar nutrient concentrations and floristic composition of cerrado sensu stricto and cerradão communities in central Brazil. In: Pa F, Ratter J (eds) Nature and dynamics of forest-savanna boundaries. Chapman & Hall, London, pp 171–184
Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43
Kitayama K, Pattison R, Cordell S, Webb D, Mueller-Dombois D (1997) Ecological and genetic implications of foliar polymorphism in Metrosideros polymorpha Gaud. (Myrtaceae) in a habitat matrix on Mauna Loa. Hawaii. Annals Botany 80:491–497
Lawrence D (2003) The response of tropical tree seedlings to nutrient supply: meta-analysis for understanding a changing tropical landscape. J Trop Ecol 19:239–250
Lewis SL, Tanner EVJ (2000) Effects of above- and belowground competition on growth and survival of rain forest tree seedlings. Ecology 81:2525–2538
Liu JX, Zhang DQ, Zhou GY, Duan HL (2012) Changes in leaf nutrient traits and photosynthesis of four tree species: effects of elevated CO2, N fertilization and canopy positions. J Plant Ecol 5:376–390
Lovelock CE, Ball MC, Choat B, Engelbrecht BMJ, Holbrook NM, Feller IC (2006) Linking physiological processes with mangrove forest structure: phosphorus deficiency limits canopy development, hydraulic conductivity and photosynthetic carbon gain in dwarf Rhizophora mangle. Plant Cell Environ 29:793–802
Lu X, Mo J, Li D, Zhang W, Fang Y (2007) Effects of simulated N deposition on the photosynthetic and physiologic characteristics of dominant understorey plants in Dinghushan Mountain of subtropical China. J Beijing For Univ 29:1–9
Lu X, Mo J, Gilliam FS, Zhou G, Fang Y (2010) Effects of experimental nitrogen additions on plant diversity in an old-growth tropical forest. Glob Change Biol 16:2688–2700
Marschner H (1995) Mineral nutrition in higher plants. Academic Press, London
Mirmanto E, Proctor J, Green J, Nagy L, Suriantata (1999) Effects of nitrogen and phosphorus fertilization in a lowland evergreen rainforest. Philos Trans R Soc Lond Ser B-Biol Sci 354:1825–1829
Morgan JM (1984) Osmoregulation and water-stress in higher-plants. Ann Rev Plant Physiol Plant Mol Biol 35:299–319
Newbery DM, Chuyong GB, Green JJ, Songwe NC, Tchuenteu F, Zimmermann L (2002) Does low phosphorus supply limit seedling establishment and tree growth in groves of ectomycorrhizal trees in a central African rainforest? New Phytol 156:297–311
Oliveira MT, Medeiros CD, Frosi G, Santos MG (2014) Different mechanisms drive the performance of native and invasive woody species in response to leaf phosphorus. supply during periods of drought stress and recovery. Plant Physiol Biochem 82:66–75
Ostertag R (2009) Foliar phosphorus accumulation in relation to leaf traits: an example in a tropical wet forest in Hawaii. S Afr J Bot 75:415–415
Pasquini SC, Santiago LS (2012) Nutrients limit photosynthesis in seedlings of a lowland tropical forest tree species. Oecologia 168:311–319
Phillips OL, van der Heijden G, Lewis SL, Lopez-Gonzalez G, Aragao L, Lloyd J, Malhi Y, Monteagudo A, Almeida S, Davila EA, Amaral I, Andelman S, Andrade A, Arroyo L, Aymard G, Baker TR, Blanc L, Bonal D, de Oliveira ACA, Chao KJ, Cardozo ND, da Costa L, Feldpausch TR, Fisher JB, Fyllas NM, Freitas MA, Galbraith D, Gloor E, Higuchi N, Honorio E, Jimenez E, Keeling H, Killeen TJ, Lovett JC, Meir P, Mendoza C, Morel A, Vargas PN, Patino S, Peh KSH, Cruz AP, Prieto A, Quesada CA, Ramirez F, Ramirez H, Rudas A, Salamao R, Schwarz M, Silva J, Silveira M, Slik JWF, Sonke B, Thomas AS, Stropp J, Taplin JRD, Vasquez R, Vilanova E (2010) Drought-mortality relationships for tropical forests. New Phytol 187:631–646
Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83:553–559
Quesada CA, Lloyd J, Schwarz M, Patino S, Baker TR, Czimczik C, Fyllas NM, Martinelli L, Nardoto GB, Schmerler J, Santos AJB, Hodnett MG, Herrera R, Luizao FJ, Arneth A, Lloyd G, Dezzeo N, Hilke I, Kuhlmann I, Raessler M, Brand WA, Geilmann H, Moraes JO, Carvalho FP, Araujo RN, Chaves JE, Cruz OF, Pimentel TP, Paiva R (2010) Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7:1515–1541
Raven JA, Handley LL, Wollenweber B (2004) Plant nutrition and water use efficiency. In: Bacon MA (ed) Water use efficiency in plant biology. CRC Press, Boca Raton, pp 171–197
Riddoch I, Lehto T, Grace J (1991) Photosynthesis of tropical tree seedlings in relation to light and nutrient supply. New Phytol 119:137–147
Santiago LS (2015) Nutrient limitation of eco-physiological processes in tropical trees. Trees 29:1291–1300
Santiago LS, Mulkey SS (2005) Leaf productivity along a precipitation gradient in lowland Panama: patterns from leaf to ecosystem. Trees 19:349–356
Santiago LS, Wright SJ (2007) Leaf functional traits of tropical forest plants in relation to growth form. Funct Ecol 21:19–27
Santiago LS, Kitajima K, Wright SJ, Mulkey SS (2004) Coordinated changes in photosynthesis, water relations and leaf nutritional traits of canopy trees along a precipitation gradient in lowland tropical forest. Oecologia 139:495–502
Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316
Saraceno MIS (2006) Efeitos da fertilização a longo prazo no metabolism fotossintético, nas características foliares e no crescimento em árvores do cerrado. In: Departamento de Ecologia, vol. Mestre em Ecologia. Universidade de Brasília, Instituto de Ciências Biológicas, Brasília, Brazil, p 65
Sayer EJ, Tanner EVJ (2010) Experimental investigation of the importance of litterfall in lowland semi-evergreen tropical forest nutrient cycling. J Ecol 98:1052–1062
Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2007) Removal of nutrient limitations by long-term fertilization decreases nocturnal water loss in savanna trees. Tree Physiol 27:551–559
Schreeg LA, Mack MC, Turner BL (2013) Nutrient-specific solubility patterns of leaf litter across 41 lowland tropical woody species. Ecology 94:94–105
Schreeg LA, Santiago LS, Wright SJ, Turner BL (2014) Stem, root, and older leaf N: P ratios are more responsive indicators of soil nutrient availability than new foliage. Ecology 95:2062–2068
Sinclair TR, Vadez V (2002) Physiological traits for crop yield improvement in low N and P environments. Plant Soil 245:1–15
Tanner EVJ, Kapos V, Franco W (1992) Nitrogen and phosphorus fertilization effects on Venezuelan montane forest trunk growth and litterfall. Ecology 73:78–86
Thompson WA, Stocker GC, Kriedemann PE (1988) Growth and photosynthetic response to light and nutrients of Flindersia brayleyana F Muell a rainforest tree with broad tolerance to sun and shade. Aust J Plant Physiol 15:299–315
Thompson WA, Huang LK, Kriedemann PE (1992) Photosynthetic response to light and nutrients in sun-tolerant and shade-tolerant rainforest trees. II. Leaf gas exchange and component processes of photosynthesis. Aust J Plant Physiol 19:19–42
Vitousek PM (2004) Nutrient cycling and limitation. Princeton University Press, Princeton
Vitousek PM, Aplet GH, Turner DR, Lockwood JJ (1992) The Mauna Loa environmental matrix: foliar and soil nutrients. Oecologia 89:372–382
Vitousek PM, Walker LR, Whiteaker LD, Matson PA (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23:197–215
Winter K, Garcia M, Gottsberger R, Popp M (2001) Marked growth response of communities of two tropical tree species to elevated CO2 when soil nutrient limitation is removed. Flora 196:47–58
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov V, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625
Wu P-F, Ma X-Q, Tigabu M, Huang Y, Zhou L-L, Cai L, Hou X-L, Oden PC (2014) Comparative growth, dry matter accumulation and photosynthetic rate of seven species of Eucalypt in response to phosphorus supply. J For Res 25:377–383
Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—a retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44:907–920
Yavitt JB, Wright SJ (2008) Seedling growth responses to water and nutrient augmentation in the understorey of a lowland moist forest, Panama. J Trop Ecol 24:19–26
Zhu F, Lu X, Mo J (2014) Phosphorus limitation on photosynthesis of two dominant understory species in a lowland tropical forest. J Plant Ecol 7:526–534
Acknowledgments
We gratefully acknowledge Alex Barron, Sandra Bucci, Walt Carson, Sarah Pasquini, Jennifer Powers, Fabian Scholz, Jim Sickman, Ben Turner, Peter Vitousek, Klaus Winter, Joe Wright, and Nina Würzburger for insightful discussions; Xiankai Lu and Keith Bloomfield for contributing raw data; the Smithsonian Tropical Research Institute and the University of California, Riverside, for logistical support; and a University of California Faculty Fellowship to Santiago.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Santiago, L.S., Goldstein, G. (2016). Is Photosynthesis Nutrient Limited in Tropical Trees?. In: Goldstein, G., Santiago, L. (eds) Tropical Tree Physiology. Tree Physiology, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-319-27422-5_14
Download citation
DOI: https://doi.org/10.1007/978-3-319-27422-5_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-27420-1
Online ISBN: 978-3-319-27422-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)