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Emergent macrophytes in phosphorus limited marshes: do phosphorus usage strategies change after nutrient addition?

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Abstract

Two strategies for phosphorus (P) economy in P-limiting environment are conservation of use and enhanced acquisition. Using two wetland macrophytes as an example, we show how these strategies change when the P-limitation is removed. Phosphorus resorption and activities of root phosphatases were evaluated over 4 years in Eleocharis cellulosa Torr. and Typha domingensis Pers. from nutrient addition experiment (P, N, N&P, control) established in 15 P limited marshes of Belize. We hypothesized that after P addition both species will increase tissue P content and decrease P resorption efficiency and root phosphatase activity. Initially high phosphorus resorption efficiency, PRE, significantly decreased in Eleocharis 2 years after the first nutrient addition, while no significant decrease was recorded for Typha. Even more dramatic was 5- to 6-fold increase in P in senescent tissues of Eleocharis as compared to less than 2-fold increase in Typha. Root phosphatase activity was high for both species from control plots. After P addition, Eleocharis showed 35% to 70% decrease in enzyme activity correlated to availability of inorganic P in sediments. Eleocharis and Typha employ the “conservation of use” strategy when growing in P limited oligotrophic marshes. In addition, Eleocharis is also using the “enhanced acquisition” strategy. These strategies change when the P limitation is removed but the response varies between the two species and thus changes in the proportion of these two species in a community may result in differences in ecosystem processes such as decomposition.

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References

  • Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8

    Article  PubMed  CAS  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  CAS  Google Scholar 

  • Asmar F, Gissel-Nielsen G (1997) Extracellular phosphomono- and phosphodiesterase associated with and released by the roots of barley genotypes: a non-destructive method for the measurement of the extracellular enzymes of roots. Biol Fertil Soils 25:117–122

    Article  CAS  Google Scholar 

  • Boers AM, Veltman RLD, Zedler JB (2007) Typha x glauca dominance and extended hydroperiod constrain restoration of wetland diversity. Ecol Eng 29:232–244

    Article  Google Scholar 

  • Cai ZQ, Bongers F (2007) Contrasting nitrogen and phosphorus resorption efficiencies in trees and lianas from a tropical montane rain forest in Xishuangbanna, south-west China. J Trop Ecol 23:115–118

    Article  Google Scholar 

  • Chen HJ, Mendelssohn IA, Lorenzen B, Brix H, Miao SL (2005) Growth and nutrient responses of Eloecharis cellulosa (Cyperaceae) to phosphate level and redox intensity. Am J Bot 92:1457–1466

    Article  Google Scholar 

  • Craft CB, Richardson CJ (1993) Peat accretion and phosphorus accumulation along a eutrophication gradient in the northern Everglades. Biogeochemistry 22:133–156

    Article  CAS  Google Scholar 

  • Craft CB, Vymazal J, Richardson CJ (1995) Response of Everglades plant-communities to nitrogen and phosphorus additions. Wetlands 15:258–271

    Google Scholar 

  • Davis SE, Corronado-Molina C, Childers DL, Day JW (2003) Temporally dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter in oligotrophic mangrove wetlands of the Southern Everglades. Aquat Bot 75:199–215

    Article  CAS  Google Scholar 

  • Davis SE, Childers DL, Noe GB (2006) The contribution of leaching to the rapid release of nutrients and carbon in the early decay of wetland vegetation. Hydrobiologia 569:87–97

    Article  CAS  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800

    Article  CAS  Google Scholar 

  • Feller IC, Whigham DF, O'Neill JP, McKee KL (1999) Effects of nutrient enrichment on within-stand cycling in a mangrove forest. Ecology 80:2193–2205

    Google Scholar 

  • Feller IC, McKee KL, Whigham DF, O'Neill JP (2002) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175

    Article  Google Scholar 

  • Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56:341–347

    Article  Google Scholar 

  • Garbey C, Murphy KJ, Thiebaut G, Muller S (2004) Variation in P-content in aquatic plant tissues offers an efficient tool for determining plant growth strategies along a resource gradient. Freshw Biol 49:346–356

    Article  Google Scholar 

  • Grime JP (2001) Plant Strategies,Vegetation Processes, and Ecosystem Properties. Wiley, Chichester, p 417

    Google Scholar 

  • Gűsewell S (2005) Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Funct Ecol 19:344–354

    Article  Google Scholar 

  • Gűsewell S, Koerselman M (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Plant Ecol Evol Syst 5:37–61

    Article  Google Scholar 

  • Harrington RA, Fownes JH, Vitousek PM (2001) Production and resource use efficiencies in N- and P limited tropical forests: a comparison of responses to long-term fertilization. Ecosystems (N Y, Print) 4:646–657

    Article  CAS  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  CAS  Google Scholar 

  • Hoppe HG (1993) Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. In: Kemp PF (ed) Handbook of methods in aquatic microbial ecology. Lewis Publ., Boca Raton, FL, pp 423–431

    Google Scholar 

  • Johnson D, Leake JR, Lee JA (1999) The effects of quantity and duration of simulated pollutant nitrogen deposition on root-surface phosphatase activities in calcareous and acid grasslands: a bioassay approach. New Phytol 141:433–442

    Article  CAS  Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • King RB, Baillie IC, Abell TMB, Dunsmore JR, Gray DA, Pratt JH, et al (1992) Land Resources Assessment of Northern Belize. 513p

  • Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792

    Article  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Huang WZ (2002) Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey. Soil Biol Biochem 34:1207–1218

    Article  CAS  Google Scholar 

  • Kroehler CJ, Linkins AE (1988) The root surface phosphatases of Eriophorum vaginatum: effects of temperature, pH, substrate concentration and inorganic phosphorus. Plant Soil 105:3–10

    Article  CAS  Google Scholar 

  • Kuhn NL, Mendelssohn IA, McKee KL, Lorenzen B, Brix H, Miao SL (2002) Root phosphatase activity in Cladium jamaicense and Typha domingensis grown in Everglades soil at ambient and elevated phosphorus levels. Wetlands 22:794–800

    Article  Google Scholar 

  • 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 (Lond) 98:693–713

    Article  Google Scholar 

  • Macek P, Rejmánková E (2007) Response of emergent macrophytes to experimental nutrient and salinity additions. Funct Ecol 21:478–488

    Article  Google Scholar 

  • McKee KI, Mendelssohn IA, Hester MW (1988). Reexamination of pore water sulfide concentrations and redox potentials near the aerial roots of Rhizophora mangle and Avicennia germinans. Amer J Bot 75:1352–1364

    Article  Google Scholar 

  • McNamara AE, Hill WR (2000) UV-B irradiance gradient affects photosynthesis and pigments but not food quality of periphyton. Freshw Biol 43:649–662

    Google Scholar 

  • Miller RO (1998) Extractable chloride, nitrate, orthophosphate, potassium, and sulfate-sulfur in plant tissue: 2% acetic acid extraction. In: Karla YP (ed) handbook of reference methods for plant analyses. CRC, New York, pp 115–118

    Google Scholar 

  • Miao SL (2004) Rhizome growth and nutrient resorption: mechanisms underlying the replacement of two clonal species in Florida Everglades. Aquat Bot 78:55–66

    Article  CAS  Google Scholar 

  • Miao SL, Newman S, Sklar FH (2000) Effects of habitat nutrients and seed sources on growth and expansion of Typha domingensis. Aquat Bot 68:297–311

    Article  Google Scholar 

  • Newman S, Grace JB, Koebel JW (1996) Effects of nutrients and hydroperiod on Typha, Cladium, and Eleocharis: implications for Everglades restoration. Ecol Appl 6:444–783

    Article  Google Scholar 

  • Newman S, McCormick PV, Miao SL, Laing JA, Kennedy WC, O'Dell MB (2004) The effect of phosphorus enrichment on the nutrient status of a northern Everglades slough. Wetlands Ecol Manag 12:63–79

    Article  CAS  Google Scholar 

  • Noe GB, Childers DL, Jones RD (2001) Phosphorus biogeochemistry and the impact of phosphorus enrichment: why is the Everglades so unique? Ecosystems (N Y, Print) 4:603–624

    Article  CAS  Google Scholar 

  • Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2004) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289

    Article  CAS  Google Scholar 

  • Playsted CWS, Johnston ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170:491–500

    Article  PubMed  CAS  Google Scholar 

  • Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693

    Article  PubMed  CAS  Google Scholar 

  • Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49

    Article  CAS  Google Scholar 

  • Rejmánková E (2001) Effect of experimental phosphorus enrichment on oligotrophic tropical marshes in Belize, Central America. Plant Soil 236:33–53

    Article  Google Scholar 

  • Rejmánková E (2005) Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytol 167:471–482

    Article  PubMed  CAS  Google Scholar 

  • Rejmánková E, Houdková K (2006) Wetland plant decomposition under different nutrient conditions: what is more important, litter quality or site quality? Biogeochemistry 80:245–262

    Article  Google Scholar 

  • Rejmánková E, Pope KO, Post R, Maltby E (1996) Herbaceous wetlands of the Yucatan Peninsula: communities at extreme ends of environmental gradients. Int Rev Gesamten Hydrobiol 81:223–252

    Article  Google Scholar 

  • Rejmánková E, Komarek J, Komárková J (2004) Cyanobacteria—a neglected component of biodiversity: patterns of species diversity in inland marshes of northern Belize (Central America). Div Dist 10:189–199

    Article  Google Scholar 

  • Rejmánková E, Grieco J, Achee N, Masuoka P, Pope K, Roberts D et al (2006) Freshwater community interactions and malaria. In: Collinge SK, Ray Ch (eds) Disease Ecology, Oxford

  • Rejmánková E, Macek P, Kimberly Epps K (in press) Wetland ecosystem changes after three years of phosphorus addition. Wetlands

  • Richardson AE, George TS, Hens M, Simpson RJ (2005a) Utilization of soil organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI, Cambridge, pp 165–184

    Google Scholar 

  • Richardson SJ, Peltzer DA, Allen RB, McGlone MS (2005b) Resorption proficiency along a chronosequence: responses among communities and within species. Ecology 86:20–25

    Article  Google Scholar 

  • SAS Institute Inc 1998. Statview 5.0.1 Reference—SAS Institute, Inc., Cary, North Carolina

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  PubMed  CAS  Google Scholar 

  • Tarafdar JC, Claassen N (2005) Preferential utilization of organic and inorganic sources of phosphorus by wheat plant. Plant Soil 275:285–293

    Article  CAS  Google Scholar 

  • Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9:548–555

    Article  PubMed  CAS  Google Scholar 

  • Touchette BW, Burkholder JM (2007) Effects of temperature and nitrate on phosphomonoesterase activities between carbon source and sink tissues in Zostera marina L. J Exp Mar Biol Ecol 342:313–324

    Article  CAS  Google Scholar 

  • Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954

    Article  Google Scholar 

  • Turner BL, Newman S (2005) Phosphorus cycling in wetland soils: the importance of phosphate diesters. J Environ Qual 34:1921–1929

    Article  PubMed  CAS  Google Scholar 

  • Turner BL, Baxter R, Ellwood NTW, Whitton BA (2001) Characterization of the phosphatase activities of mosses in relation to their environment. Plant Cell Environ 24:1165–1176

    Article  CAS  Google Scholar 

  • van Heerwaarden LM, Toet S, Aerts R (2003a) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669

    Article  Google Scholar 

  • van Heerwaarden LM, Toet S, Aerts R (2003b) Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. J Ecol 91:1060–1070

    Article  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Vitousek PM (1998) Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems (N Y, Print) 1:401–407

    Article  CAS  Google Scholar 

  • Walk TC, Jaramillo R, Lynch JP (2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant Soil 279:347–366

    Article  CAS  Google Scholar 

  • Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophylll species. Funct Ecol 17:10–19

    Article  Google Scholar 

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Acknowledgments

We thank to Russell King, Ireneo Briceno, Dagmara Sirová, and Petr Macek for their assistance in the field and to Joy and Joel Futrell for laboratory assistance. Comments of Marcel Rejmanek to the first draft of the manuscript are appreciated. Comments and suggestions of two anonymous reviewers greatly improved the manuscript. This research was supported by NSF grant # 0089211 to E.R.

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Correspondence to Eliška Rejmánková.

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Rejmánková, E., Snyder, J.M. Emergent macrophytes in phosphorus limited marshes: do phosphorus usage strategies change after nutrient addition?. Plant Soil 313, 141–153 (2008). https://doi.org/10.1007/s11104-008-9687-0

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