Nutrient conservation strategies of a mangrove species Rhizophora stylosa under nutrient limitation

Plant and Soil

Volumn 326, Issue 1, 2010, Pages 469-479

  Lin, Yi Ming ^a   Liu, Xiao Wei ^a   Zhang, Hui ^a   Fan, Hang Qing ^b   Lin, Guang Hui ^a  

^a XIAMEN UNIVERSITY   (China)

^b Guangxi Mangrove Research Center   (China)

Author keywords

N:P ratio; Nutrient resorption; Rhizophora stylosa; Tannin

Indexed keywords

ADAPTATION; COASTAL ZONE; MANGROVE; NUTRIENT LIMITATION; NUTRIENT USE EFFICIENCY; PHENOLIC COMPOUND; SEASONAL VARIATION; SENESCENCE; TANNIN;

RHIZOPHORA STYLOSA; RHIZOPHORACEAE;

EID: 72149117099     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-009-0026-x     Document Type: Article

References (79)

1. Aber JD, Melillo JM, McClaugherty CA (1990) Predicting long term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Can J Bot 68: 2201-2208. doi: 10. 1139/b90-287.
2. Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10: 402-407. doi: 10. 1016/S0169-5347(00)89156-9.
3. Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84: 597-608. doi: 10. 2307/2261481.
4. Birk EJ, Vitousek PM (1986) Nitrogen availability and nitrogen use efficiency in loblolly pine stands. Ecology 67: 69-79. doi: 10. 1043/0012-9658(1986)067[0069: NAANUE]2. 0. CO; 2.
5. Boerner REJ (1984) Foliar nutrient dynamics and nutrient use efficiency of four deciduous tree species in relation to site fertility. J Appl Ecol 21: 1029-1040. doi: 10. 2307/2405065.
6. Bryant JP, Chapin FSIII, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357-368. doi: 10. 2307/3544308.
7. Cates RG, Rhoades DF (1977) Patterns in the production of antiherbivore chemical defenses in plant communities. Biochem Syst Ecol 5: 185-193. doi: 10. 1016/0305-1978(77)90003-5.
8. Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11: 233-260. doi: 10. 1146/annurev. es. 11. 110180. 001313.
9. Chapin FS, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64: 376-391. doi: 10. 1043/0012-9658(1983)064[0376: SCINAP]2. 0. CO; 2.
10. Chapin FS, Moilanen L (1991) Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72: 709-715. doi: 10. 1043/0012-9658(1991)072[0709: NCONAP]2. 0. CO; 2.
11. Close DC, McArthur C (2002) Rethinking the role of many plant phenolics-protection from photodamage not herbivores? Oikos 99: 166-172. doi: 10. 1034/j. 1600-0706. 2002. 990117. x.
12. Constantinides M, Fownes JH (1994) Nitrogen mineralization from leaves and litter of tropical plants: relationship to nitrogen, lignin and soluble polyphenol concentrations. Soil Biol Biochem 26: 49-55. doi: 10. 1016/0038-0717(94)90194-5.
13. Covelo F, Gallardo A (2001) Temporal variation in total phenolics concentration of Quercus robur in forested and harvested stands in northwestern Spain. Can J Bot 79: 1262-1269. doi: 10. 1139/cjb-79-11-1262.
14. Escudero A, del Arco JM, Sanz JC, Ayala J (1992) Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90: 80-87. doi: 10. 1007/BF00317812.
15. Fan HQ, Chen GH, He BY, Mo ZC (2005) Mangrove coastal wetland in Shankou and management. Ocean, Beijing, p 126 in Chinese.
16. Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51: 565-581. doi: 10. 2307/1934037.
17. Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65: 477-505. doi: 10. 1043/0012-9615(1995)065[0477: EONEOG]2. 0. CO; 2.
18. Fierer N, Schimel JP, Cates RG, Zou JP (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33: 1827-1839. doi: 10. 1016/S0038-0717(01)00111-0.
19. Fife DN, Nambiar EKS (1997) Changes in the canopy and growth of Pinus radiata in response to nitrogen supply. For Ecol Manage 93: 137-152. doi: 10. 1016/S0378-1127(96)03917-5.
20. Fircks Y, Ericsson T, Sennerby-Forsse L (2001) Seasonal variation of macronutrients in leaves, stems and roots of Salix dasyclados Wimm. grown at two nutrient levels. Biomass Bioenerg 21: 321-334. doi: 10. 1016/S0961-9534(01)00045-9.
21. Gallardo A, Merino J (1992) Nitrogen immobilization in leaf litter at two Mediterranean ecosystems of SW Spain. Biogeochemistry 15: 213-228. doi: 10. 1007/BF00002937.
22. Graham HD (1992) Stabilization of Prussian blue color in the determination of polyphenols. J Agric Food Chem 40: 801-805. doi: 1 0. 1021/jf00017a018.
23. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164: 243-266. doi: 10. 1111/j. 1469-8137. 2004. 01192. x.
24. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Ecol Evol Syst 5: 37-61. doi: 10. 1078/1433-8319-0000022.
25. Güsewell S, Koerselman W, Verhoeven JTA (2003) Biomass N: P ratios as indicators of nutrient limitation for plant populations in wetlands. Ecol Appl 13: 372-384. doi: 10. 1890/1051-0761(2003)013[0372: BNRAIO]2. 0. CO; 2.
26. Hagerman AE (2002) Tannin Chemistry. http://www. users. muohio. edu/hagermae/tannin. pdf.
27. Helmisaari HS (1992) Nutrient retranslocation within the foliage of Pinus sylvestris. Tree Physiol 10: 45-58.
28. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67: 283-335. doi: 10. 1086/417659 doi: 10. 1086/417659.
29. Hernes PJ, Benner R, Cowie GL, Goni MA, Bergamaschi BA, Hedges JI (2001) Tannin diagenesis in mangrove leaves from a tropical estuary: a novel molecular approach. Geochim Cosmochim Acta 65: 3109-3122. doi: 10. 1016/S0016-7037(01)00641-X.
30. Horner JD, Cates RG, Gosz JR (1987) Tannin, nitrogen and cell wall composition of green vs. senescent Douglas-fir foliage: within- and between- stand differences in stands of unequal density. Oecologia 72: 515-519. doi: 10. 1007/BF00378976.
31. Kandil FE, Grace MH, Seigler DS, Cheeseman JM (2004) Polyphenolics in Rhizophora mangle L. leaves and their changes during leaf development and senescence. Trees (Berl) 18: 518-528. doi: 10. 1007/s00468-004-0337-8.
32. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77: 1716-1727. doi: 10. 2307/2265777.
33. Kleiner KW, Raffa KF, Dickson RE (1999) Partitioning of 14C-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia 119: 408-418. doi: 10. 1007/s004420050802.
34. Koricheva J (1999) Interpreting phenotypic variation in plant allelochemistry: problems with the use of contents. Oecologia 119(4): 467-473. doi: 10. 1007/s004420050809.
35. Koricheva J (2002) The carbon-nutrient balance hypothesis is dead; long live the carbon-nutrient balance hypothesis? Oikos 98: 537-539. doi: 10. 1034/j. 1600-0706. 2002. 980319. x.
36. Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems - a review. Plant Soil 256: 41-66. doi: 10. 1023/A: 1026206511084.
37. Kraus TEC, Zasoski RJ, Dahlgren RA (2004) Fertility and pH effects on polyphenol and condensed tannin contents in foliage and roots. Plant Soil 262: 95-109. doi: 10. 1023/B: PLSO. 0000037021. 41066. 79.
38. Kuhajek JM, Payton IJ, Monks A (2006) The impact of defoliation on the foliar chemistry of southern rata (Metrosideros umbellata). N Z J Ecol 30: 237-249.
39. Kuiters AT (1990) Role of phenolic substances from decomposing forest litter in plant-soil interactions. Acta Bot Neerl 27: 329-348.
40. Lajtha K (1987) Nutrient resorption efficiency and the response to phosphorus fertilization in the desert shrub Larrea tridentata (DC.). Biogeochemistry 4: 265-276. doi: 10. 1007/BF02187370.
41. Lambers H, Chapin FSIII, Pons TL (1998) Plant Physiological Ecology. Springer Verlag, New York, USA.
42. Lin G, Sternberg Lda SL (1992) Effects of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangroves (Rhizophora mangle L.). Aust J Plant Physiol 19: 509-517. doi: 10. 1071/PP9920509.
43. Lin P, Wang WQ (2001) Changes in the leaf composition, leaf mass and leaf area during leaf senescence in three species of mangroves. Ecol Eng 16: 415-424. doi: 10. 1016/S0925-8574(00)00126-9.
44. Lin YM, Liu JW, Xiang P, Lin P, Ye GF, Sternberg Lda SL (2006) Tannin dynamics of propagules and leaves of Kandelia candel and Bruguiera gymnorrhiza in the Jiulong River Estuary, Fujian, China. Biogeochemistry 78: 343-359. doi: 10. 1007/s10533-005-4427-5.
45. Lin YM, Liu JW, Xiang P, Lin P, Ding ZH, Sternberg Lda SL (2007) Tannins and nitrogen dynamics in mangrove leaves at different age and decay stages (Jiulong River Estuary, China). Hydrobiologia 583: 285-295. doi: 10. 1007/s10750-006-0568-3.
46. Lin YM, Sternberg Lda SL (2007) Nitrogen and phosphorus dynamics and nutrient resorption of Rhizophora mangle leaves in south Florida, USA. Bull Mar Sci 80: 159-169.
47. Lodhiyal N, Lodhiyal LS (2003) Biomass and net primary productivity of Bhabar Shisham forests in Central Himalaya, India. For Ecol Manage 176: 217-235. doi: 10. 1016/S0378-1127(02)00267-0.
48. Loomis WE (1932) Growth-differentiation balance versus carbo-hydrate-nitrogen ratio. Proc Am Soc Hotic Sci 29: 240-245.
49. Lorio PL Jr (1986) Growth differentiation-balance: a basis for understanding southern pine beetle-tree interactions. For Ecol Manage 14: 259-273.
50. Mafongoya PL, Giller KE, Palm CA (1998) Decomposition and nitrogen release patterns of three pruning and litter. Agrofor Syst 38: 77-97. doi: 10. 1023/A: 1005978101429.
51. Maie N, Behrens A, Knicker H, Kögel-Knabner I (2003) Changes in the structure and protein binding ability of condensed tannins during decomposition of fresh needles and leaves. Soil Biol Biochem 35: 577-589. doi: 10. 1016/S0038-0717(03)00051-8.
52. Mansfield JL, Curtis PS, Zak DR, Pregitzer KS (1999) Genotypic variation for condensed tannin production in trembling Aspen (Populus tremuloides, Salicaceae) under elevated CO2 and in high- and low-fertility soil. Am J Bot 86: 1154-1159. doi: 10. 2307/2656979.
53. Matthews S, Mila I, Scalbert A, Donnelly DMX (1997) Extractable and non-extractable proanthocyanidins in barks. Phytochemistry 45: 405-410. doi: 10. 1016/S0031-9422(96)00873-4.
54. McKee KL, Feller IC, Popp M, Wanek W (2002) Mangrove isotopic (δ15N and δ13C) fraction across a nitrogen vs phosphorus limitation gradient. Ecology 83: 1065-1075. doi: 10. 1890/0012-9658(2002)083[1065: MINACF]2. 0. CO; 2.
55. Miao SL (2004) Rhizome growth and nutrient resorption: mechanisms underlying the replacement of two clonal species in Florida Everglades. Aquat Bot 78: 55-66. doi: 10. 1016/j. aquabot. 2003. 09. 001.
56. Millard P, Neilsen GH (1989) The influence of nitrogen supply on the uptake and remobilization of stored N for the seasonal growth of apple trees. Ann Bot (Lond) 63: 301-309.
57. Mooney HA, Gulmon SL (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32: 198-206. doi: 10. 2307/1308943.
58. Nambiar EKS, Fife DN (1987) Growth and nutrient retranslocation in needles of radiata pine in relation to nitrogen supply. Ann Bot (Lond) 60: 147-156.
59. Nanjing Institute of Soil Science (1978) Physical and Chemical Analysis of Soils. Science and Technology Press of Shanghai, Shanghai (in Chinese).
60. Nitao JK, Zangerl AR, Berenbaum MR (2002) CNG: requiescat in pace? Oikos 98: 540-546. doi: 10. 1034/j. 1600-0706. 2002. 980320. x.
61. Northup RR, Yu Z, Dahlgren RA, Vogt KA (1995) Polyphenol control of nitrogen release from pine litter. Nature 377: 227-229. doi: 10. 1038/377227a0.
62. Northup RR, Dahlgren RA, McColl JG (1998) Polyphenols as regulators of plant-litter-soil interactions in northern Califonia's pygmy forest: A positive feedback? Biogeochemistry 42: 189-220. doi: 10. 1023/A: 1005991908504.
63. Palm CA, Sanchez PA (1991) Nitrogen release of some tropical legumes as affected by their lignin and polyphenolic contents. Soil Biol Biochem 23: 83-88. doi: 10. 1016/0038-0717(91)90166-H.
64. Pugnaire FI, Chapin FS (1993) Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology 74: 124-129. doi: 10. 1043/0012-9658(1993)074[0124: CONRFL]2. 0. CO; 2.
65. Ralhan PK, Singh SP (1987) Dynamics of nutrients and leaf mass in Central Himalayan forest trees and shrubs. Ecology 68: 1974-1983. doi: 10. 1043/0012-9658(1987) 068[1974: DONALM]2. 0. CO; 2.
66. Rejmánková E (2005) Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytol 167: 471-482. doi: 10. 1111/j. 1469-8137. 2005. 01449. x.
67. Riipi M, Ossipov V, Lempa K, Haukioja E, Koricheva J, Ossipova S, Pihlaja K (2002) Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth, and accumulation of phenolics? Oecologia 130: 380-390. doi: 10. 1007/s00442-001-0826-z.
68. Serrano L (1992) Leaching from vegetation of soluble polyphenolic compounds, and their abundance in temporary ponds in the Doñana National Park (SW Spain). Hydrobiologia 229: 43-50. doi: 10. 1007/BF00006989.
69. Sharma BM (1983) Mineral content of leaves of some common tropical forest trees and their associated soils in Ibadan, Nigeria. Can J Res 13: 556-562. doi: 10. 1139/x83-081.
70. Teklay T (2004) Seasonal dynamics in the concentrations of micronutrients and organic constituents in green and senescent leaves of three agroforestry species in southern Ethiopia. Plant Soil 267: 297-307. doi: 10. 1007/s11104-005-0124-3.
71. Terrill TH, Rowan AM, Douglas GB, Barry TN (1992) Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grain. J Sci Food Agric 58: 321-329. doi: 10. 1002/jsfa. 2740580306.
72. Tomlinson PB (1986) The Botany of Mangroves. Cambridge University Press, Cambridge.
73. Tuomi J (1992) Toward integration of plant defence theories. Trends Evol Ecol 7: 365-367. doi: 10. 1016/0169-5347(92)90005-V.
74. Tuomi J, Nemiela P, Haukioja E, Sirén S, Neuvonen S (1984) Nutrient stress: an explanation for antiherbivore responses to defoliation. Oecologia 61: 208-210. doi: 10. 1007/BF00396762.
75. Walbridge MR (1991) Phosphorus availability in acid organic soils of the lower North Carolina plain. Ecology 72: 2083-2100. doi: 10. 1043/0012-9658(1991)072[2083: PAIAOS]2. 0. CO; 2.
76. Wen YG, Liu SR, Yuan CA (2002) The population distribution of mangrove at Yingluogang of Guangxi, China. Acta Ecol Sin 22: 1160-1165 in Chinese with English abstract.
77. Yoshida S, Forno DA, Cock JH, Gomez KA (1972) Laboratory manual for physiological studies of rice, 2nd edn. The International Rice Research Institute, Philiphines, pp 7-9 36-38.
78. Zhang LH, Lin YM, Ye GF, Liu XW, Lin GH (2008) Changes in the N and P concentrations, N: P ratios, and tannin content in Casuarina equisetifolia branchlets during development and senescence. J For Res 13: 302-311. doi: 10. 1007/s10310-008-0081-9.
79. Zucker WV (1983) Tannins: does structure determine function? An ecological perspective. Am Nat 121: 335-365. doi: 10. 1086/284065.