Plant and Soil

, Volume 342, Issue 1–2, pp 105–115 | Cite as

Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution

  • Wenqing Wang
  • Siyang You
  • Yunbo Wang
  • Li Huang
  • Mao Wang
Regular Article


The latitudinal distribution of mangrove species is limited mainly by low temperature. Leaf scorch and massive leaf fall are the predominant symptoms of frost damage. Nutrient resorption during leaf senescence is an important adaptation mechanism of mangroves. Abnormal defoliation disturbs nutrient resorption. We evaluated the effects of frost on nutrient loss of mangroves and the protective effects of warmer seawater inundation on reducing nutrient loss. On January 14, 2009, the most cold-tolerant mangrove Kandelia obovata at its naturally latitudinal limit (Fuding, China, 27°17′N) was exposed to freezing temperature (−2.4°C) for 4 h (minimum −2.8°C). The freezing air temperature occurred during flood tide, resulting that the flooded shoots were protected by warmer seawater. Frost caused 31.3% and 13.0% defoliation on the exposed shoots and the flooded shoots, respectively. Frost restricted nutrient resorption during leaf senescence. K. obovata resorbed 61% N and 42% P during normal leaf senescence, respectively. However, frost-damaged leaves only resorbed 13% N and 10% P during the course, respectively. Foliar N:P molar ratios were <31, suggesting N limitation. Tidal inundation can partially protect mangroves from frost damage. Reduced nutrient resorption efficiency and massive leaf fall caused by frost add pressure to mangroves under nutrient limitation at their latitudinal limits.


Mangrove Kandelia obovata Frost Low temperature Nutrition resorption Flooding Latitudinal limit 



We would like to thank Prof SY Lee, Prof S Shi and anonymous reviewers for their helpful comments during manuscript preparation. This research was jointly supported by the National Natural Science Foundation of China (No. 30930017), the National Basic Research Program of China (No. 2009CB426306) and the National Special Research Programs for Non-Profit Trades (Oceanography) (No. 200805072).


  1. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  2. Alongi DM, Boto KG, Robertson A (1992) Nitrogen and phosphorus cycles. In: Robertson AI, Alongi DM (eds) Tropical mangrove ecosystems. American Geophysical Union, Washington, DC, pp 251–292Google Scholar
  3. Alongi DM, Clough BF, Robertson AI (2005) Nutrient-use efficiency in arid-zone forests of the mangroves Rhizophora stylosa and Avicennia marina. Aquat Bot 82:121–131CrossRefGoogle Scholar
  4. Anderson C, Lee SY (1995) Defoliation of the mangrove Avicennia marina in Hong Kong: cause and consequences. Biotropica 27:218–226CrossRefGoogle Scholar
  5. Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543CrossRefGoogle Scholar
  6. Biebl R, Kinzel H (1965) Blattbau und Salzhaushalt von Laguncularia racemosa (L.) Gaertn. f. und anderer Mangrovebaüme auf Puerto Rico. Oesterr Bot Zeit 112:56–93CrossRefGoogle Scholar
  7. Chapin FS, Moilanen L (1991) Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72:709–715CrossRefGoogle Scholar
  8. Chapman VJ, Ronaldson JW (1958) The mangrove and salt-marsh flats of the Auckland Isthmus. N Z Dep Sci Ind Res 125:1–79Google Scholar
  9. Chen L, Wang W, Zhang Y, Huang L, Zhao C, Yang S, Yang Z, Chen Y, Xu H, Zhong C, Su B, Fang B, Chen N, Zeng C, Lin G (2010) Damage to mangroves from extreme cold in early 2008 in southern China. J Plant Ecol 34:186–194 (in Chinese)Google Scholar
  10. Collier DE, Thibodeau BA (1995) Changes in respiration and chemical content during autumnal senescence of Populus tremuloides and Quercus rubra leaves. Tree Physiol 15:759–764PubMedGoogle Scholar
  11. Cram WJ, Torr PG, Rose DA (2002) Salt allocation during leaf development and leaf fall in mangroves. Trees Struct Func 16:112–119Google Scholar
  12. Duke NC (1990) Phenological trends with latitude in the mangrove tree Avicennia marina. J Ecol 78:113–133CrossRefGoogle Scholar
  13. Duke NC (1992) Mangrove floristics and biogeography. In: Robertson AI, Alongi DM (eds) Tropical mangrove ecosystems. American Geophysical Union, Washington, DC, pp 63–100Google Scholar
  14. Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Glob Ecol Biogeogr Lett 7:27–47CrossRefGoogle Scholar
  15. Ellis WL, Bowles JW, Erickson AA et al (2006) Alteration of the chemical composition of mangrove (Laguncularia racemosa) leaf litter fall by freeze damage. Estuar Coast Shelf Sci 68:363–371CrossRefGoogle Scholar
  16. Ellison JC (1994) Climate change and sea level rise impacts on mangrove ecosystems. In: Pernetta JC, Leemans R, Elder D, Humphrey S (eds) Impacts of climate change on ecosystems and species: marine and coastal ecosystems. A Marine Conservation and Development Report, IUCN, Gland, Switzerland, pp 11–30Google Scholar
  17. Fan H, Qiu G (2004) Insect pests of Avicennia marina mangroves along the coast of Beibu Gulf in China and the research strategies. Guihaia 6:558–562 (in Chinese)Google Scholar
  18. Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505CrossRefGoogle Scholar
  19. Feller IC, Whigham DF, O’Neill JP, McKee KL (1999) Effects of nutrient enrichment on within-stand cycling in a mangrove forest. Ecology 80:2193–2205CrossRefGoogle Scholar
  20. Feller IC, Whigham DF, McKee KM, O’Neill JP (2002) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175CrossRefGoogle Scholar
  21. Feller IC, Whigham DF, McKee KL, Lovelock CE (2003) Nitrogen limitation of growth and nutrient dynamics in a distributed mangrove forest, Indian River Lagoon, Florida. Oecologia 134:405–414PubMedGoogle Scholar
  22. Feller IC, Lovelock CE, McKee KL (2007) Nutrient addition differentially affects ecological processes of Avicennia germinans in nitrogen vs. phosphorus limited mangrove. Ecosystems 10:347–359CrossRefGoogle Scholar
  23. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Persp Plant Ecol Evol Syst 5:37–61CrossRefGoogle Scholar
  24. Hoch WA, Zeldin EL, McCown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21:1–8PubMedGoogle Scholar
  25. Hogarth PJ (2007) The biology of mangroves and seagrasses. Oxford University Press, New YorkCrossRefGoogle Scholar
  26. Hong PN, San HT (1993) Mangroves of Vietnam. IUCN, BangkokGoogle Scholar
  27. Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937PubMedCrossRefGoogle Scholar
  28. Hsueh ML, Lee HH (2000) Diversity and distribution of the mangrove forests in Taiwan. Wetl Ecol Manage 8:233–242CrossRefGoogle Scholar
  29. Hutching P, Saenger P (1987) Ecology of mangroves. University of Queensland Press, QueenslandGoogle Scholar
  30. Kangas PC, Lugo AE (1990) The distribution of mangroves and saltmarsh in Florida. J Trop Ecol 31:32–39Google Scholar
  31. Kao WY, Shin CN, Tsa TT (2004) Sensitivity to chilling temperatures and distribution differ in the mangrove species Kandelia candel and Avicennia marina. Tree Physiol 24:89–864Google Scholar
  32. Kawakami N, Watanabe A (1993) Translatable mRNAs for chloroplast-targeted proteins in detached radish cotyledons during senescence in darkness. Plant Cell Physiol 34:697–704Google Scholar
  33. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727CrossRefGoogle Scholar
  34. Koch MS (1997) Rhizophora mangle L. seedling development into the sapling stage across resource and stress gradients in subtropical Florida. Biotropica 29:427–439CrossRefGoogle Scholar
  35. Krauss KW, Lovelock CE, McKee KL, López-Hoffman L, Ewe SML, Sousa WP (2008) Environmental drivers in mangrove establishment and early development: a review. Aquat Bot 89:105–127CrossRefGoogle Scholar
  36. Lee SY (1991) Herbivory as an Ecological Process in a Kandelia candel (Rhizophoraceae) mangal in Hong Kong. J Trop Ecol 7:337–348CrossRefGoogle Scholar
  37. Lin P, Wang W (2001) Changes in the leaf composition, leaf mass and leaf area during leaf senescence in three species of mangroves. Ecol Eng 16:415–424CrossRefGoogle Scholar
  38. Lin YM, Liu XW, Zhang H, Fan HQ, Lin GH (2010) Nutrient conservation strategies of a mangrove species Rhizophora stylosa under nutrient limitation. Plant Soil 326:469–479CrossRefGoogle Scholar
  39. Lovelock CE, Feller IC, McKee KL, Englbrecht BMJ, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama. Funct Ecol 18:25–33CrossRefGoogle Scholar
  40. Lovelock CE, Feller IC, Ellis J, Schwarz AM, Hancock N, Nichols P, Sorrell B (2007) Mangrove growth in New Zealand estuaries: the role of nutrient enrichment at sites with contrasting rates of sedimentation. Oecologia 153:633–641PubMedCrossRefGoogle Scholar
  41. Lugo AE, Patterson-Zucca C (1977) The impact of low temperature stress on mangrove structure and growth. J Trop Sci 18:149–161Google Scholar
  42. Markley JL, McMillan C, Thompson JGA (1982) Latitudinal differentiation in response to chilling temperatures among population of three mangroves Avicennia germinans, Laguncularia racemosa, and Rhizophora mangle from the western tropical Atlantic and Pacific Panama. Can J Bot 60:2704–2715CrossRefGoogle Scholar
  43. Maxwell GS, Havanond S, Nakamura T (1997) The ecogeography of Kandelia candel in Thailand, Hong Kong and Southern Islands of Japan. Bull Nati Taiwan Normal Univ 32:89–95Google Scholar
  44. May JD, Killingbeck KT (1992) Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology 73:1868–1878CrossRefGoogle Scholar
  45. McMillan C, Sherrod CL (1986) The chilling tolerance of black mangrove, Avicennia germinans, from the Gulf of Mexico coast of Texas Louisiana and Florida. Contrib Mar Sci 29:9–16Google Scholar
  46. Medina E, Cuevas E, Lugo AE (2010) Nutrient relations of dwarf Rhizophora mangle L. mangroves on peat in eastern Puerto Rico. Plant Ecol 207:13–24CrossRefGoogle Scholar
  47. 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 63:301–309Google Scholar
  48. Moore RT, Miller PC, Albright D, Tieszen LL (1972) Comparative gas exchange characteristics of three mangrove species during the winter. Photosynthetica 6:387–393Google Scholar
  49. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  50. Naidoo G (1987) Effects of salinity and nitrogen on growth and water relations in the mangrove Avicennia marina (Forsk.) Vierh. New Phytol 107:317–325CrossRefGoogle Scholar
  51. Naidoo G (2006) Factors contributing to dwarfing in the mangrove Avicennia marina. Ann Bot 97:1095–1101PubMedCrossRefGoogle Scholar
  52. Nakasuga T (1979) Analysis of the mangrove stand. Sci Bull Coll Agric Univ Ryukyus 26:413–519Google Scholar
  53. Norman HA, McMillan C, Thompson GA (1984) Phosphatidylglycerol molecular species in chilling-sensitive and chilling-resistant populations of Avicennia germinans (L) L. Plant Cell Physiol 25:1437–1444Google Scholar
  54. Ochieng CA, Erftemeijer PL (2002) Phenology, litterfall and nutrient resorption in Avicennia marina (Forssk.) Vierh in Gazi Bay, Kenya. Trees Struct Func 16:167–171Google Scholar
  55. Pugnaire FI, Chapin FS (1993) Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology 74:124–129CrossRefGoogle Scholar
  56. Rao RG, Woitchik AF, Goeyens L, van Riet A, Kazungu J, Dehairs F (1994) Carbon, nitrogen contents and stable carbon isotope abundance in mangrove leaves from an east African coastal lagoon (Kenya). Aquat Bot 47:175–183CrossRefGoogle Scholar
  57. Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30:1148–1160PubMedCrossRefGoogle Scholar
  58. Rejmánková E (2005) Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytol 167:471–482PubMedCrossRefGoogle Scholar
  59. Ross MS, Ruiz PR, Sah JS, Hanan EJ (2009) Chilling damage in a changing climate in coastal landscapes of the subtropical zone: a case study from south Florida. Glob Change Biol 15:1817–1832CrossRefGoogle Scholar
  60. Sherrod CL, McMillan C (1985) The distributional history and ecology of mangrove vegetation along the northern Gulf of Mexico coastal region. Contrib Mar Sci 28:129–140Google Scholar
  61. Sherrod CL, Hockaday DL, McMillan C (1986) Survival of red mangrove, Rhizophora mangle, on the Gulf of Mexico coast of Texas. Contrib Mar Sci 29:27–36Google Scholar
  62. Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448CrossRefGoogle Scholar
  63. Smith JAC, Popp M, Lüttge U, Cram WJ, Diaz M, Griffiths H, Lee HSJ, Medina E, Schäfer C, Stimmel KH, Thonke B (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela VI. Water relations and gas exchange of mangroves. New Phytol 111:293–307CrossRefGoogle Scholar
  64. Stuart SA, Choat B, Martin KC et al (2007) The role of freezing in setting the latitudinal limits of mangrove forests. New Phytol 173:576–583PubMedCrossRefGoogle Scholar
  65. Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, CambridgeGoogle Scholar
  66. Tong YF, Lee SY, Morton B (2003) Effects of artificial defoliation on growth, reproduction and leaf chemistry of the mangrove Kandelia candel. J Trop Ecol 19:397–406CrossRefGoogle Scholar
  67. Twilley RW, Lugo AE, Patterson-Zucca C (1986) Litter production and turnover in basin mangrove forests in southwest Florida. Ecology 67:670–683CrossRefGoogle Scholar
  68. Walter H, Steiner M (1936) Die Ökologie der OstAtrikanischen Mangroven. Z Bot 30:65–193Google Scholar
  69. Wang W, Lin P (1999) Transfer of salt and nutrients in Bruguiera gymnorrhiza leaves during development and senescence. Mangrove Salt Marsh 3:1–7CrossRefGoogle Scholar
  70. Wang W, Lin P (2001) Comparative study on seasonal changes in element concentrations in leaves of Kandelia candel and Rhizophora stylosa at Jiulongjiang estuary. Acta Ecol Sin 21:1233–1238 (in Chinese)Google Scholar
  71. Wang W, Wang M (2007) The mangroves of China. Science, BeijingGoogle Scholar
  72. Wang W, Wang M, Lin P (2003) Seasonal changes in element contents in mangrove element retranslocation during leaf senescence. Plant Soil 252:187–193CrossRefGoogle Scholar
  73. Yang S, Lin P (1998) Ecological studies on the resistance and adaptation to cold of some tidal mangrove species in China. Acta Phytoecol Sin 22:60–67 (in Chinese)Google Scholar
  74. Yang S, Lin P, Li Z, Wang W, Nakasuga T (1999) Effect of low night temperature on photosynthetic properties of mangrove seedlings. J Xiamen Univ (Nat Sci) 38:617–622 (in Chinese)Google Scholar
  75. Yates EJ, Ashwath N, Midmore DJ (2002) Responses to nitrogen, phosphorus, potassium and sodium chloride by three mangrove species in pot culture. Trees Struct Func 16:120–125Google Scholar
  76. Yoshida S, Forno DA, Cock JH, Gomez KA (1972) Laboratory manual for physiological studies of rice, 2nd edn. The International Rice Research Institute, ManilaGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Wenqing Wang
    • 1
    • 2
    • 3
  • Siyang You
    • 1
  • Yunbo Wang
    • 1
  • Li Huang
    • 4
  • Mao Wang
    • 1
    • 3
    • 5
  1. 1.Key Laboratory of Ministry of Education for Coastal and Wetland Ecosystems, School of Life SciencesXiamen UniversityXiamenChina
  2. 2.State Key Laboratory of Marine Environmental ScienceXiamen UniversityXiamenChina
  3. 3.Australian Rivers InstituteGriffith UniversityGold CoastAustralia
  4. 4.Zhejiang Provincial Institute of Marine Aquaculture ResearchWenzhouChina
  5. 5.School of Life SciencesXiamen UniversityXiamenChina

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