, Volume 828, Issue 1, pp 41–56 | Cite as

Physiologically adaptive plasticity in nutrient resorption efficiency of Avicennia officinalis L. under fluctuating saline environments in the Sundarbans of Bangladesh

  • Md. Rabiul AlamEmail author
  • Hossain Mahmood
  • Tanay Biswas
  • Md. Masudur Rahman
Primary Research Paper


Nutrient resorption efficiency is an important nutrient conservation and ecophysiological mechanism of mangroves growing in saline environments. This study investigated the nitrogen, phosphorus, and potassium resorption efficiency of Avicennia officinalis L. growing across a salinity gradient with seasonal variations in the Sundarbans of Bangladesh. Due to decreasing salinity during the monsoon and postmonsoon seasons, the nutrient availability in soil and nutrient resorption efficiency did not vary significantly among the low-salinity, medium-salinity, and high-salinity zones. However, the nutrient availability in the medium-salinity and high-salinity zones was significantly lower than that in the low-salinity zone during the premonsoon season due to increased salinity. Consequently, nutrient resorption efficiency in the medium-salinity and high-salinity zones was significantly higher than that in the low-salinity zone during the premonsoon. Further, leaf vein density of A. officinalis in the medium-salinity and high-salinity zones was significantly higher than that in the low-salinity zone. This modification in vein density was the mechanism for the higher nutrient resorption efficiency of A. officinalis in the medium-salinity and high-salinity zones than that in the low-salinity zone. This plasticity in nutrient resorption efficiency is a physiologically adaptive mechanism that enables A. officinalis to persist in increasingly saline environments due to climate change.


Climate change Interstitial soil salinity Leaf vein density Mangrove Retranslocation Salinity zone 



The authors acknowledge the financial support from Nagao Natural Environment Foundation (Granted in 2015), 3-3-7 Kotobashi, Sumida-ku, Tokyo 130-0022, Japan. The authors also acknowledge the technical support from Nutrient Dynamics Laboratory of Forestry and Wood Technology Discipline, Khulna University, Bangladesh. We specially thank Nature Research Editing Service for English language editing (Order # D5X9VSFY; key: F1E5-7666-541F-01F9-64AB).

Compliance with ethical standards

Conflict of interest

There is no conflict of interest associated with this article.


  1. Aerts, R. & F. S. Chapin, 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30: 1–67.Google Scholar
  2. Akenga, P., A. Salim, A. Onditi, A. Yusuf & W. Waudo, 2014. Determination of selected micro and macronutrients in sugarcane growing soils at Kakamega North District, Kenya. IOSR Journal of Applied Chemistry 7(7): 34–41.CrossRefGoogle Scholar
  3. Alam, M. R., H. Mahmood, M. M. Rahman, T. Biswas, S. Nasrin & M. S. T. L. R. Khushi, 2017. Ecological status and environmental protective role of Avicennia officinalis in the vulnerable coastal regions of Bangladesh: an overview. The Indian Forester 143(9): 817–822.Google Scholar
  4. Alam, M. R., H. Mahmood, M. S. T. L. R. Khushi & M. M. Rahman, 2018a. Adaptive phenotypic plasticity of Avicennia officinalis L across the salinity gradient in the Sundarbans of Bangladesh. Hydrobiologia 808(1): 163–174.CrossRefGoogle Scholar
  5. Alam, M. R., H. Mahmood & M. M. Rahman, 2018b. Maternal origins induced plasticity in salt adaptability of Avicennia officinalis L. seedlings in the Sundarbans of Bangladesh. Hydrobiologia 820: 227–244.CrossRefGoogle Scholar
  6. Allen, S. E., 1974. Chemical Analysis of Ecological Materials. Blackwell Scientific Publications, Oxford.Google Scholar
  7. Baethgen, W. E. & M. M. Alley, 1989. A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant Kjeldahl digests. Communications in Soil Science and Plant Analysis 20(9 & 10): 961–969.CrossRefGoogle Scholar
  8. Basar, A., 2012. Water security in the coastal region of Bangladesh: would desalinization be a solution to the vulnerable communities of the Sundarbans? Bangladesh e Journal of Sociology 9: 31–39.Google Scholar
  9. Brodribb, T. J., T. S. Field & G. J. Jordan, 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144: 1890–1898.CrossRefGoogle Scholar
  10. Chapman, V. J., 1976. Mangrove vegetation. J. Cramer, Vaduz.Google Scholar
  11. Chen, H., X. Benbo, W. Shudong, Z. Lihua, Z. Haichao & L. Yiming, 2016. Nutrient resorption and phenolics concentration associated with leaf senescence of the subtropical mangrove Aegiceras corniculatum: implications for nutrient conservation. Forests 7: 290.CrossRefGoogle Scholar
  12. Christensen, J. H., B. Hewitson, A. Busuioc, A. Chen, X. Gao, I. Held, R. Jones, R. K. Kolli, W. T. Kwon, R. Laprise, et al., 2007. Regional climate projections. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marqquis, K. B. Averyt, M. Tignor & H. L. Miller (eds), Climate change 2007: The physical science basis. Contribution of working group to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge: 847–940.Google Scholar
  13. Dunbar-Co, S., A. M. Wieczorek & C. W. Morden, 2008. Molecular phylogeny and adaptive radiation of the endemic Hawaiian Plantago species (Plantaginaceae). American Journal of Botany 95: 1177–1188.CrossRefGoogle Scholar
  14. Espinosa LY, J Flores (2011) A review of sea-level rise effect on mangrove forest species: anatomical and morphological modifications, global warming impacts—case studies on the economy, human health, and on urban and natural environments, S. Casalegno (Ed.), ISBN: 978-953-307-785-7, InTech 15: 253–276.Google Scholar
  15. Feller, I. C., D. F. Whigham, J. P. O’Neill & K. L. McKee, 1999. Effects of nutrient enrichment on within-stand cycling in a mangrove forest. Ecology 80: 2193–2205.CrossRefGoogle Scholar
  16. Fife, D. N. & E. K. S. Nambiar, 1997. Changes in the canopy and growth of Pinus radiata in response to nitrogen supply. Forest Ecology and Management 93: 137–152.CrossRefGoogle Scholar
  17. Fife, D. N., E. K. S. Nanbiar & E. Saur, 2008. Retranslocation of foliar nutrients in evergreen tree species planted in a Mediterranean environment. Tree Physiology 28: 187–196.CrossRefGoogle Scholar
  18. Gopal, B. & M. Chauhan, 2006. Biodiversity and its conservation in the Sundarbans Mangrove Ecosystem. Aquatic Sciences 68: 338–354.CrossRefGoogle Scholar
  19. Hogarth, P. J., 1999. The Biology of Mangroves. Oxford University Press, New York.Google Scholar
  20. Hutchings, P. & P. Saenger, 1987. Ecology of Mangroves. University of Queensland Press, Australia.Google Scholar
  21. Iftekhar, M. S. & P. Saenger, 2008. Vegetation dynamics in the Bangladesh Sundarbans mangroves: a review of forest inventories. Wetlands Ecology and Management 16: 291–312.CrossRefGoogle Scholar
  22. Janousek, C. N. & C. L. Folger, 2013. Inter-specific variation in salinity effects on germination in Pacific Northwest tidal wetland plants. Aquat. Bot. 111: 104–111.CrossRefGoogle Scholar
  23. Jennerjahn, T. C., E. Gilman, K. W. Krauss, L. D. Lacerda, I. Nordhaus & E. Wolanski, 2017. Mangrove ecosystems under climate change. In Rivera-Monroy, V. H., et al. (eds), Mangrove Ecosystems: A Global Biogeographic Perspective. Springer International Publishing, New York: 211–244.CrossRefGoogle Scholar
  24. Kathiresan, K. & B. L. Bingham, 2001. Biology of mangroves and mangrove ecosystem. Advances in Marine Biology 40: 81–251.CrossRefGoogle Scholar
  25. Killingbeck, K. T., 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77: 1716–1727.CrossRefGoogle Scholar
  26. Krauss, K. W., C. E. Lovelock, K. L. McKee, L. Lopez-Hoffman, S. M. L. Ewe & W. P. Sousa, 2008. Environmental drivers in mangrove establishment and early development: a review. Aquatic Botany 89: 105–127.CrossRefGoogle Scholar
  27. Krauss, K. W. & M. C. Ball, 2013. On the halophytic nature of mangroves. Trees 27: 7–11.CrossRefGoogle Scholar
  28. Ławniczak, A. E., 2011. Nitrogen, phosphorus, and potassium resorption efficiency and proficiency of four emergent macrophytes from nutrient-rich wetlands. Polish Journal of Environmental Studies 20(5): 1227–1234.Google Scholar
  29. Lovelock, C. E., D. R. Cahoon, D. A. Friess, G. R. Guntenspergen, K. W. Krauss, R. Reef, K. Rogers, M. L. Saunders, F. Sidik, A. Swales, N. Saintilan, L. X. Thuyen & T. Triet, 2015. The vulnerability of Indo-Pacific mangrove forests to sea-level rise. LETTER (Nature) 526: 559–563.CrossRefGoogle Scholar
  30. Mahmood, H. & O. Saberi, 2005. Degradation rate of leaf litter Bruguiera parviflora of mangrove forest of Kuala Selangor, Malaysia. Indian Journal of Forestry 28: 144–149.Google Scholar
  31. Mahmood, H., S. Saha, M. R. H. Siddique & M. N. Hasan, 2014. Salinity Stress on Growth, Nutrients and Carbon Distribution in Seedlings Parts of Heritiera fomes. International Journal of Environmental Engineering 1(4): 71–77.Google Scholar
  32. Mahmood, H., 2015. Handbook of selected plant species of the Sundarbans and the embankment ecosystem, Sustainable Development and Biodiversity Conservation in Coastal protection Forests, Bangladesh, GIZ GmbH, German Federal Ministry for Economic Cooperation and Development (BMZ).Google Scholar
  33. Marschner, H., 1995. Mineral nutrition of higher plants. Academic press, New York.Google Scholar
  34. Matesanz, S., E. Gianoli & F. Valladares, 2010. Global change and the evolution of phenotypic plasticity in plants. Annals of the New York Academy of Sciences 1206: 35–55.CrossRefGoogle Scholar
  35. McKee, K. L. & P. L. Faulkner, 2000. Restoration of biogeochemical function in mangrove forests. Restoration Ecology 8: 247–259.CrossRefGoogle Scholar
  36. Medina, E., E. Cuevas & A. E. Lugo, 2010. Nutrient relations of dwarf Rhizophora mangle L. mangroves on peat in eastern Puerto Rico. Plant Ecology 207: 13–24.CrossRefGoogle Scholar
  37. Millard, P. & G. H. Neilsen, 1989. The influence of nitrogen supply on the uptake and remobilization of stored N for the seasonal growth of apple trees. Annals of the Botany 63: 301–309.CrossRefGoogle Scholar
  38. Minar, M. H., M. B. Hossain & M. D. Shamsuddin, 2013. Climate change and coastal zone of Bangladesh: vulnerability, resilience and adaptability. Middle-East Journal of Scientific Research 13(1): 114–120.Google Scholar
  39. Motsara, M. R. & R. N. Roy, 2008. Guide to laboratory establishment for plant nutrient analysis. FAO fertilizer and plant nutrition bulletin 19, Food and Agriculture Organization of the United Nations, Rome.Google Scholar
  40. Mulvaney, R. L., 1996. Nitrogen- inorganic forms. In Sparks, D. L. (ed.), Methods of Soil Analysis: Chemical Methods, Part 3. Soil Science Society of America, Madison: 1123–1184.Google Scholar
  41. Murphy, J. & J. P. Riley, 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27: 31–36.CrossRefGoogle Scholar
  42. Mustari, S. & A. H. M. Z. Karim, 2014. Impact of salinity on the socio-environmental life of coastal people of Bangladesh. AJHSS 3(1): 12–18.Google Scholar
  43. Naskar, K. & D. N. G. Bakshi, 1987. Mangrove Swamps of the Sundarbans: An ecological perspective. Naya Prokash, Calcutta.Google Scholar
  44. Noor, T., N. Batoon, R. Mazhar & N. Ilyas, 2015. Effects of siltation, temperature and salinity on mangrove plants. European Academic Research 2(11): 14172–14179.Google Scholar
  45. Osland, M. J., L. C. Feher, K. T. Griffith, K. C. Cavanaugh, N. M. Enwright, R. H. Day, C. L. Stagg, K. W. Krauss, R. J. Howard, J. B. Grace & K. Rogers, 2016. Climatic controls on the global distribution, abundance, and species richness of mangrove forests. Ecological Society of America, Columbus: 1–19.Google Scholar
  46. Roth-Nebelsick, A., D. Uhl, V. Mosbrugger & H. Kerp, 2001. Evolution and function of leaf venation architecture: a review. Annals of Botany 87: 553–566.CrossRefGoogle Scholar
  47. Sack, L., C. Scoffoni, A. D. McKown, K. Frole, M. Rawls, J. C. Havran, H. Tran & T. Tran, 2012. Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications 3: 837.CrossRefGoogle Scholar
  48. Sack, L. & C. Scoffoni, 2013. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198: 983–1000.CrossRefGoogle Scholar
  49. Saenger, P., 2002. Mangrove Ecology, Silviculture and Conservation. Kluwer Academic Publishers, Dordrecht.CrossRefGoogle Scholar
  50. Siddiqi, N. A., 2001. Mangrove Forestry in Bangladesh. Institute of Forestry and Environmental Sciences, University of Chittagong, Chittagong.Google Scholar
  51. Singh, S. P., K. Bargali, A. Joshi & S. Choudhry, 2005. Nitrogen resorption in leaves of tree and shrub seedlings in response to increasing soil fertility. Current Science 89(2): 389–396.Google Scholar
  52. Spalding, M. D., F. Blasco & C. D. Field, 1997. World Mangrove Atlas. The International Society for Mangrove Ecosystems, Okinawa.Google Scholar
  53. Suárez, N. & E. Medina, 2005. Salinity effect on plant growth and leaf demography of the mangrove, Avicennia germinans L. Trees 19: 721–727.CrossRefGoogle Scholar
  54. Timothy, R. P., M. Yoshiaki & M. L. Carol, 1984. A manual of chemical and biological methods for seawater analysis. Pergamon press, Oxford.Google Scholar
  55. Tomlinson, P. B., 1986. The Botany of Mangroves. Cambridge University Press, UK.Google Scholar
  56. Twilley, R. W., A. E. Lugo & C. Patterson-Zucca, 1986. Litter production and turnover in basin mangrove forests in southwest Florida. Ecology 67: 670–683.CrossRefGoogle Scholar
  57. Van-Heerwaarden, L. M., S. Toet & R. Aerts, 2003. Nitrogen and phosphorus resorption efficiency and proficiency in six subarctic bog species after 4 years of nitrogen fertilization. J Ecol 91: 1060–1070.CrossRefGoogle Scholar
  58. Waisel, Y., 1972. Biology of Halophytes. Academic press, New York and London.Google Scholar
  59. Wang, W., Z. Yan, S. You, Y. Zhang, L. Chen & G. Lin, 2011. Mangroves: obligate or facultative halophytes? A review. Trees 25: 953–963.CrossRefGoogle Scholar
  60. Weatherburm, M. W., 1967. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39: 971–974.CrossRefGoogle Scholar
  61. Zhang, J. L., S. B. Zhang, Y. J. Chen, Y. P. Zhang & L. Poorter, 2015. Nutrient resorption is associated with leaf vein density and growth performance of dipterocarp tree species. Journal of Ecology 103: 541–549.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Forestry and Wood Technology DisciplineKhulna UniversityKhulnaBangladesh
  2. 2.Mangrove Silviculture DivisionBangladesh Forest Research InstituteKhulnaBangladesh

Personalised recommendations