Skip to main content

Advertisement

Springer Nature Link
Log in

What happens to soil chemical properties after mangrove plants colonize?

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Understanding soil chemical properties is necessary to characterize the basic properties of ecosystems. In mangrove ecosystems, soil iron, phosphorus, methane and nitrogen have been well studied under field conditions. However, it is difficult to understand fundamental relationships between mangrove root functions and soil chemical properties, because of the multiple factors present in field data. The aim of this study was to clarify what will happen to soil chemical properties after mangrove plant colonize. To examine the effect of mangrove roots on these soil properties, three representative mangrove species (Avicennia marina, Rhizophora stylosa and Bruguiera gymnorrhiza) were cultivated in a greenhouse and selected soil chemical properties were monitored in comparison with those in unplanted soil. We detected oxidative effects in all three species, including deposition of iron oxide on root surfaces, lowered methane concentrations and increased oxidized inorganic nitrogen concentrations in the soil pore-water, suggesting that radial oxygen loss from mangrove roots had affected these soil chemical properties. Besides the oxidative effects, enhanced Fe2+ concentrations in the soil pore-water were present in A. marina, and enhanced phosphorus concentrations in the soil pore-water were present in all three species, suggesting that mangrove roots provide Fe- and phosphate-solubilizing substrates. The most remarkable change was in soil nitrogen enrichment. During the experimental period, amounts of nitrogen in the mangrove soils increased four times more than in uncolonized soil. Six months from the start of cultivation, bacterial nitrogen fixation (nitrogenase activity) was significantly higher in soil colonized by mangrove plants than in uncolonized soil, suggesting that mangrove roots stimulated bacterial nitrogen fixation. Among these properties, Phosphate mobilization and soil nitrogen enrichment are likely to be particularly important for the growth of mangrove plants, because phosphate and nitrogen are generally limited in mangrove ecosystems. This self-supporting ability of mangroves observed in this study could be one key to the high productivity of mangrove ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Alongi DM, Boto KG, Robertson AI (1992) Nitrogen and phosphorus cycles. In: Robertson AI, Alongi DM (eds) Tropical mangrove ecosystems. American Geophysical Union, Washington DC, pp 253–292

    Google Scholar 

  • Alongi DM, Tirendi F, Dixon P, Trott LA, Brunskill GJ (1999) Mineralization of organic matter in intertidal sediments of a tropical semi-enclosed delta. Estuar Coast Shelf Sci 48:451–467

    Article  CAS  Google Scholar 

  • Alongi DM, Wattayakorn G, Boyle S, Tirendi F, Payn C, Dixon P (2004) Influence of roots and climate on mineral and trace element storage and flux in tropical mangrove soils. Biogeochemistry 69:105–123

    Article  CAS  Google Scholar 

  • Alongi DM, Pfitzner J, Trott LA, Tirendi F, Dixon P, Klumpp DW (2005) Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang estuary, Chaina. Estuar Coast Shelf Sci 63:605–618

    Article  CAS  Google Scholar 

  • Bagwell CE, Piceno YM, Ashburne-Lucas A, Lovell CR (1998) Physiological diversity of the rhizosphere diazotroph assemblages of selected salt marsh grasses. Appl Environ Microbiol 64:4276–4282

    PubMed  CAS  Google Scholar 

  • Benner R, Peele ER, Hodson RE (1986) Microbial utilization of dissolved organic matter from leaves of the red mangrove, Rhizophora mangle, in the fresh creek estuary, Bahamas. Estuar Coast Shelf Sci 23:607–619

    Article  CAS  Google Scholar 

  • Biswas H, Mukhopadhyay SK, Sen S, Jana TK (2007) Spatial and temporal patterns of methane dynamics in the tropical mangrove dominated estuary, NE coast of Bay of Bengal, India. J Mar Syst 68:55–64

    Article  Google Scholar 

  • Bodelier PLE, Roslev P, Henckel T, Frenzel P (2000) Stimulation of ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403:421–424

    Article  PubMed  CAS  Google Scholar 

  • Boto KG, Robertson AI (1990) The relationship between nitrogen fixation and tidal exports of nitrogen in a tropical mangrove system. Estuar Coast Shelf Sci 31:531–540

    Article  CAS  Google Scholar 

  • Chauhan R, Ramanathan AL, Adhya TK (2008) Assessment of methane and nitrous oxide flux from mangroves along Eastern coast of India. Geofluids 8:321–332

    Article  CAS  Google Scholar 

  • Cundell AM, Brown MS, Stanford R, Mitchell R (1979) Microbial degradation of Rhizophora mangle leaves immersed in the sea. Estuar Coast Mar Sci 9:281–286

    Article  CAS  Google Scholar 

  • El-Tarabily KA, Youssef T (2010) Enhancement of morphological, anatomical and physiological characteristics of seedlings of the mangrove Avicennia marina inoculated with a native phosphate-solubilizing isolate of Oceanobacillus picturae under greenhouse conditions. Plant Soil 332:147–162

    Article  CAS  Google Scholar 

  • Emerson D, Weiss JV, Megonigal JP (1999) Iron-oxidising bacteria associated with ferric hydroxide precipitates (Fe-plaque) on roots of wetland plants. Appl Environ Microbiol 65:2758–2761

    PubMed  CAS  Google Scholar 

  • Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505

    Article  Google Scholar 

  • Feller IC, McKee KL, Whigham DF, O’Neill JP (2003a) Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62:145–175

    Article  CAS  Google Scholar 

  • Feller IC, Whigham DF, McKee KL, Lovelock CE (2003b) Nitrogen limitation of growth and nutrient dynamics in a mangrove forest, Indian River Lagoon, Florida. Oecologia 134:405–414

    PubMed  Google Scholar 

  • Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorous by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70:107–124

    Article  CAS  Google Scholar 

  • Gilbert B, Frenzel P (1998) Rice roots and CH4 oxidation: the activity of bacteria, their distribution and the microenvironment. Soil Biol Biochem 30:1903–1916

    Article  CAS  Google Scholar 

  • González-Farias F, Mee LD (1988) Effect of mangrove humic-like substances on biodegradation rate of detritus. J Exp Mar Biol Ecol 119:1–13

    Article  Google Scholar 

  • Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    Article  CAS  Google Scholar 

  • Haoliang L, Chongling Y, Jingchun L (2007) Low-molecular-weight organic acids exuded by Mangrove (Kandelia candel (L.) Druce) roots and their effect on cadmium species change in the rhizosphere. Environ Exp Bot 61:159–166

    Article  Google Scholar 

  • Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207

    Article  PubMed  CAS  Google Scholar 

  • Harriss RC, Sebacher DI, Bartlett KB, Bartlett DS, Crill PM (1988) Sources of atmospheric methane in the South Florida environment. Glob Biogeochem Cycles 2:231–243

    Article  CAS  Google Scholar 

  • Hicks B, Silvester W (1985) Nitrogen fixation associated with New Zealand mangrove (Avicennia marina (Forsk.) Vierh. Var. resinifera (Forrsk. f.) Bakl). Appl Environ Microbiol 49:955–959

    PubMed  CAS  Google Scholar 

  • Holguin G, Guzman MA, Bashan Y (1992) Two new nitrogen-fixing bacteria from the rhizosphere of mangrove trees: their isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp. FEMS Microbiol Ecol 10:207–216

    Article  Google Scholar 

  • Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soils 33:265–278

    Article  CAS  Google Scholar 

  • Huang B, Yu K, Gambrell RP (2009) Effects of ferric iron reduction and regeneration on nitrous oxide and methane emissions in a rice soil. Chemosphere 74:481–486

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, Weston LA (2003) Root exudates: an overview. In: de Kroon H, Visser EJW (eds) Root ecology. Springer, Berlin, pp 235–255

    Google Scholar 

  • Inoue T, Nohara S, Takagi H, Anzai Y (2011) Contrast of nitrogen contents around roots of mangrove plants. Plant Soil 339:471–483

    Article  CAS  Google Scholar 

  • King GM, Garey MA (1999) Ferric iron reduction by bacteria associated with the roots of freshwater and marine macrophytes. Appl Environ Microbiol 65:4393–4398

    PubMed  CAS  Google Scholar 

  • Kothamasi D, Kothamasi S, Bhattacharyya A, Kuhad R, Babu C (2006) Arbuscular mycorrhizae and phosphate solubilizing bacteria of the rhizosphere of the mangrove ecosystem of Great Nicobar island, India. Biol Fertil Soils 42:358–361

    Article  Google Scholar 

  • Kreuzwieser J, Buchholz J, Rennenberg H (2003) Emission of methane and nitrous oxide by Australian mangrove ecosystems. Plant Biol 5:423–431

    Article  CAS  Google Scholar 

  • Krishnan KP, Bharathi PAL (2009) Organic carbon and iron modulate nitrification rates in mangrove swamps of Goa, south west coast of India. Estuar Coast Shelf Sci 84:419–426

    Article  CAS  Google Scholar 

  • Krishnan KP, Fernandes SO, Chandan GS, Bharathi PAL (2007) Bacterial contribution to mitigation of iron and manganese in mangrove sediments. Mar Pollut Bull 54:1427–1433

    Article  PubMed  CAS  Google Scholar 

  • Kristensen E, Jensen MH, Banta GT, Hansen K, Holmer M, King GM (1998) Transformation and transport of inorganic nitrogen in sediments of a southeast Asian mangrove forest. Aquat Microb Ecol 15:165–175

    Article  Google Scholar 

  • Kumar T, Ray S, Brahmachary RL, Ghose M (2009) Preliminary GC-MS analysis of compounds present in the root exudates of three mangrove species. Acta Chromatogr 21:117–125

    Article  CAS  Google Scholar 

  • Lee RY, Joye SB (2006) Seasonal patterns of nitrogen fixation and denitrification in oceanic mangrove habitats. Mar Ecol Prog Ser 307:127–141

    Article  Google Scholar 

  • Lovell CR, Piceno YM, Quattro JM, Bagwell CE (2000) Molecular analysis of diazotroph diversity in the rhizosphere of the smooth cordgrass, Spartina alterniflora. Appl Environ Microbiol 66:3814–3822

    Article  PubMed  CAS  Google Scholar 

  • Lovelock CE, Feller IC, McKee KL, Engelbrecht BMJ, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama. Funct Ecol 18:25–33

    Article  Google Scholar 

  • Lovley DR (1995) Microbial reduction of iron, manganese and other metals. Adv Agron 54:175–231

    Article  CAS  Google Scholar 

  • Lugomela C, Bergman B (2002) Biological N2-fixation on mangrove pneumatophores: preliminary observations and perspectives. Ambio 31:7–8

    Google Scholar 

  • Lynch JM, Whipps JM (1991) Substrate flow in the rhizosphere. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 15–24

    Google Scholar 

  • Melillo JM, Naiman RJ, Aber JD, Linkins AE (1984) Factors controlling mass loss and nitrogen dynamics of plant litter decaying in northern streams. Bull Mar Sci 35:341–356

    Google Scholar 

  • Mendelssohn IA, Postek MT (1982) Elemental analysis of deposits on the roots of Spartina alterniflora Loisel. Am J Bot 69:904–912

    Article  Google Scholar 

  • Mortimer RJG, Harris SJ, Krom MD, Freitag TE, Prosser JI, Barnes J, Anschutz P, Hayes PJ, Davies IM (2004) Anoxic nitrification in marine sediments. Mar Ecol Prog Ser 276:37–51

    Article  CAS  Google Scholar 

  • Otero XL, Ferreira TO, Vidal-Torrado P, Macías F (2006) Spatial variation in pore water geochemistry in a mangrove system (Pai Matos island, Cananeia-Brazil). Appl Geochem 21:2171–2186

    Article  CAS  Google Scholar 

  • Paludan C, Morris JT (1999) Distribution and speciation of phosphorus along a salinity gradient in intertidal marsh sediments. Biogeochemistry 45:197–221

    Google Scholar 

  • Pelegrí SP, Twilley RR (1998) Heterotrophic nitrogen fixation (acetylene reduction) during leaf-litter decomposition of two mangrove species from south Florida, USA. Mar Biol 131:53–61

    Article  Google Scholar 

  • Pelegrí SP, Rivera-Monoroy VH, Twilley RR (1997) A comparison of nitrogen fixation (acetylene reduction) among three species of mangrove litter, sediments, and phneumatophores in south Florida, USA. Hydrobiologia 356:73–79

    Article  Google Scholar 

  • Penha-Lopes G, Kristensen E, Flindt M, Mangion P, Bouillon S, Paula J (2010) The role of biogenic structures on the biogeochemical functioning of mangrove constructed wetlands sediments—A mesocosm approach. Mar Pollut Bull 60:560–572

    Article  PubMed  CAS  Google Scholar 

  • Pi N, Tam NFY, Wu Y, Wong MH (2009) Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquat Bot 90:222–230

    Article  Google Scholar 

  • Pi N, Tam NFY, Wong MH (2010) Effects of wastewater discharge on formation of Fe plaque on root surface and radial oxygen loss of mangrove roots. Environ Pollut 158:381–387

    Article  PubMed  CAS  Google Scholar 

  • Prasad MBK, Ramanathan AL (2010) Characterization of phosphorus fractions in the sediments of a tropical intertidal mangrove ecosystem. Wetlands Ecol Manag 18:165–175

    Article  Google Scholar 

  • Purvaja R, Ramesh R (2001) Natural and anthropogenic methane emission from coastal wetlands of South India. Environ Manag 27:547–557

    Article  CAS  Google Scholar 

  • Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30:1148–1160

    Article  PubMed  CAS  Google Scholar 

  • Robertson AI (1988) Decomposition of mangrove leaf litter in tropical Australia. J Exp Mar Biol Ecol 116:235–247

    Article  Google Scholar 

  • Roden EE, Wetzel RG (1996) Organic carbon oxidation and suppression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments. Limnol Oceanogr 41:1733–1748

    Article  CAS  Google Scholar 

  • Snowden RED, Wheeler BD (1995) Chemical changes in selected wetland plant species with increasing Fe supply, with specific reference to root precipitates and Fe tolerance. New Phytol 131:503–520

    Article  CAS  Google Scholar 

  • Sotomayor D, Corredor JE, Morrell JM (1994) Methane flux from mangrove sediments along the southwestern coast of Puerto-Rico. Estuaries 17:140–147

    Article  CAS  Google Scholar 

  • Spalding M, Kainuma M, Collins L (2010) World atlas of mangrove. Earthscan, London

    Google Scholar 

  • Stoltzfus JR, So R, Malarvithi PP, Ladha JK, de Bruijn FJ (1997) Isolation of endophytic bacteria from rice and assessment of their potential for supplying rice with biologically fixed nitrogen. Plant Soil 194:25–36

    Article  CAS  Google Scholar 

  • Strangmann A, Bashan Y, Giani L (2008) Methane in pristine and impaired mangrove soils and its possible effect on establishment of mangrove seedlings. Biol Fertil Soils 44:511–519

    Article  CAS  Google Scholar 

  • Taylor GJ, Crowder AA (1983) Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70:1254–1257

    Article  CAS  Google Scholar 

  • Twilley RR, Lugo AE, Pattersonzucca C (1986) Litter production and turnover in basin mangrove forests in south west Florida. Ecol 67:670–683

    Article  Google Scholar 

  • Van Bodegom P, Goudriaan J, Leffelaar P (2001) A mechanistic model on methane oxidation in a rice rhizosphere. Biogeochemistry 55:145–177

    Article  Google Scholar 

  • Vazquez P, Holguin G, Puente ME, Lopez-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    Article  CAS  Google Scholar 

  • Yang SS, Chang HL (1998) Effects of environmental conditions on methane production and emission from paddy soil. Agric Ecosyst Environ 69:69–80

    Article  CAS  Google Scholar 

  • Zuberer DA, Silver WS (1978) Biological dinitrogen fixation (acetylene reduction) associated with Florida mangroves. Appl Environ Microbiol 35:567–575

    PubMed  CAS  Google Scholar 

  • Zuberer DA, Silver WS (1979) N2-fixation (acetylene reduction) and the microbial colonization of mangrove roots. New Phytol 82:467–471

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ms. S. Matsumoto for her assistance with laboratory measurements. We also thank Mr. M. Hashizume and Mr. T. Takagi for their comments and advice. This work has been partly supported by a Grant-in-Aid for Young Scientist (B) (No. 20770020) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of the Japanese Government.

Author information

Authors and Affiliations

  1. National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki, 305-8506, Japan

    Tomomi Inoue & Seiichi Nohara

  2. Kawakami Farm, 4041 Owari, Tsukubamirai, Ibaraki, Japan

    Katsumi Matsumoto

  3. 1-4-2 Azuma, Tsukuba, Ibaraki, 305-0031, Japan

    Yasuharu Anzai

Authors
  1. Tomomi Inoue
    View author publications

    Search author on:PubMed Google Scholar

  2. Seiichi Nohara
    View author publications

    Search author on:PubMed Google Scholar

  3. Katsumi Matsumoto
    View author publications

    Search author on:PubMed Google Scholar

  4. Yasuharu Anzai
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Tomomi Inoue.

Additional information

Responsible Editor: Katja Klumpp.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Inoue, T., Nohara, S., Matsumoto, K. et al. What happens to soil chemical properties after mangrove plants colonize?. Plant Soil 346, 259–273 (2011). https://doi.org/10.1007/s11104-011-0816-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-0816-9

Keywords