Soil and Mangroves

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    REGULAR ARTICLE

    What happens to soil chemical properties after mangrove

    plants colonize? Tomomi Inoue   & Seiichi Nohara   &

    Katsumi Matsumoto   & Yasuharu Anzai

    Received: 17 September 2010 /Accepted: 2 May 2011 /Published online: 21 May 2011 # Springer Science+Business Media B.V. 2011

    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 man-

    grove 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 oxi-

    dized 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 (nitro-

    genase 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.

    Keywords   Mangrove . Root . Soil chemicals . Iron .

    Phosphorus . Nitrogen . Methane

    Plant Soil (2011) 346:259–273

    DOI 10.1007/s11104-011-0816-9

    Responsible Editor: Katja Klumpp.

    T. Inoue (*) : S. Nohara 

     National Institute for Environmental Studies,

    16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan

    e-mail: tomomi.inoue@nies.go.jp

    K. Matsumoto

    Kawakami Farm,

    4041 Owari,

    Tsukubamirai, Ibaraki, Japan

    Y. Anzai

    1-4-2 Azuma,

    Tsukuba, Ibaraki 305-0031, Japan

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    Introduction

    This study focused on mangrove plants that form

    highly productive ecosystems in coastal areas of 

    tropical and subtropical regions. For several decades,

    areas of mangroves have continuously declined

    around the world, despite their important ecosystem role (Spalding et al.   2010). To characterize these

     productive ecosystems and provide scientific guide-

    lines for their conservation, knowledge of their soil

    chemical properties is necessary, because these

     properties are the basis of the ecosystems.

    When plant seeds germinate and start to grow, soil

    chemical properties are affected. It is known that 

     plants excrete a variety of substrates that facilitate the

    availability of macro- and micronutrients in the

    rhizosphere, by enhancing absorption of appropriate

    nutrients even under nutrient deficient conditions. For  instance, organic acids exuded from plant roots, such

    as citrate and malate, are known to mobilize P from

    sparingly soluble Fe, Al and Ca phosphates (Gardner 

    et al.   1983). Therefore, greater amounts of nutrients

    such as P and Fe are sometimes observed in the plant 

    root zone compared with the bulk soil (Inderjit and

    Weston   2003). Besides root exudates, plant roots

    continuously provide organic matter such as decaying

    root parts. These organic matter-rich root zones are

    different from the bulk soil and provide niches in

    which bacteria thrive (Lynch and Whipps   1991),  because heterotrophic bacteria can use these plant-

    derived carbon compounds as electron donors to

    generate energy. Therefore, soil microbial metabolic

     processes also change in association with plant 

    colonization. In addition to the above mentioned root 

    functions, radial oxygen loss may be an important 

    characteristic factor in mangrove root zones. Coastal

    habitats for mangroves are always affected by tidal

    fluctuation, and thus, the soil surface is repeatedly

    flooded. To cope with the hypoxia in root cells, most 

    mangrove species develop oxygen transporting mech- anisms and an aerial root system. This allows

    atmospheric oxygen to diffuse towards root tips

    through internal lacunae (a gas – space continuum).

    Supplied oxygen is partially utilized for aerobic

    respiration of the roots, and the rest diffuses towards

    the rhizosphere via the root surface. This results in the

    formation of a thin oxidative layer around the oxygen-

    releasing root surface and affects soil microbial

     processes. Radial oxygen loss from mangrove plant 

    root has been detected in  Avicennia marina  (Forsk.)

    Vierh.,   Kandelia obovata,   Lumnitzera racemosa

    Willd,   Bruguiera gymnorrhiza   (L.) Lam., and

     Excoecaria agallocha   L. (Pi et al.   2009,   2010). So

    far, the following four soil chemical properties, iron,

     phosphorus, nitrogen and methane have been com-

     paratively well studied in mangroves growing in rooted soil.

    Iron is basically found as Fe(II)/Fe(III) oxide com-

     plexes in soil. Ferrous ion (Fe2+) is released by

    chemical reduction under conditions of low redox

     potential and/or chelation with organic acids. There are

    some reports that concentration of ferrous ion (Fe2+) in

    mangrove soil pore water is positively correlated with

    live root density (Alongi et al.  1999, 2005; Otero et al.

    2006). These observations indicate that mangrove roots

    lead to enhanced Fe mobilization. On the other hand,

    Pi et al. (2010) reported that they observed iron oxide deposition on the root surface in two mangrove

    species,   B. gymnorrhiza   and   E. agallocha, probably

     because of oxygenation by oxygen-releasing roots.

    Mangrove roots thus may form Fe2+-Fe(III) oxide

    contrasts in the rhizosphere.

    Phosphorus has been well studied, probably

     because it is one of the most limiting elements in

    mangrove ecosystems (Feller et al.   2003a ,   b;

    Lovelock et al. 2004; Reef et al.  2010). In mangrove

    soils, phosphorus tends to be adsorbed on Fe/Al-

    oxides, Ca compounds and polymerized organic matter (Paludan and Morris   1999; Prasad and

    Ramanathan   2010). The immobilized phosphorus

    cannot be used by plants unless it is released by

     phosphate solubilizing bacteria and/or chelation with

    organic acids. So far, phosphate-solubilizing bacteria 

    have been detected in three mangroves,   A. marina,

     Avicennia germinans   (L.) Stearn, and   Laguncularia

    racemosa   (L.) Gaertn. f. (Vazquez et al.   2000;

    Kothamasi et al.   2006; El-Tarabily and Youssef 

    2010), but resultant phosphate mobilization in the

    rhizosphere has not yet been measured.  Nitrogen is another limiting element in mangrove

    ecosystems (Feller et al.   2003a ,   b; Lovelock et al.

    2004; Reef et al. 2010). Coastal habitats for mangrove

     plants are always exposed to tidal fluctuation, and

    thus nitrogen is continuously exported to the ocean

    (Boto and Robertson   1990). Under such circum-

    stances, bacterial nitrogen fixation is a major nitrogen

    input process in mangrove ecosystems (Hicks and

    Silvester  1985). High nitrogen fixing activity has been

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    found associated with mangrove sediments, dead

    leaves, and cyanobacterial mats covering sediment 

    surfaces (Zuberer and Silver   1979; Hicks and

    Silvester   1985; Holguin et al.   2001; Lugomela and

    Bergman   2002). These observations suggest a rela-

    tionship between nitrogen fixers and mangrove

    growth. However nitrogen fixers are also found in many other systems, including terrestrial and marine

    ecosystems, and it has not yet been confi