Soil and Mangroves

8/19/2019 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 rootson 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: [email protected]

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 ecosystemrole (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 inrooted 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 oxidedeposition 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 organicmatter (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

260 Plant Soil (2011) 346:259–273


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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 inmany other systems, including terrestrial and marine

ecosystems, and it has not yet been confirmed

whether the high nitrogen fixation is partly attributed

to mangrove plant growth or not. Besides nitrogen

fixation, oxygen-releasing roots may promote the

nitrification process. In mangrove ecosystems in

Thailand, higher nitrate concentrations in soil pore-

water in an area vegetated by the mangrove Rhizo-

phora apiculata Bl. than in an unvegetated area have

been found (Kristensen et al. 1998).

Methane production in mangrove ecosystems has been studied because it is one of the most significant

greenhouse gases. Although there are many studies

measuring the amount of methane produced in

mangrove soils (Sotomayor et al. 1994; Purvaja and

Ramesh 2001; Alongi et al. 2004; Biswas et al. 2007),

mangrove root effects on methane production have

not yet been studied. In herbaceous wetland plants,

oxidation of methane to carbon dioxide around

oxygen-releasing roots has been reported (Gilbert

and Frenzel 1998; Bodelier et al. 2000). Oxygen-

releasing mangrove roots may also have such a methane-consuming effect.

As discussed above, information on soil chemical

properties is available from previous field studies.

However, it is difficult to interpret inter-relationships

between mangrove root functions and soil chemical

properties from field data, because the data reflect

multiple factors. From field observations, we hypoth-

esized that (a) oxygen-releasing mangrove roots

would have iron oxide deposition on their surfaces,

promote nitrification process in the soil pore water

and decrease methane concentrations in soil porewater, (b) mangrove roots would enhance Fe and P

mobilization and (c) mangrove roots would stimulate

soil bacterial N-fixation. The aim of this study was to

confirm these hypotheses in three representative

mangrove species ( A. marina, Rhizophora stylosa

Griff., and B. gymnorrhiza). To eliminate external

factors (e.g. tidal fluctuations, precipitation and

intrusion of chemical entities from the surrounding

area) and focus on mangrove root effects on soil

chemical properties, we cultivated the three man-

groves in a pot system under greenhouse conditions

and monitored soil iron, phosphorus, nitrogen and

methane values for 180 days in comparison with

those values in unplanted soil.

Materials and methods

Plant materials and cultivation

Plant cultivation was conducted under full sunlight

conditions in a greenhouse (27°C air temperature,

70% humidity). Propagules of each mangrove species

were randomly collected from more than 30 different

mature trees in mangrove forest located at Kabira Bay

in north-west Ishigaki, Japan (24°26′52″ N, 124°08′

03″

E) during the relevant fruiting season; September for A. marina, July for R. stylosa and January for B.

gymnorrhiza. The mean dry weights of the propagules

were 0.96±0.09 in A. marina, 7.37±1.77 in R .stylosa

and 4.18±1.32 g in B. gymnorrhiza (mean ± SD, N =

20). The lower part (5 cm for R. stylosa and B.

gymnorrhiza, 1 cm for A. marina) of each propagule

was buried in the sediment in plastic pots (159 mm

diameter, 190 mm depth) and flooded with 25%

instant sea water (Marin Merit, Matsuda, Ltd., Osaka,

Japan) to 10 cm above the soil surface. After being

cultured for 2 years, 40 healthy plants for each specieswere selected and individually transplanted into

separate plastic pots (250 mm diameter, 450 mm

depth) filled with 15 L (27.5 kg dry weight) of soil.

For each species, the transplanting was performed

exactly 2 years after the collection of propagules. At

transplanting, the height and leaf number of each

species was, respectively, 48.4±5.3 cm and 74±8 in

A. marina, 55.3±5.6 cm and 22±0 in R. stylosa and

62±4.8 cm and 18±0 in B. gymnorrhiza, (mean ± SD,

N =40). Another 40 pots without plants were prepared

as control treatments. The soil used for the cultivationwas a mixture of commercial potting compost and

sand (1:2 by volume). The soil texture was a sandy

loam and the organic matter content of the soil was

1.2%. The total nitrogen and sulfur concentrations of

the soil were determined as 5.0 and 40.0 mg g dry

weight −1, respectively by an elemental analyzer

(Flash EA 1112, Thermo Fisher Science, Waltham,

USA). Concentrations of the total forms of other

elements in the soil were P: 20.0, K: 6.0, Al: 60.0, Ca:

Plant Soil (2011) 346:259–273 261


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200.0: Fe: 10.0, Mg: 30.0 mg g dry weight −1

determined by an inductively coupled plasma atomic

emission spectrometer (ICP-JA, Nippon Jarrell-Ash,

Kyoto, Japan), following digestion by a mixture of

sulfuric, nitric and perchloric acids. The cultivation

experiment was run for 180 days. All pots were

maintained in the greenhouse under similar growthconditions of a 10 cm flooding depth with 25% sea

water. The water level of each pot was monitored

daily and readjusted for evaporation by addition of

water. The salinity of the flooded water was also

monitored daily by an electrode sensor (WM-22EP,

HORIBA, Kyoto, Japan) and readjusted within ±1%.

Thirty days from the start of the experiment, the pH

and redox potential in the control pots were 6.8±0.2

and 65.3±3.5 mv (mean ± SD, N =40), respectively.

For each species, 10 pots were randomly selected at

30, 60, 120, and 180 days from the start of theexperiment and chemical properties of the soil pore-

water, soil and plant material were measured.

Soil pore-water, soil and plant material

To collect soil pore-water, a water sampling tube was

inserted into each pot at the start of the experiment.

The water sampling tube comprised three parts: (a) an

unglazed tube (2 mm diameter, 10 cm length); (b) a

Teflon-lined tube (2 mm diameter, 30 cm length); and

(c) a hollow needle. The unglazed tube was buried inthe sediment at 10 – 20 cm depth. When collecting soil

pore-water, the needle was inserted into the silicon lid

of the vacuum-sealed glass vessels, and soil pore-

water was drawn into the vessel. The first 2 ml of

water was discarded with the next 35 ml immediately

filtered through a 0.2-μ m mesh filter (DISMIC-25cs,

cellulose Acetate, ADVANTEC, Tokyo, Japan) with a

plastic syringe (ss-30ESZ, TERUMO, Tokyo, Japan)

to remove bacteria. Twenty milliliters of the sampled

water was used to measure dissolved NH4+, NO2

−,

NO3−

and phosphate, by an auto-analyzer (AACS-II,Bran+Luebbe, Norderstedt, Germany). Another 10 ml

of the sampled water was used for CH4 measurement.

The sampled water was transferred to 30 ml

sterilized glass vials and sealed with Teflon-silicon

septa. The vials were kept at 27°C in a water bath

(NTS-4000B, Tokyo Rikakikai, Tokyo, Japan).

Methane concentrations in the head space of the

glass vials were determined by a gas chromatograph

equipped with a Por apak Q column and FID

detector (GC-4000, GL Science, Tokyo, Japan).

The remaining 5 ml of the sampled water was used

for Fe2+ measurement. After filtering, 5 ml of

10 mM o-phenanthroline hydrochloride (Wako Pure

Chemical Industries, Ltd, Osaka, Japan) and 5 ml of

sodium acetate buffer solution (pH=5.5) were im-

mediately added to the water samples. The peak absorbance at 510 nm of the Fe2+-phenanthroline

complex was determined by a UV/visible spectro-

photometer (U1000, Hitachi, Tokyo, Japan).

After completion of water sampling, 50 ml of soil

(92 g dry weight) was collected from around the

submerged unglazed tube using a core sampler (2.5 cm

diameter, 10 cm height). The soils were dried at room

temperature and their nitrogen concentrations deter-

mined by the elemental analyzer. Each sample was

measured three times and the mean value determined.

At 60, 120 and 180 days from the start of theexperiment, the dry weights of roots, aboveground

parts and leaf litter in each pot were measured after

oven-drying at 80°C for 72 h. Plant material nitrogen

concentrations were measured by the elemental

analyzer after fine grinding. Each sample was

measured three times and the mean value determined.

The relative growth rate (RGR) and the nitrogen

use efficiency (NUE) of the plants were calculated as

follows:

RGR ¼ ln W

f ln W

i

Δt ; ð1Þ

NUE ¼ W f W i N f N i

; ð2Þ

where Wi (g) and Wf (g) are the total dry weights at

the beginning (30 days) and end (180 days) of the

experiment, respectively, and Δt (days) is the growth

period (150 days). Ni (g) and Nf (g) are the amount of

nitrogen contained in plant material at the beginning

and end of the experiment, respectively.The amounts of nitrogen in each pot were

calculated as follows:

N j ¼ n j W tj ; ð3Þ

Where N j (g) is the amount of nitrogen contained in j

in each pot (j = soil, water, plant, litter), n j (Ng g−1) is

the nitrogen content of j and Wtj (g) is the weight of j

in each pot at t days from the start of the experiment

(t =30, 60, 90, 150 days).

262 Plant Soil (2011) 346:259–273


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Root Fe plaques

At 60, 120 and 180 days from the start of the

experiment, the amount of iron oxide deposition on

plant root surfaces caused by oxygen release from the

roots was determined by the cold DCB (dithionite

citrate bicarbonate) technique (Taylor and Crowder 1983). Fresh fine roots (corresponding to approxi-

mately 0.5 g dry weight) collected from each plant

were agitated in 45 ml of DCB reagent at 20°C for

3 h, and the wash collected. The roots and beaker

were rinsed into the wash with deionized water. The

resulting solution was made to 100 ml and the iron

concentration was determined by an inductively

coupled plasma atomic emission spectrometer (ICP-

JA, Nippon Jarrell-Ash, Kyoto, Japan). Roots used for

measurement were less than 2 mm in diameter.

Nitrogenase activity

At the end of the experiment (180 days), soil nitrogen

fixation was indirectly assessed by the acetylene reduc-

tion technique (Hardy et al. 1968). A 5-ml soil core

(1 cm diameter, 5 cm height) from 1 – 6 cm soil depth in

each pot was transferred to a 50-ml glass vial together

with 5 ml of the water contained in the pot. Two vial

sets were prepared for each pot. The vials were purged

with argon to provide an anoxic atmosphere and sealed

with Teflon-silicon septa. For one of the vial sets, 4 mlof the gas phase was evacuated and replaced with 4 ml

of acetylene through the Teflon-silicon septa. The other

vial was used as a control and incubated without

addition of acetylene to test the endogenous production

of ethylene. The vials were shaken in the dark at 30°C

in a water bath and 0.2 ml of the gas phase was sampled

at 0.3, 3, 6 and 9 h after the acetylene injection.

Ethylene concentrations in the gas samples were

determined by the gas chromatograph equipped with a

Porapak N column and FID detector (GC-4000, GL

Science Inc., Tokyo, Japan). Nitrogenase activity wasdetermined from the accumulation of ethylene in the

vials with time, using linear regression analysis. A

similar procedure was used for fresh root materials to

determine the activity of nitrogen fixers on the roots.

Data analysis

In this study, 10 randomly selected pots from each

mangrove species were used for measurements on each

sampling day and then discarded to avoid pseudo-

replicates. For each variable (Fe2+, CH4, PO43−, NO2

−,

NO3−, NH4

+, soil N content and plant N content),

mean values of the 10 pots were calculated at each

sampling day. Two-way analysis of variance (ANOVA)

was used to test the effects of mangrove species, days

elapsed from mangrove colonization and interactions between both on soil chemical properties and plant N

content. Differences among treatments means were

compared and tested for significance at the p


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species, B. gymnorrhiza showed the lowest Fe2+

concentration at the end of the experiment.

After 30 days from colonization, the three

mangrove species enhanced dissolved phosphate

ion concentrations in the soil pore-water (Fig. 1c).

The degree of enhancement was significantly higher

in A. marina than in the other two species. At the endof the experiment, phosphate ion concentrations

were 89, 95 and 304% higher in R. stylosa, B.

gymnorrhiza and A. marina compared with the

control, respectively. Although the greatest enhance-

ment was observed in A. marina, the concentration

curve reached saturation 120 days after plant

colonization and mean values did not significantly

differ between then and 180 days.

The three mangrove species lowered methane

concentrations in the soil pore-water (Fig. 1d). In

the control pots, the CH4 concentration graduallyincreased with elapsed time. At the end of the

experiment, CH4 concentrations in the soil pore water

were 24, 30 and 35% lower in R. stylosa, A. marina

and B. gymnorrhiza than in the control, respectively.

Nitrogen

Changes in the amounts of nitrogen with time are

shown in Fig. 2. Although soil nitrogen in the control

pots gradually decreased with elapsed time, it rapidly

increased in the mangrove planted pots between 120and 180 days after colonization (Fig. 2a ). At the end

of the experiment, the amounts of nitrogen contained

in the soil were 294, 329 and 338% higher in A.

marina, R. stylosa and B. gymnorrhiza pots than in

the control, respectively. In all mangrove colonized

pots, inorganic nitrogen dissolved in the soil pore-

water started to decrease between 30 and 60 days after

colonization, while the control pots maintained their

initial value throughout the experiment (Fig. 2b). At

Table 1 ANOVA results for soil chemical properties in the

cultivated pots, showing degrees of freedom (d.f.), F -value (F)

and probability under a null model ( P )

d.f. F P

[Fe2+] in soil pore-water

Treatment 3 24.2 0.000

Days 2 21.6 0.000

Treatment × Days 6 6.1 0.000

Fe plaque on root surface


Days 2 41.7 0.000


Phosphate in soil pore-water


Days 3 35.8 0.000


[CH4] in soil pore-water Treatment 3 20.6 0.000

Days 2 16.7 0.000


Soil N content


Days 3 173.8 0.000


Inorganic N in soil pore-water

Treatment 3 126.1 0.000

Days 3 71.0 0.000


Plant N content


Days 2 170.6 0.000


Litter N content

Treatment 2 198.7 0.000

Days 3 369.7 0.000


[NO2−] in soil pore-water


Days 3 15.3 0.000


[NO3−] in soil pore-water


Days 3 34.0 0.000


[NH4+

] in soil pore-water

Treatment 3 128.1 0.000

Table 1 (continued)

d.f. F P

Days 3 72.6 0.000


The effects of treatment (planted by A. marina, R. stylosa, B.

gymnorrhiza or control), elapsed time since colonization (30,

60, 120, 180 days), and both interactions on soil chemical

properties in the cultivated pots were tested by two-way

ANOVA. Values with P


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the end of the experiment, the amount of nitrogen

contained in the soil pore-water was 98, 99 and 99%

lower in R. stylosa, A. marina and B. gymnorrhiza

pots than in the control pots, respectively. During the

experimental period, most of the inorganic nitrogen in

the soil pore-water was present as the ammonium ion,

NH4+ (Fig. 3c), and thus the change in NH4

+

concentration with time was of a very similar form

to that of total N (NO2−+NO3

−+NH4+) (Figs. 2 b and

3c). At the end of the experiment, NH4+ concentration

was 84, 95 and 98% lower in R. stylosa, A. marina

and B. gymnorrhiza pots than in the control pots,

0 60 120 1800

2

4

6

F e r r o u s

i o n

( m g

L - 1 )

60 120 180

0

10

20

30

40

50

0

no data

M e

t h a n e

( µ m o

l L - 1 )

0

2

4

6

0 60 120 180

no data

a

bbb

a

b

c

bc

R o o

t F e p

l a q u e

( µ g F e g r o o

t d r y w e

i g h t -

1 )

0

4

8

12

16

0 60 120 180

no data

a

b

b

a

bb

c

A. marina

R. stylosa

B. gymnorrhiza

Control

P h o s p

h a t e

i o n

( µ g

P L - 1 )

no data

no data

a

bb

c

a

b

c

d

Fig. 1 Periodic changes in a amount of iron oxide plaque on

root surfaces, b Fe2+ concentration in the soil pore-water, c

phosphate ion concentrations in the soil pore-water and d CH4concentrations in the soil pore-water. Results are expressed as

mean ± standard error (n =10). Different letters indicate

significant differences ( p


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respectively. In contrast, the three mangrove species

enhanced concentrations of the oxidized forms of

nitrogen, nitrite and nitrate, in the soil pore-water

compared with the control pots (Fig. 3a, b). Both

NO2− and NO3

− concentrations increased between 30

and 60 days after plant colonization, but remainedlargely unchanged thereafter. At the end of the

experiment, NO2− concentrations were 79, 99 and

123% higher in R. stylosa, A. marina and B.

gymnorrhiza than in the control pots, respectively,

while concentrations of NO3− were 20, 55 and 55%

higher in A. marina, R. stylosa and B. gymnorrhiza

than in the control pots, respectively.

During the experimental period, the amounts of

nitrogen contained in the biomass of all three

mangrove plant materials increased as the plants grew

(Fig. 2c). Among the three species, nitrogen concen-

trations in aboveground material were highest in A.

marina followed by R. stylosa and B. gymnorrhiza

(Fig. 4). For belowground material, the nitrogen

concentration was basically higher in R. stylosa than

in B. gymnorrhiza while values for A. marinafluctuated. For all three species, nitrogen concentra-

tions were higher in aboveground than belowground

parts, as were biomass dry weights (Table 1). Be-

tween 120 and 180 days after colonization, all three

species began to supply leaf litter on the soil surface

(Fig. 2d). Dry weights of litter were highest in A.

marina, followed by R. stylosa and B. gymnorrhiza;

1.32±0.07, 0.53±0.06 and 0.41±0.04 g, respectively

(mean ± SE, N =10). The carbon to nitrogen ratio C/N

(g g−1) of the litter was highest in A. marina, followed

by R. stylosa and B. gymnorrhiza (Fig. 5). The C/Nratio of litter was significantly lower than that in the

aboveground parts of A. marina, while the other two

species had higher C/N ratios in the litter.

Nitrogenase activity

At the end of the experiment, soil nitrogenase activity

significantly differed among the treatments (Fig. 6).

Mangrove colonization enhanced soil nitrogenase

activity with values being 16, 33 and 176 times

higher in A. marina, R. stylosa and B. gymnorrhiza pots than in control pots, respectively. Root materials

of the three mangrove plants also showed nitrogenase

activity (Fig. 6). Compared on a volume basis,

nitrogenase activity of mangrove root materials was

significantly higher than in the control soil. In A.

marina, nitrogenase activity was higher in the soil

than in root materials, while there were no significant

differences between soil and root materials in R.

stylosa and B. gymnorrhiza.

Plant growth and nitrogen use efficiency

Thirty days after the start of the experiment, the three

mangrove species had similar total biomass dry

weights (Table 1). During the following 150 days,

the biomass of A. marina and R. stylosa increased to

about twice that at 30 days, while that of B.

gymnorrhiza increased about three times (Table 2).

As a result, the relative growth rate was significantly

higher in B. gymnorrhiza than in A. marina and R.

60 120 180

60 120 180

60 120 180

0

N i t r i t e i o n

( µ g N L - 1 )

0.5

1.0

1.5

2.0

N i t r a t e i o n

( µ g N L - 1 )

0

2.5

2.0

1.5

1.0

0.5

A m m o n i u m i o n

( m g N L - 1 )

0

0.8

0.6

0.4

0.2

days

aaa

b

aa

b

c

a

bcc

B. gymnorrhiza

A. marina

R. stylosa

Control

a

b

c

Fig. 3 Periodic changes in inorganic nitrogen concentrations; a NO2

−, b NO3− and c NH4

+ dissolved in the soil pore-water.

Results are expressed as mean ± standard error (n =10).

Different letters indicate significant differences ( p


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stylosa ( P


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(nitrite and nitrate) in the soil pore-water. According

to model studies of rice plant roots, most of the

oxygen released from the roots will be consumed by

the chemical oxidation of Fe2+, while the rest will be

consumed by aerobic heterotrophs (Van Bodegom et al. 2001). In flooded soil, the reduced ferrous iron,

Fe2+, tends to accumulate and this will be chemically

oxidized to Fe(III) (hydroxyl) oxide precipitates on

oxygen-releasing root surfaces. Reddish brown col-

ored iron oxide plaques covering wetland herbaceous

plant root surfaces have been observed in many

studies (Snowden and Wheeler 1995; Emerson et al.

1999; King and Garey 1999). In mangrove plants,

iron oxide plaque has been detected in two species, B.

gymnorrhiza and E. agallocha (Pi et al. 2010). This

study found that A. marina and R. stylosa can alsoform iron oxide plaque on their root surfaces

(Fig. 1a ). Even in the same plant species, the amount

of plaque fluctuates due to several factors, such as

root oxidizing ability and availability of Fe2+ in the

soil. For example, Mendelssohn and Postek (1982)

reported that amounts of root iron oxide plaque of

Spartina alterniflora varied from 32 μ g g−1 root dry

weight in inland areas to 1,648 μ g g−1 root dry weight

in stream side areas. Therefore, plaque on mangrove

plant roots would also be expected to fluctuate

according to the habitat and plant conditions. In thisstudy, A. marina rapidly increased its root iron oxide

plaque after 120 days from the start of the experiment.

The three species all began to produce aerial roots at

this time (data not shown): pneumatophores for A.

marina, prop roots for R. stylosa and knee roots for B.

gymnorrhiza. The great enhancement of iron oxide

plaque in A. marina after 120 days might be due to

the development of the effective pneumatophore

aerial root system. Furthermore, Fe2+ concentration

in soil pore-water increased remarkably after A.

marina colonization (Fig. 1b). This high availability

of Fe2+ might be another reason for the high

accumulation of iron oxide plaque on roots. Although

we measured iron oxide plaque using young fine roots(


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may be unsuitable for methanogenesis. In this study,

we observed gradually increased methane concentra-

tions with elapsed time in control pots (Fig. 1d). This

suggests that the redox potential gradually decreased

in soil uncolonized by mangroves. Furthermore, high

production of Fe(III)-oxides on root surfaces stim-

ulates bacterial Fe(III) reduction, because Fe(III)-reducing bacteria can use Fe(III)-oxides as electron

acceptors to oxidize organic compounds (Lovley

1995). This microbial Fe(III)-oxide reduction may

possibly suppress methanogenesis and sul fate-

reducing bacteria, because these processes compete

for the same carbon in the root zone (Roden and

Wetzel 1996; Biswas et al. 2007; Huang et al. 2009).

The low methane concentrations in mangrove pots

observed in this study might be attributed to the

resultant combination of enhanced bacterial methane

oxidization, lowered methanogenesis and competitionwith Fe(III)-reducing bacteria in the oxidized rhizo-

sphere. The contribution of each process would vary

depending on many factors, including the amount

of nutrient input and plant growth condition.

Recently, it has been reported that human impacts,

such as inputs of high nutrient loadings from

sewage, aquaculture and agriculture, could be

contributing to enhanced methane production in

mangrove ecosystems (Kreuzwieser et al. 2003;

Alongi et al. 2005; Strangmann et al. 2008; Chauhan

et al. 2008; Penha-Lopes et al. 2010).For inorganic nitrogen, the reduced form of NH4

+

tends to be abundant in anaerobic soils. The presence

of oxygen will lead to oxidation of NH4+ to NO2

− by

ammonia oxidizing bacteria, and the NO2− is then

continuously oxidized to NO3− by nitrite oxidizing

bacteria. Results of this study suggest that the roots of

the three mangrove species also possess the ability to

change nitrogen metabolism in rooted soil to produce

NO2− and NO3

− (Fig. 3a, b). In addition to the aerobic

autotrophic nitrification process, recent studies have

suggested the possibility of anaerobic autotrophicnitrification at the expense of electron acceptors such

as Fe and/or Mn (Mortimer et al. 2004; Krishnan et al.

2007). Krishnan and Bharathi (2009) reported that the

nitrification rate in mangrove sediments showed a

positive relationship with Fe (contained in the

sediment) and with the abundance of autotrophic

nitrifiers. Accumulation of iron oxide plaque on the

root surface observed in this study might also

contribute to anaerobic autotrophic nitrification. The

resultant NO2− and NO3

− will be converted to

gaseous N2 and/or N2O (denitrification) that will

diffuse to the atmosphere. Besides denitrification,

assimilation by bacteria and absorption by plant roots

may also contribute to decreased NO2− and NO3

−

concentrations in the soil pore-water. In this study,

concentration curves of NO2−

and NO3−

seemed to besaturated 60 days from plant colonization. This

suggests that the combination of input (nitrification)

and output (denitrification, bacterial assimilation and

plant absorption) processes had reached steady state.

Although the concentrations of NO2− and NO3

− seem

to have reached steady state 60 days from plant

colonization, NH4+ concentrations decreased remark-

ably for the first 120 days from plant colonization

(Fig. 2b). Such a low NH4+ concentration in soil pore-

water is consistent with field observations (within the

μ M range) in tropical mangrove forests (Alongi et al.1992). In our previous field study, we also observed

lower inorganic nitrogen concentrations in soil pore-

water in the root zone of the three mangroves

compared with areas having no roots (Inoue et al.

2011). In the field study, production of NO2− and

NO3− in the root zone was also detected as found

here. In this study, relatively lower NO2− concen-

trations in A. marina compared with those in the

other two species was observed (Fig. 3b). This

suggests that A. marina had low nitrite inputs

(nitrification) and/or high nitrite outputs (nitriteoxidization and/or denitrification).

Fe and P mobilization

Along with the iron oxide plaque formation on root

surfaces, we also observed increases in Fe2+ concen-

trations in the soil pore-water of pots growing A.

marina (Fig. 1a, b). These observations suggest that

A. marina roots have the greatest ability to mobilize

Fe to form clear Fe2+-Fe(III) oxide contrasts in the

rhizosphere among the three species. Fe mobilizationis promoted by reduction under conditions of low

redox potential and chelation with organic acids such

as exudates from plant roots. Otero et al. (2006)

reported that Fe2+ concentrations were higher in the

upper soil layer where mangrove plant ( L. racemosa,

Rhizophora mangle L., Avicennia schaueriana Stapf.

et Leechm. and S. alterniflora) live roots were

abundant. They also found that the redox potential

in the upper soil layer was higher than in lower layers.

Plant Soil (2011) 346:259–273 269


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These observations suggest that enhanced Fe2+ was

not due to chemical reduction, but to chelation with

root exudates. In this study, enhanced Fe2+ concen-

trations in A. marina might have also attributed to

chelation with organic acids released from roots. We

did not measure root exudates in the experimental

pots, and thus further investigation into root exudatesin the three mangrove species is needed. So far,

exudates from four mangrove species ( K. obovata, B.

gymnorrhiza, E. agallocha and H. fomes) have been

characterized (Haoliang et al. 2007; Kumar et al.

2009). After 120 days from plant colonization, the Fe2+

curve for A. marina seemed to reach saturation. This

suggests the existence of processes consuming Fe2+

such as Fe oxide deposition and plant absorption, and

that input (Fe mobilization) and output (Fe2+ consump-

tion) processes reached steady state.

Although enhancement of Fe2+

was observed onlyin A. marina, phosphate mobilization was observed in

all three species in this study (Fig. 1c). As with

ferrous ion concentrations, phosphate ion concentra-

tion curves for A. marina reached saturation 120 days

after the plant colonization, suggesting the steady

state of input (P mobilization) and output processes (P

immobilization and plant uptake). Phosphate displace-

ment from Al/Fe-P is promoted by chelation with

organic acids (Gyaneshwar et al. 2002). Enhancement

of phosphate in this study may be attributed to

organic acids from roots and/or phosphate solubiliz-ing bacteria. Among the three species, enhancement

of phosphate in soil pore-water was remarkable in A.

marina. El-Tarabily and Youssef (2010) isolated rock

phosphate solubilizing bacteria from the rhizosphere

of A. marina and one of them showed a high ability to

produce a variety of organic acids, as well as acid and

alkaline phosphatases. Considering the different

phosphate enhancement between A. marina and the

other two species, phosphate-solubilizing substrates

may also differ among the three species.

Nitrogen enrichment

The most remarkable change mangrove plants made

in this study was in soil nitrogen enrichment (Fig. 2a ).

Oxygen-releasing roots also support free-living het-

erotrophic nitrogen fixers associated with their roots

and rhizomes (Stoltzfus et al. 1997; Bagwell et al.

1998; Lovell et al. 2000). The nitrogen fixing process

requires great amounts of energy (carbon). Further-

more, the enzyme that mediates this reaction, nitro-

genase, is extremely oxygen-sensitive. Therefore,

oxygen-releasing root zones that have abundant

carbon in micro-aerobic conditions may create ideal

conditions for nitrogen fixers. Nitrogen fixation has

been observed in sediments and algae in many

mangrove forests (Zuberer and Silver 1978, 1979;Hicks and Silvester 1985; Holguin et al. 1992, 2001;

Pelegrí and Twilley 1998; Lugomela and Bergman

2002). Under field conditions, nitrogen fixation

fluctuates spatially and temporally (Lee and Joye

2006), and there are complex relationships among

many factors. Consequently it has been difficult to

assess plant growth effects on nitrogen fixation. In

this study, we detected higher nitrogenase activity in

mangrove-colonized soils than in the unplanted soils

(Fig. 6, data at 1 – 6 cm soil depth). This suggests that

the three mangrove species have the ability tostimulate nitrogen fixation. It also suggests that the

reported observations of nitrogen fixation in many

mangrove forests may be a consequence not only of

the intertidal habitat, but also of mangrove plant

colonization per se. Furthermore, nitrogenase activity

in the experimental pots differed significantly among

the three species in this study. This suggests the

possibility that rooted plant species may be a factor

determining the capability for nitrogen fixation. In

this study, we compared soil nitrogen fixation among

the plant species using a 1 – 6 cm soil depth. Soilchemical and biological properties vary significantly

with soil depth (Alongi et al. 1992), and thus the

spatial profile of nitrogen fixation requires further

study. We also detected nitrogenase activity in the

roots of the three species. Although the mean

values for roots were significantly higher than that

of the uncolonized soil, standard deviations for root

nitrogenase activity of R. stylosa and B. gymnorrhiza

were comparatively high. This suggests that the

distribution of nitrogen fixers on roots is not uniform,

but differs with position on the root (root tip or base,lateral or main root) and/or with root condition (fresh

or old root).

Among the three species, nitrogenase activity,

relative growth rate and nitrogen use efficiency were

all greatest in B. gymnorrhiza. Furthermore, B.

gymnorrhiza and R. stylosa might re-absorb or re-

translocate nitrogen prior to leaf fall, because litter C/

N ratios of the two species were higher than those of

fresh aboveground parts. These observations suggest

270 Plant Soil (2011) 346:259–273


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that B. gymnorrhiza is the most nitrogen-economical

species (plants which have a high ability to enrich the

nitrogen content of rooted soil, and a high ability to

increase their biomass with low nitrogen supply)

among the three species. In contrast, A. marina

showed lower nitrogen use efficiency than B. gymnor-

rhiza, and had comparatively high nitrogen concen-trations in the plant material. This suggests that A.

marina may have high bacterial nitrogen fixation

around its roots to meet its high nitrogen demand.

However, nitrogenase activities in A. marina soil and

root materials were lowest among the three species.

The nitrogenase activity of the decaying leaf litter was

not measured, but A. marina showed remarkably

higher nitrogen concentrations (low C/N) in its leaf

litter compared with fresh aboveground material in

this study (Fig. 5). This suggests that high bacterial

nitrogen assimilation might accompany degradationof the A. marina leaf litter. After litter fall, mangrove

litter is gradually enriched in nitrogen via bacterial

nitrogen immobilization, which occurs during decom-

position. The rate of nitrogen fixation varies among

plant species, probably because of differences in

chemical composition of the leaves. Generally, leaves

with higher nitrogen content (lower C/N) decompose

more rapidly (Melillo et al. 1984; Twilley et al. 1986)

and leaves with higher phenolics contents decompose

more slowly (Cundell et al. 1979; González-Farias

and Mee 1988). In this study, the abovegroundnitrogen content was highest in A. marina, followed

by R. stylosa and B. gymnorrhiza. Previous studies on

the leaf composition of other mangrove species, for

example, Avicennia germinans and Rhizophora man-

gle have reported that A. germinans leaf litter has

higher initial nitrogen content and lower phenolics

content (Robertson 1988), while R. mangle leaf litter

has lower initial nitrogen (Twilley et al. 1986; Pelegrí

et al. 1997) and higher phenolics content (Cundell et

al. 1979; Benner et al. 1986; Robertson 1988). From

these observations, Avicennia species are likely tohave rapidly decomposable leaves (high nitrogen and

low phenolics), thereby enriching the nitrogen content

of the litter layer accumulated on the soil surface.

Conclusion

All three mangrove species showed changes in the

four measured soil chemical properties, iron, phos-

phate, nitrogen and methane, in their rooted soils,

although the extent of change differed among the

species. Colonization by the three mangrove species

resulted in effects on soil chemical properties associ-

ated with oxidation: deposition of iron oxide on

mangrove root surfaces, enhanced NO2− and NO3

−,

and decreased CH4 concentrations in soil pore-water.

Also, mobilization of ferrous ion (in A. marina) and phosphate ion (in all three species) occurred, probably

due to root exudates. For nitrogen, the three man-

grove species significantly stimulated bacterial nitro-

gen fixation in rooted soils, leading to soil nitrogen

enrichment. While the insoluble soil nitrogen content

increased, dissolved inorganic nitrogen in soil pore-

water significantly decreased.

Among these properties, phosphate mobilization

and soil nitrogen enrichment are likely to be partic-

ularly important for the growth of mangrove plants,

because phosphate and nitrogen are generally limitedin mangrove ecosystems (Feller et al. 2003a , b;

Lovelock et al. 2004; Reef et al. 2010). Strongly

weathered tropical soils tend to contain low soluble

phosphate concentrations, with most of the phosphate

existing as immobile Al/Fe-P, Ca-P and organic

matter-P. For nitrogen, export by repeated tidal

fluctuation occurs in seaward regions (Boto and

Robertson 1990). Although nitrogen and phosphate

supply to mangrove plants seems to be insufficient for

their optimum growth in many practical field con-

ditions (Feller 1995; Feller et al. 2003a , b; Lovelock et al. 2004), the self-supporting nitrogen and phos-

phorus ability of mangroves observed in this study

could be one key to the high productivity of

mangrove ecosystems.

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.

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