173

REVIEW ARTICLE

Cycling and Global Fluxes of Nitrogen in Mangroves
Daniel M. ALONGI
Australian Institute of Marine Science
PMB 3, Townsville MC, Queensland 4810, Australia
e-mail: d.alongi@aims.gov.au
0

Abstract
Recent advances necessitate a critical reappraisal of nitrogen cycling in mangrove ecosystems. Nitrogenconcentrations in soil, water and vegetation are low, but N-use and recycling efficiencies are high and N
residence times are short, driven by rapid forest production and the need to conserve N. Most mangroveassociated fauna preferentially assimilate benthic algae, phytoplankton, algal detritus or complex mixtures ofthese forms to meet N demand. Consumer preferences, locations and types of habitat, and the relative
availability of other foods determine the trophic significance of mangrove litter. A nitrogen mass balance
model of the world’s mangrove forests indicates that: (1) 2687 Gg N yr-1 is required to sustain global mangrove net primary production (NPP); (2) N burial is ≈ 25% of total N input; (3) N2 fixation is ≤ 5% of total N
input; (4) production in roots and litter account for 40% and 50% of mangrove NPP, respectively; (5) tidal export equates to ≈ 55% of N input; and (6) denitrification and N2O effluxes account for < 10% of total N losses.
Despite proportionately large tidal losses, the global flux of nitrogen in mangrove forests is roughly in balance
due to multiple adaptations and strategies to efficiently use and retain nitrogen.
Key words: mangrove, nitrogen, nitrogen cycle, nitrogen retention, nutrient conservation

1. Introduction
Mangrove forests and their associated waterways
constitute one of the most important aquatic environments along the world’s subtropical and tropical coastlines. Mangroves inhabit over 152,000 km2 of coastal
area but occupy < 1% of global tropical forest area; they
are the only woody halophytes that live in salt water.
These forested wetlands serve a wide variety of economic and ecological roles: as habitat for terrestrial andmarine flora and fauna; as ecosystem engineers shaping
and maintaining the intertidal zone; as a renewable resource of wood and food; and as key accumulation sites
for soils, sediment particles and associated elements (Van
Lavieren et al., 2012).
Mangroves are the most productive plants in the sea
and are among the most productive forest types on earth,with average rates of gross and net primary productionof 4.6 kg C ha-1 yr-1 and 1.9 kg C ha-1 yr-1, respectively(Alongi, 2009). Most mangrove ecosystems are net
autotrophic. High rates of forest primary productivity
drive high requirements for nutrients and trace elements
to sustain growth, production and physiological maintenance of the trees. Such large needs translate into rapid
uptake of soil nutrients that are transformed by Archaea,bacteria, fungi, protozoa and microalgae, as well as
dependence on the tight links between carbon fixationand nutrient cycling. While plant-soil relations in manGlobal Environmental Research
17/2013: 173-182
printed in Japangroves are fairly well understood, how these relationships sustain high productivity in the long term and how
they impact on the linkages between mangroves andadjacent coastal environments are poorly known.
Nitrogen is one of the key essential elements for thesustenance of plant and animal life, but the dynamics of
N in relation to mangrove ecosystem change and development over time is not well understood. The criticalneed for N in the nutrition of mangrove organisms has
been confirmed repeatedly (Alongi et al., 1992; Alongi,2009). Yet no synthesis exists for mangrove N dynamics
and recent advances in N cycling necessitate a criticalreevaluation of how the many different forms of dissolved and particulate nitrogen (DN, PN) function inmangroves, and to what extent, in what form(s), and how
much, N is exchanged between forests, the atmosphereand the tropical coastal ocean.

2. Solutes and Solids
Concentrations of dissolved inorganic and organic N
in mangrove tidal water and in soil interstitial water are
consistently in the µM range (Table 1). The major formsof organic N in tidal waters are complexes of particulate
and dissolved organic nitrogen (PON, DON) originatingfrom decayed vegetation and polyphenolic acids; dissolved inorganic nitrogen (DIN) consists mostly of NH4+
with much lower concentrations of NO2- and NO3-. Con©2013 AIRIES174

Daniel M. ALONGI

centrations of DN and PN in tidal water vary in relation
to the onset of the monsoon, salinity, tidal state, plankton
production, organic pollution and water residence time
(Bala Krishna Prasad et al., 2006). Some creeks andwaterways exhibit either little temporal variation or N
concentration peaks that are not readily explainable(Trott & Alongi, 1999).
In interstitial water, spatial variations are more evident than temporal variations as soil nutrient pools relate
closely to soil composition and grain size, pH, salinity,
the presence of fine roots and degree of anoxia (Alongi,2009). Plant uptake plays a central role in controlling soil
nutrient pools, the sizes of which relate to the relative
abundance of live and dead roots. In theory, dissolved
nutrient concentrations should relate closely to seasonality of plant uptake and growth, with lower concentrations
during periods of rapid plant growth, but rarely has thisrelationship been observed in nature (Boto & Wellington,1984). That such a relationship goes unobserved is unsurprising considering that other factors regulate the sizeof the interstitial nutrient pools, such as rates and pathways of microbial decomposition and transformation,
bioturbation, infiltration of tidal water and groundwater,
faunal excreta, root decomposition and leakage, and inputs from external sources, including human wastes(Alongi, 2009).
The composition of DON in mangrove soil and inoverlying water is poorly understood. The few studies
that have detailed the constituents of DON (Stanley et al.,Table 1 Range of concentrations (µM) of DIN and DON in
mangrove waters and in soil interstitial water. From data
and references in Alongi et al. (1992), Trott and Alongi(1999), Ayukai et al. (2000), Alongi et al. (2002,
2004a), and Bala Krishna Prasad et al. (2006).
N species

Tidal water

Soil interstitial water

0.05 – 15.3
5.3 – 75.2

0.5 – 240*
3 – 1200*

0.1 – 1.2
22 – 264

0.1 – 15.5
0 – 0.2

5 – 405 – 80<1 – 548
26 – 811+

NH4
Unpolluted
PollutedNO2- + NO3Unpolluted
Polluted
DON
Unpolluted
Polluted*= free + exchangeable

1987; Maie et al., 2006, 2008) found that it is composedof polyphenolic acids and lesser amounts of urea, fatty
and amino acids, and proteins, plus some still unidentified inert organic matter.
Concentrations of PN in tidal waters are controlled by
the same factors that regulate DN, although few studies
have measured PN. The few data indicate low and variable concentrations ranging from <5 to 150 µM (Ayukai
et al., 2000). Tides play an important role in regulatingwater-column N concentrations, with large tides causing
greater dilution and variation than small tides. The extent
of freshwater input also plays a major role in controlling
N concentrations, as rivers discharge large volumes offreshwater and suspended particles whose seasonalvariability lead directly to variability in PN and DN concentrations.
Soil PN originates from dead and live roots and othertree matter, planktonic and benthic plant and animal
detritus, microbial biomass, and a mixture of terrestrial
and marine organic matter derived from land and sea(Alongi, 2009). PN concentrations, like those of DN,
vary in relation to soil grain size and composition; as thepercentage of sand increases relative to silt and clay
content, N content decreases. Soil PN values can range
from nearly undetectable in sandy carbonate sediments toas high as 1.7% by sediment DW in pure clay and peat
deposits (Alongi et al., 2004a).
PN concentrations in mangrove vegetation also vary
among tree parts and species, and with tree age (Table 2).
Concentrations are greatest in leaves, followed by deadand live roots, and wood. The percentage of PN tied up inliving biomass increases with tree age (Table 2). On awhole-forest basis, regardless of species, most N (≈95%)
is found in mangrove soils rather than in forest biomass(Table 3).
Table 3 Mean inventory of N (kg ha-1) in living tree biomass,
dead fine roots, and soil in Rhizophora stylosa andAvicennia marina forests in dry tropical Australia.
Values in the last row are percentage of N of total forest
N pool in each forest component. Adapted from Alongi
et al. (2003).
Rhizophora stylosa
Dead
Trees
Soil
roots

Avicennia marina
Dead
Trees
Soil
roots

532

100

10,330412

168

11,653

4.8%

1%

94.2%

3.4%

1.4%

95.2%

Table 2 Nitrogen concentrations (mg g-1) in different tree parts of Rhizophora apiculata (R.a.), Rhizophora stylosa (R.s.),and Avicennia marina (A.m.) in the wet and dry tropics. Adapted from Alongi et al. (2003, 2004b).
NA = age unknown.
Age(yr)
Wet tropics (Thailand)
R.a.
3
R.a.
5
R.a.
25
Dry tropics (Australia)
R.s.
NA
A.m.
NA
Spp.

%N in living
biomass

Leaf

Branch

Stem

Prop
Root

Live
Roots

Dead
Roots

2
3
12

12
10
13

3.3
3.4
4.0

2.3
1.7
1.4

2.6
2.3
1.8

6.4
5.2
4.1

6.4
6.4
7.8

5
3

9.9
14.4

1.6
2.8

1.6
2.9

2.4
―

3.2
4.5

6.4
7.8

Cycling and Global Fluxes of Nitrogen in Mangroves

3. N Availability, Plant Nutrition and
Limitation
The acquisition of nutrients is the key process sustaining growth of mangroves. Nitrogen, in addition to P
and Fe, most often limits growth, but acquiring N is not astraightforward process in mangrove environments.
Despite a number of ecophysiological mechanisms andstrategies, mangrove trees must tolerate or avoid anoxia
and salt, and balance carbon gain and water loss, while
acquiring minerals to synthesize structural and reproductive tissue (Reef et al., 2010).
N availability depends on environmental factors suchas salinity, temperature, soil fertility and geochemical

175

redox reactions between dissolved organic and inorganic
constituents in interstitial water. In highly reducing mangrove soils, for instance, metal sulfide complexes readilybind to organic nutrients thereby limiting the amount of
nutrients available to the plant (Alongi, 2009). Mangrove
growth is non-linear when the supply of N increases,
even when salinity is kept constant. In culture experiments, stem growth of Rhizophora apiculata and
Xylocarpus granatum is enhanced to the highest rate (50mmol m-2 d-1) of DIN supply (Fig. 1), whereas stem
growth of Bruguiera gymnorrhiza, Avicennia marina,
and Xylocarpus moluccensis levels off at a DIN supply
rate of 10 mmol m-2 d-1; stem growth of Ceriops tagal
peaks at a supply rate of ≈25 mmol N m-2 d-1 (Fig. 1).

Fig. 1 Relationship between growth of saplings of the mangroves Rhizophora apiculata (top left panel),
Bruguiera gymnorrhiza (top right panel), Avicennia marina (middle left panel), Ceriops tagal (middle
right panel), Xylocarpus granatum (bottom left panel), and Xylocarpus moluccensis (bottom right panel)with increasing rates of DIN supply. The lines in each panel represent best-fit regressions. Adapted from
Alongi (2011).

176

Daniel M. ALONGIIn the field, different mangrove species exhibit different growth responses to added DIN (Krauss et al.,2006; Reef et al. 2010). N or P limitation depends greatly
on the frequency of tidal inundation. For instance, in the
Caribbean, fringing mangroves are N-limited, but permanently flooded forests or those deep within islands are
P-limited (Feller et al., 2002). In an earlier test in Australian mangroves, Boto and Wellington (1983) found N
limitation from the water’s edge to the high intertidal, but
co-limitation of P only in the high intertidal zone.
High rates of mangrove productivity equate to highrates of N uptake, but also imply that N requirements
must be met by high nutrient-use efficiencies and highrates of N resorption from leaves (Lin et al., 2010). A
comparison of mangrove N-use efficiencies with thosemeasured in terrestrial evergreen and deciduous trees,
and in forbs and graminoids shows a wide spread of values, with efficiencies in mangroves at the upper end of
the range (Fig. 2A). The apparent strategy of using N
efficiently relates well to the low N concentrations foundin leaves and other mangrove tree parts (Table 2), as wellas to resorption efficiencies that are at the higher end of
the range for tropical trees (Fig. 2B).
Conserving N is clearly advantageous. Developmentof large below-ground reservoirs of dead roots andmaximizing N allocation to the youngest parts of mangrove trees are efficient retention mechanisms. Also,
mangroves are evergreen with sclerophyllous leaves androot/shoot biomass ratios similar to or higher than thosefound in other tropical trees, including desert plants (Reefet al., 2010). The former characteristic implies smaller
nutrient investment in new leaves and lower N loss due tolong tissue lifespan. Sclerophylly is linked to both low
soil nutrient content and low water availability; sclerophyllous leaves are characterized by long lifespans, slow
decomposition, and reduced leaf herbivory. Mangrove
leaves lose a high proportion of water before wilting,having life-spans typical for tropical and subtropicalbroadleaved evergreens.
Recycling mechanisms are thus well-developed inmangroves, and this characteristic is reflected in residence times for total ecosystem N that, as in most marine
systems, are relatively short (Galloway et al., 2003). For
instance, the mean residence time for ecosystem N in
Rhizophora stylosa forests in arid Western Australia is
2-4 yr (Alongi et al., 2005a) with a shorter residence timefor ecosystem N of < 2 yr in A. marina forests. A numberof factors explain the differences in nutrient-use among
species, such as species-specificity in nutrient allocationand ecophysiological mechanisms, the proportion ofenergy and N used in chemical defences, and leaf andfine root lifespans. Another effective N conservation
strategy is increasing the efficiency of various metabolic
processes and in utilizing dominant soil N pools. Mangroves, like other plants, invest a large proportion of root
metabolism in the uptake and assimilation of NH4+ whichtranslates into a comparatively low energy investmentcompared with utilizing NO3- or possibly DON.

Fig. 2 Comparison of rates of (A) N-use efficiency and (B) N resorption efficiency inmangroves with tropical plantation trees and all other forest types. Adapted from
Alongi (2009).

Cycling and Global Fluxes of Nitrogen in Mangroves

4. Soil N and Microbial Transformation
Processes
The dominance of NH4+ in mangrove soils reflects
high rates of ammonification in relation to other Ntransformation processes as well as plant preferences, theorigin(s) of PN, other pathways of utilization (e.g.,
microalgal uptake of NO3-), soil anoxia and sedimentary
history. Recent genetic studies underscore the rich diversity of bacterial functional types in mangrove soils,
including evidence for genetic sequences associated with
dissimilatory reduction of NO3-, N immobilization, N2
fixation, and denitrification (Andreote et al., 2012; Liuet al., 2012). A highly diverse suite of heterotrophic
prokaryotes numerically and functionally dominate
mangrove soils, accounting for about 80% of total living
biomass (excluding trees). Knowledge of the linkages
between various N transformation processes in mangrovesoils is limited, but pathways such as denitrification andN2 fixation have been measured often.
The complete soil N cycle has been deduced only in177three mangrove ecosystems — on Phuket Island(Kristensen et al., 2000) and in Sawi Bay in Thailand(Alongi et al., 2002) and in Missionary Bay on
Hinchinbrook Island in Australia (Alongi, 2009). In thesoil N cycle (Fig. 3) nearly all NH4+ is taken up by fineroots. DN originates from the microbial decompositionof organic N found in dead plants, faeces, dead animaland microbial matter, and rich mixtures of organics
transported into and onto the forest floor from rivers andadjacent coastal waters. Most of this organic N is broken
down to NH4+ by ammonifying bacteria, with proportionally little loss to the atmosphere via anammox(anaerobic NH4+ oxidation) and denitrification. N2 fixation is ordinarily not a major process within mangrovesoils, although surface algal mats house large colonies
of N2 fixers that are often very important in the flux of
DN across the soil-water interface. Macroalgae on
aboveground roots can also utilize comparatively large
amounts of DN.
About 5% of total N input is buried in mangrove soils(Table 4), but highest rates of N burial occur in forests

Fig. 3 Plant-soil-microbial N fluxes in the mature mixed Rhizophora spp. forests in
Missionary Bay, Hinchinbrook Island, Australia. Adapted from Alongi (2009).
Table 4 N inputs (mmol N m-2 d-1) to soils in Thai mangrove forests of different age and intertidal position.
Adapted from Alongi et al. (2002).

(A) NH4 input from tidal
water(B) NO3 input from tidal
water(C) DON input from tidal
water(D) Rain N(E) N2 fixation(F) N burial(G) Flux via NH4 pool
Total N Input [Σ (A) to (G)]% N buried% total N denitrified

25-yr old, mid-intertidal 5-yr old, high-intertidal
R. apiculata forest
R. apiculata forest
0.5
0.05

3-yr old, mid-intertidal
R. apiculata forest
0.01

3-yr old, high-intertidal
Ceriops decandra forest
0.04

2.0

2.0

0.2

2.4

1.0

0.1

0.2

0.1

0.01
0
1.6
32.0
37.1
4%
35

0.01
0.06
1.3
7.5
11.0
12%
4%

0.01
0.2
2.1
19.1
21.8
10%
6%

0.01
0.05
1.4
8.4
12.4
11%
23%

178

Daniel M. ALONGI

receiving the least tidal inundation. DN uptake from theoverlying tidal water accounts for only 9%-10% of N required for mangrove nutrition as most plant needs are
satisfied via fine root uptake. Thus, as in most tropicalterrestrial forests (Hedin et al., 2009), the turnover timeof the soil NH4+ pool is short (< 5-50 hr) reflecting rapid
rates of uptake. Overall, functional differences in plantsoil-microbe relations appear to be partly a function of
the interactive effects between stand age and intertidal
position.
Evidence for a tight coupling between trees, microbes
and soil nutrients has been obtained from studies ofinterstitial DON dynamics. Stanley et al. (1987) foundthat unless soils are poisoned to kill microbes and inhibit
root uptake, no DON is released from the soil despite astrong concentration gradient across the soil-water interface. The non-protein amino acid, ß-glutamic acid, is avaluable biomarker as it is ordinarily immobilized in theinterstitial water. Once soil microbes are poisoned, however, large amounts of this amino acid are released into
the overlying water. This phenomenon suggests that
DON transport is so rapid between trees, microbes andsoil that there is only a small residual pool.
High rates of ammonification in mangrove soils aresupported by DON released from roots. Proteins andnucleotides are hydrolyzed and catabolized by ammonifying bacteria into NH4+, with transformation rates
partly dependent on rates of organic N input and rates ofplant uptake (Alongi, 2009). In N-limited mangroves,
NH4+ is also produced from dissimilatory NO3- reduction(Fernandes et al., 2012a). This pathway conserves N bylimiting the availability of NO3- for N2O formation anddenitrification.
Denitrification is usually a slow process in mangroves(Fernandes et al., 2010, 2012a) as about 15% of total N
input to mangrove soils is denitrified. In other coastal
ecosystems, the percentage of N lost via denitrification
ranges from 20%-70% (Seitzinger, 1988). Low rates ofnitrification and anammox may limit denitrification inmangroves (Meyer et al., 2005; Fernandes et al., 2010,2012a, b), as do low NO3- availability, temperature,salinity, the presence of algal mats, and soil organic matter content. NO3- availability is the main driver ofdenitrification which is often uncoupled from nitrification, implying significant N immobilization. Low rates ofnitrification are associated with extensive uptake of NH4+by the trees, as uptake from tidal waters is not a major
source of NO3-. Anaerobic nitrification may be coupled
to Fe reduction (Krishnan & Loka Bharathi, 2009), so
NO2- production through nitrification in deep soils may
fuel the anammox process. However, although data arescant, rates of anammox in mangroves are low (< 2 µmol
N2 m-2 d-1) compared to other marine environments(Meyer et al., 2005; Fernandes et al., 2012a). Nitrification and anammox reactions may be inhibited by soluble
tannins or sulfides in the interstitial water.
The fixation of atmospheric N2 to NH4+ via nitrogenase activity by diazotrophic prokaryotes can counterbalance losses by denitrification. However, in many

mangrove soils, N2 fixation is low and mediated bysulfate reducers and other microbes inhabiting therhizosphere. N2 fixation rates range from 0-4,310 µmol
m-2 d-1, with a mean fixation rate of ≈ 620 µmol m-2 d-1(Alongi, 2009) compared with denitrification rates of
0-11,000 µmol m-2 d-1 with a mean denitrification rate of
1,530 µmol m-2 d-1 (Alongi, 2009), roughly 2.5 times theaverage rate of N2 fixation. N2 fixers are, however, very
active and diverse in the rhizosphere (Liu et al., 2012), on
prop roots, litter, fresh leaves, logs and bark. Further, N2
fixation can occur deep within the rhizosphere and inextensive root systems (Naidoo et al., 2008) in mutualistic relationships in which N2-fixing bacteria provide N
for immediate plant use and non N2-fixing rhizobacteria
and fungi provide metabolic by-products that benefit thegrowth of N2 fixers (Holguin & Bashan, 1996).
Nitrous oxide is an important greenhouse gas and in
mangroves N2O fluxes vary greatly between seasons andforests, ranging from undetectable to release rates > 330µmol m-2 d-1; some forests even show net uptake of N2O(Alongi et al., 2005b; Fernandes et al., 2010; Allen et al.,2011; Chen et al., 2012). N loading, temperature, soil
redox status and the rate of nitrification and denitrification are important drivers of N2O flux (Fernandes et al.,2010).
Mangrove tidal waterways are also a source ofN2O. N2O concentrations correspond to tidally-inducedchanges in DIN concentrations in mangrove waters, withpeak concentrations at high tide and minima at low tide
(Barnes et al., 2007; Upstill-Goddard et al., 2007). Thispattern is consistent with the idea that tidal pumping
transports high interstitial concentrations of nutrients anddissolved gases into creek waters after the hydrostaticpressure gradually declines towards low tide. Very similar tidal patterns have been observed in Vietnamese andJapanese mangroves (Imamura et al., 2007).

5. N Sources in Food Webs
Ubiquitous litter, rotting vegetation, and muddy turbid water create a strong impression that organic detritus
and attached microbes are the main sources of N fuelling
mangrove food webs. This notion was supported by workup until the early 1990s indicating that conspicuous
mangrove consumers eat mostly detritus (Robertson
et al., 1992). The working paradigm was that attachedmicrobes reduced complex, indigestible vascular plant
detritus to simple, more readily digestible forms, withmicrobial enrichment itself providing sufficient N foradequate nutrition. This paradigm supported the corollary that vegetation is an important subsidy to the adjacent coastal zone.
The advent of stable isotope research ushered in amuch more nuanced view, suggesting that most consumers preferentially assimilate fresh benthic microalgae andmacroalgae, phytoplankton, algal detritus, or complex
mixtures of these autotrophs, to meet their N requirements. Non-vascular plant material is not only more digestible, but N-rich, compared to N not readily available

Cycling and Global Fluxes of Nitrogen in Mangrovesin vascular plant material.
Workers have naturally focused on the diets of themost conspicuous consumers — crabs, fish, and shrimp.
During the 1980s in northern Australia, and subsequently
throughout the Indo-Pacific, the Caribbean, Africa andSouth America, sesarmid and grapsid crabs were found tobe foundational ecosystem engineers in mangrove forests(Kristensen, 2008). This discovery constituted a paradigm shift from the early notions of the trophic importance of detritus transported to offshore waters, to therealization that a large (but variable) fraction of litter isconsumed or hidden in crab burrows thereby reducing theamount of detritus available for export and thus also
serving as a mechanism to conserve nutrients (Robertson
et al., 1992).
How do sesarmid and grapsid crabs meet their N requirements? It was initially thought that crabs met theirneeds by voraciously eating large amounts of N-poor
litter and propagules, and assimilating the associatedN-rich, microbial biomass. This explanation seemed
reasonable considering that crabs can consume up to
100% of total litter standing stock in some forests(Robertson et al., 1992), and that they paste fragments oflitter onto their burrow walls facilitating fungal andbacterial colonization to make the litter more palpableand nutritious over time.
This notion presented a paradox in that mangrove
leaves, even aged ones, have both high tannin content andC/N ratios that are too high to sustain adequate nutrition,even with high consumption rates. Some workers suggested that crabs supplement their diet by ingesting sediment and associated bacteria and microalgae (Bouillon
et al., 2002), but sediment consumption would have to beinordinately high to meet N demands (Thongham &Kristensen, 2005), so crabs may obtain sufficient N
from supplementary consumption of animal tissue, suchas carcasses of fish and crustaceans, and meiofauna(Kristensen et al., 2010). For example, in laboratory
experiments the sesarmid Neoepisarma veriscolor preferentially eats fish meat, which contributes up to 50% of
the crab’s dietary N (Kristensen et al., 2010).
Like most higher organisms, crabs need to consume avariety of foods to maintain a balanced diet. This idea is
supported by feeding experiments and biochemical analyses of grapsid crabs from Indonesia (Nordhaus et al.,2011) where Episesarma spp. and Perisesarma spp. areomnivorous, feeding mainly on detritus, mangrove litterand bark, and on lesser amounts of roots, algae and animal tissue; chemical analyses indicate that bacteria
contribute significantly to the amount of N available forthese crabs. As found by Gatune et al. (2012) for penaeid
shrimp post larvae, the nutritive value of mangrove littercan be further enhanced by consumption of surface
microbial biofilms. Other means to acquire dietary N
exist. For example, Caribbean sponges living as epibionts
on Rhizophora mangle roots have bacterial endobionts
capable of degrading and assimilating mangrove-derived
dissolved organic matter; the endobionts in turn transfer
N-rich compounds back to the sponges to nourish growth179(Hunting et al., 2010).
Mangrove-associated fish, shrimp, and zooplankton
also have varied diets with many, but not all, species
having a clear preference for phytoplankton or benthic
algae rather than mangrove detritus (Thimdee et al.,2008; Giarrizzo et al., 2011; Chew et al., 2012; Vaslet
et al., 2012). But within a mangrove estuary or forest,
multiple food webs partitioned by dietary preferences can
exist. In the Klong Ngao mangroves of Thailand, forexample, four trophic levels exist with at least two fish
species capable of dietary switching; extremely turbid
water limits phytoplankton production in these Thaiwaters such that litter is the main source of nutrition(Thimdee et al., 2008). In northern Brazil, C and N stable
isotope analyses indicate three distinct food webs: (1) amangrove food web, consisting of epibenthos andzooplanktivorous food chains; (2) an algal food web
where fiddler crabs, polychaetes, mullets and several
other fish species directly consume benthic algae; and (3)a mixed food web of mainly benthivorous fishes that
consume a wide variety of foods (Giarrizzo et al., 2011).
If other significant primary producers such as
seagrass meadows are nearby, the dietary sources areeven more complex. In Florida and Belize, for example,
the contribution of mangroves and seagrasses to predatory fishes varies by type of mangrove habitat (i.e., fringe
versus basin mangroves) and fish residency status (Vaslet
et al., 2012). Residents show a stronger mangrove signal
than transients that actively forage in nearby seagrassbeds. In overwash mangroves, most fish show a stronger
seagrass signal, especially juvenile reef fish that shelterin mangroves but feed in adjacent seagrass beds. The
trophic significance of mangrove N to consumers thus
depends on location and type of habitat, relative availability of other primary producers, species dietary preferences and the universal need to secure a balanced diet.

6. Ecosystem and Global N Budgets
Only one complete N budget exists for a mangrove
ecosystem — the Missionary Bay mangroves at thenorthern end of Hinchinbrook Island in Australia (Alongi
et al., 1992; Alongi, 2009). The budget shows two main
N inputs to the ecosystem (Table 5): (1) N2 fixation by
microbes living on logs and other pieces of fallen timber,surface soils, live tree stems and above-ground prop roots,and (2) incoming tides. Net tidal exchange represents thelargest loss of N, as litter is exported via mangrove waterways. Secondary N losses are denitrification and sedimentation. There are likely other sources and sinks for N
in this ecosystem, but these are probably small. Overall,
the N cycle in the Missionary Bay ecosystem is in balance considering the many extrapolations and systematicand relative errors involved in a large number of individual measurements made over time. Of course, othermangrove ecosystems show net N export (Kurosawa
et al., 2003; Silva et al., 2007), and some systems evenshow a net loss due to NH3 degassing (Biswas et al.,2005).

180

Daniel M. ALONGITable 5 N fluxes (kmol N yr-1) in the mangrove ecosystem ofMissionary Bay, Australia. The budget was constructedusing data from papers cited on page 279 in Alongi et al.
(1992).
Process
Precipitation
NO2+NO3
NH4+
DON
PN

Input

OutputTable 6 A nitrogen mass balance of the world’s mangrove
ecosystems. The model assumes a global mangrove areaof 152,000 km2 (Spalding et al., 2010).
Pathway

Net exchange

Groundwater
2.4

Net primary
production
Wood
LitterRoots
N2 fixation

subtotal = 2.4
BurialExport466.2
479.7
1192.7930.7
376.7
subtotal = 3446

Tidal exchange
NO2+NO3
NH4+
DON
PN

437.5
928.0
12684.3

525.0
-87.5
696.8
231.2
8821.43862.96360.8-6360.8
subtotal = - 2354.2

Denitrification
658.4-658.4

342.5
17405

-342.5
95.9

Sedimentation
Total

17501

N flux(Gg N yr-1)

309

1152

2687

67
68

2

Inputs

0.7
0.5
1.3
0.1
subtotal = 2.6

N2 fixation
SaltpanSoil Surface
Prop roots
Logs/timber
Stems

C:N ratio(weight:
weight)C flux(Tg C yr-1)1

The Hinchinbrook work (Fig. 3, Table 3) suggests thata number of mechanisms operate to conserve N in mangroves: (1) very high rates of soil N recycling to the extent that most DN is taken up by the trees; (2) crabs
retaining litter N in the soil; (3) tree stems, roots, logs,
and other timber providing maximum surface area tofacilitate microbial colonization and maximize N2 fixation; (4) large pools of below-ground dead roots acting as
nutrient reservoirs; and (5) most N exported being highly
refractory, not labile, and high in concentrations of humic
and fulvic acids and polyphenolics.
The importance of these retention mechanisms canalso be discerned from an estimate of the main N flows in
the world’s mangrove ecosystems (Table 6). This global
mass balance is only indicative, but is instructive in pinpointing the magnitude of global sinks and sources ofmangrove N. Derived from C:N stoichiometry (see Table
6 footnotes), the mass balance indicates that: (1) 2687 Gg
N yr-1 is required to sustain global mangrove net primary
production; (2) N burial is ≈ 25% of total N input; (3) N2
fixation is ≤ 5% of total N input; (4) ≈ 40% of N input
required for total mangrove NPP is vested in below-ground root production; (5) ≈ 50% of N required for
mangrove NPP is vested in litter; (6) tidal export equatesto ≈ 55% of N vested in mangrove NPP; (7) < 10% ofmangrove N is lost via denitrification and N2O emissions;and (8) N fluxes are in net balance as the net gain
(351 Gg N yr-1) is very small compared to the total inputs,
outputs and sources of error.

Denitrification
Soil N2O
releaseWater N2O
release

220
523

305
1307
10754
1005
Total Inputs =2787

Outputs
29407
29 (POC) +3.5 (P), 16
14 (DOC)
(D)8

740
1496
1809
109
109

Total Outputs =2436
Net Gain = 351
1from Alongi (2009)
from Alongi et al. (2003)
from Robertson et al. (1992)
4
determined by the difference between total NPP and wood + litter
production
5
median rates for soil, logs and prop roots in Alongi (2009) multipliedby global area
7
median C: N ratio (wt: wt) at 1m soil depth (Alongi et al., 2004a,
2005b)
8
median POC: PON and DOC: DON ratios from Alongi (2009)9
median rates in Alongi (2009) multiplied by global area
2
3

Most N needed to support mangrove primary production must eventually come from net tidal import of
sediment particles from upstream or from the coastal
ocean or both, given the relatively small amounts of N
fixed within forests. Much of this allochthonous N isefficiently recycled via plant-soil-microbe pathways as
75% of mangrove N is vested in litter fall, exported bytides and buried in sediments. This notion is supported by
the fact that a large proportion of N is vested in producing
fine roots below ground. Of course, this preliminary
global budget is crude and does not include minor pathways that may be important in some forests, but it doessuggest that despite large tidal losses, N fluxes in theworld’s mangrove forests are roughly in balance due tothe evolution of a number of highly efficient N conservation strategies and adaptations.
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Daniel M. ALONGIDaniel M. ALONGI is a Senior Principal Research
Scientist at the Australian Institute of Marine
Science and specializes in biogeochemical researchof tropical coastal ecosystems. He is especiallyinterested in the structure and function ofmangrove forests and has been working on these
topics for the past 28 years.

(Received 31 December 2012, Accepted 7 May 2013)