(1) (1) Table 5.

3 Mean rate of secondary production, respiration, assimilation and net product

ion efficiency (NPE production assimilation ratio) in several species of crabs and other epibe
nthos occupying mangrove forest and small and large creek banks in the caete estuary, northe
rn Brazil (Data drom Koch and Wollf 2002)

the foods consumed are highly nutritious. Koch and Wolff (2002) also postulated that these hi
gh efficiencies and the fact that the crabs assimilated organic matter equivalent to 15% of for
est net primary production reflect a positive feedback loop between the crabs, soil bacteria, an
d the trees. It thus appears that there is a network of positive feedback loops in mangrove fore
sts to enhance nutrient recycling and to help conserve nutrients.

5.3.2 Patterns of Microbial Decomposition of Litter

Crabs and other benlhic detritivores initially process nearly 50% of the total littertfall produce
d in many forests, but what happens to the rest of the material? A variable proportion is swept
away by the tides (see Chapter 6), but any litter remaining in the forest is then further decomp
osed by various microbial flora; litter shredded but uunassimilated by the crabs is returned to
the soil as waste and is also consumed by microbeas. In many cases, litter that has not been i
mmediately processed by macroconsumers is initially degraded by microbes
Detritus not processed by macroconsumers decomposes in three Stages: ( 1) leaching of soolu
ble compounds (2) saprophyticdecay, and (3) Fragmentation. A large number of studies meas
ured the microbial decay of mangrove leaf detritus (Robertson et a1 1902a. Kristensen et al .
22008) and several common features

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• Absolute decay parameters are sit and species-specific.
• Leaves decompose faster in subtidal areas than in the intertidal zone.
• Leaf decay is more effective when leaves retain their moisture.
• Leaves of species such as Avicennia and Kandelia with lower tannin content and
higher initial nitrogen concentrations decompose faster than Rhizophora and Bruguier leaves
• Leaf decomposition of the same species occurs at similar rates in both the tropics and
subtropics, but more slowly in the dry tropics where leaves are subject to intense aridity and
high salinity.

The initial stage of leaehing involves the loss, on average, of 20-40% ofthe organic carbon in
the leaf when submerged for 10-14 days. The first components to be lost are the non-
lignceilulose carbohydrates such as sugars, tannins, and other phenolic compounds. This
leachatc is quite labile and is readily degraded aerobically and incorporated into microbial
biomass with conversion efficiencies up to 90% (Kristensen et al. 2008). The remaining
particulate detritus then undergoes the second phase of decomposition with the colonization
by aerobic and anaerobic prokaryotes, and oomycotes (zoosporic members of the Protoctista).
Ascomyeetcs (true fungi) appear to play a relatively minor role in mangrove litter
colonization (Newell I996); it is the oomycotous protoctists, especially Halophytophrhora
vesiculara, that are especially wcll-adapted to capture cellulosic compounds via pervas‘on
and digestion, to the extent that these polysaccharide components are decomposed about
twice as fast as the lignins. Mangrove detritus thus becomes relatively enriched in lignin-
derived carbon over time. Lignin has a half-life of >150 years, so it is degraded only very
slowly, especially under anoxic conditions when incorporated in the soil.
The chemical changes that occur in decomposing mangrove detritus is a function not only of
enzymatic degradation and loss 0f leachable compottndsf but of compositional changes in thc
microbes that have colonized the material. Accumulation of microbial biomass over years of
decomposition results in a relative enrichment of N and P relative to C, but also an increase in
hydrolyzable amino acids, total amino acid, bacterial biomarkers, lipids, and monosatumted
and branched chain fatty acid typical of bacteria (Mmingc ct al. 2003; Tremblay and Benner
2006). Tremblay and Benner (2006) found that utter 4 years of decomposition, leaves of
Avicennia germinal“ arc composed of 60-75% N and 20-40% C derived not from the original
plant tissues, but ftom hctcrotmphic bacteria. Relative phosphorus content in decomposing
leaves of Rhizophora apiculata increases; l74-220% of the minal amount in the litter after
scvcml months. probably in concert with binding of? to humic compounds and iron (Nielsen
and Anderson 2003). These chemical studies help to explain the early l'mdings ofn general
decrease in the ON and C:? ratios of decomposing mangrove detritus over time.

The decay constants of yellow leaves deposited into mangrove soil range from 0.00-0,1 day-'
With demnpusitinn usually following the single exponential pattern, Mt= Moe-kt, where Mt
is the mass remaining after time t, Mo is the initial mass, and k is the decai constant
(Ktistensen et al 2008). This progression of

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decay is controlled by several factors such as mangrove species. initial C:N:P ratio. tidal inun
dation frequency, and abundance of detrivores. Wetting is a particularly crucial factor lu facil
iate leaching of soluble compounds und accessibility by microbes. The rate of decay is, of co
urse, also greatly augmented by shredding by leaf-eaters, such as cabs and amphipods (Kriste
nsen and Pilgaard 2003; Bosire et al. 2005 ). A significant inverse relationship exists between
the decay constant and the C:N ratio of mangrove leaf litter (F ig. 5.2). This inversc correlatio
n implies that the rate of microbial decomposition of mangrove leaf litter is strongly depende
nt on the availability of nitrogen relative to carbon.
Leaves from genera such as Avicennia and Kandelia decompose much Faster than litter origi
nating from species with more structural lignocellulose, such as Rhizophora (Fig. 5.2). In add
ition to species differences in degradability and elemental composition, there are also differen
ces between locations which can be attributed to regional differences in nutrient availability o
r forest age. Overall. however, decomposition rates and nitrogen immobilization of mangrove
litter is controlled by the initial chemical composition of the residues. Perhaps, as in terrestria
l forests (Manzoh et al. 2008), decomposers in mangrove forests lower their carbon-use effici
ency to exploit litter of low initial N content.

The decomposition of leaf litter has important trophic implications beyond the forest floor. Fo
r example, a pepuc inducer originating from bacteria decomposing mangrove leaves cues settl
ement and metamorphosis of planula lawae of the tropical jellyfish Cassiopea xamachanu (Fl
eck and Fill 1999). Planulae prefer to settle on

r2=0 486. n.11 0.08 Ka t

'7 0.06 % Av |_ | g Ka AV (h : 8 o 04 >5 m 8 O C

o 02 e

Rh Hh Rh Rh Rh So O 00 0 20 40 60 80 100

Initial molar C:N

Pig. 5.2 The inverse relationship between the decay constant and the C:N ratio of mangrove l
eaf litter (modified from fig. 4 in Kristensen et al. 2008). La = Kandelia, Rh=Rhizophora, So
=Sonneratia, Ce =Ceriops, Av; Avicennia

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the shady side of leaves and reject other substrates lbr settlement. Whether or not gregarious settleme
nt of other marine invertebrates is induced by chcimuul chemical eues released from leaves or other co
mponents in mangrove forests is unknown. but this work again illustrates how processes in the forest a
nd in tidal waters are linked.

5.3.3 Crabs as Ecosystem Engineers

Burrowing grapsid and ocypodid crabs usually dominate the bcnthie infaumt of mangroves and have c
onsiderable impact on ecosystem functioning to the extent that they have recently been labeled ‘ecosy
stem engineers’ (Kristensen 2008). ‘Ecosystem engineers’ are organisms that directly or indirectly exert
a modifying or controlling influence on the availability of resources to other species by causing change
s in the physical state of the environment. In Section 3.2.2 we saw how crab burrows alter the flow and
transport of water and suspended materials from the forests to adjacent waterways, and in the previou
s Section (5.3.1), how they consume a significant fraction of litter that falls to the floor of many forests.
Both roles have an decisive impact on nutrient retention within the ecosystem, thus minimizing the out
welling of such material.

Five processes are crucial in considering crabs as ecosystem engineers (Cannicci et al. 2008; Kristensen
2008):

 Changes in soil texture and porosily induced by their burrowing and maintenar ee activities.
 Redistribution ofmatcrials (fluids, gases) by reworking within the soil or active pumping ofmater
ial in and out of the soil via burrows.
 Hundiing and ingesting potential food resoutces and by doing so modifying and changing soil
rcdox.
 Burrows mediating transpon of substances via diffusive gas transport, passive fluid transport as
well as collapsing burrows.
 Change in the reactive states of substances via removal of toxic metabolites (e.g., H28) and intr
oduction ofoxygen deep into the soil.

Sesarrmid and fiddle ' crabs construct burrows in mangrove soils to retreat from intolerable env ronme
ntal conditions (e.g., high tide, desiccation, high temperatures) and to use as a refuge from competitior
and predation. Fiddler crabs prefer Open spaces, such the banks of mangrove creel s, where sunlight is
sufficient to foster surface growth of benthic mieroalgae. Sesamtids on the other hand prefer to bttiTo
w into soil undet the canopy where litter is most abundant and where the shaded soil and associated r
oots provide protection against high temperatures and predatms. Neither crab group actively ventilatcs
its burrows or secretes mucus to directly stimulate microbial activity. Instead, they increase microbial ac
tivity and the transport of solutes und gases by their .sporatic crawling movements and by constructing
burrows of such design as to increase the interface between soil and thc waterr/air interface. Aside fro
m transporting litter down their burrows, crabs alter the biogeochemistry of soil lining the burrow wall
by facilitating oxygen penetration, which increases the

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volume of oxidized Fe37 soil and neutralizes anaerobically-derived metabolites. There is am increased s
upply of reactive Fe37 in soils of the burrow walls tipping the delicate redox balance in favor of iron red
uction over sulfate reduction (Kristensen 2008). Smaller amounts of toxic sulfides are therefore pioduce
d and what H2S is produced is quickly convened to relatively inert pyrite or may be re-oxidized back to
sulfate.

Field experiments in which sesarmid crabs were excluded reveal some profound effects not only on sed
iment chemistry but also on forest productivity (Smith et a.. 1991). in Rhizophora-dominated forests in n
orth Queensland, Australia, Smith et 31. (1991) found that exclusion of sesarmid crabs results in increase
d levels of sulfide and ammonium in the porewater compared with control plots in which crabs are left
undisturbed. Perhaps more importantly, stipulc fall is significantly less in the exclusion plots as is mangr
ove reproductive output. This experiment underscores the crucial role of crabs in influencing the produ
ctivity of mangrove forests.

Sesarmid crabs also contribute to the rates and pathways of microbial carbon oxidation in mangrove s
oils by producing fecal pellets that sustain high microbial activity and acting as a food source for detritu
s-feeders, such as amphipods (Lee 1997). The feeding activities of fiddler crabs are different. being restr
icted to the upper few mm of soil, but these small crabs exert a clear impact on microbial activities just
as much as sesarmids do via their foraging behavior (Meziane et al. 2002). In a microcosm experiment,
Kristensen and Alongi (2006) examined the impact of the presenee/absence of the fiddler crab Uca voc
ans on microbial fluxes with and without saplings of Avicernnia marina. The saplings grew more leaves
and pneumatophores in the presence of the crabs. When crabs were absent from microcosms. dense
mieroalgal mats developed leading to stimulation of benthic primary production and respiration (Fig. 5.
3). Lowest respiration rates were

Fig. 5.3 Comparison of the impact of the presence (+)/ absence (-) of fiddler crabs and mangrove sapli
ngs on rates and pathways of microbial biochemistry (data from Krestensenn and Alongi 2006)

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measured in microcosms with crabs but without saplings; this result was due to crab grazing significantl
y reducing the standing stock of surface microalgae in turn reducing the available supply of labile carb
on for microbial decomposition. The percentage of microbial decomposition that occurred via the sulfa
te reduction pathway was greatest in this treatment as leaching of DOC from mangrove mots stimulate
d the activity of sulfate reducers. Fe 35 was the most important electron acceptor for microbial carbon m
ineralization in ungrazed soil (63-70%) whereas SO43- was more important in grazed sediment (36-44%
), especially in the presence of Avicennia (Fig. 5.3).

5.3.4 Trophic Dynamics of Other Macrobenthos

The diets of other benthic macrofauna have been elucidated by a variety ofmethods, such as gut analys
is and feeding experiments, but recent studies using stable isotopes and fatty acid biomarkers have uru
'avelled the dietaty mysteries of many invertebrates (Table 5.4). The food ofmany epifauna and infauna
has been classified as detritus when, in reality, most gut contents are unidentifiable or consist of organi
c matter from an unknown source. Fatty acid and stable isotope analyses (Table 5.4) show to a remarka
ble degree the lack ofa distinctive mangrove signal; a more common characteristic of these invertebrat
es is a signature suggesting foods derived from other autotrophs, bacteria, and organic matter plus so
me plankton. In a series of detailed studies of benthic invertebrate diets using stable isotope results, Bo
uillon and his colleagues (Bouillon et al. 2002a. b, 2004) found that in Indian mangrove estua 'ies, mang
rove-derived organic matter is not the principal food source, but that phytodetritus from the waterways
is the main food for most species; oniy a limited number ofspecies assimilate mangrove-derived organi
c matter. in the"pre-monseen season, pelagic and benthic microalgae are the preferred foods and rely
almost entirely on microalgal carbon as a food source in the post-monsoon season.

The mudskipper, although not an invertebrate, is one ot" the faunal icons of mangrove forests, occupyi
ng a specialized nice in the intertida zone, and living an amphibious lifestyle in intimate contact with ot
her benthic organisms (Clayton I993). Mudskippers arc carnivorous, feeding mostly at low tide on prey
picked from the soil surface, but until recently the contribution of various food items to their diet has n
mained illusury. A detailed analysis of the mudskipper Periuphlhalmm argemilt’t ealus inhabiting the m
angrove shoreline in Tanzania found that dietary switching; occurs from juvenile to adult stages (Kmitw
agen et a]. 2007). Fish up to 60 mm in total body length feed lnostly on small copepods and amphipod
s. Larger individuals growmg as long as 70-110 mm shift their prey selection to polyehaetes and there a
fter to a diet of mangrove crabs. Stable isotope signatures confirm these gut results and show that the
prey items are derived From local mangroves.

Benthtc carnivores and detritivores are abundant in most mangrove forests, but a new paradi
gm is emerging. in that many ot the most conspicuous soil-dwelling fuauna feed on a wide variety of f
oods. especially those of algal origin. Mangrove

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detritus is stili a key food resource for some organisms, but it probably plays an equally important role i
n nutrient recycling and retention to help sustain high rates of net canopy production in many forests.
Until recently. the trophic role of micro and macroalgae has been greatly underestimated.

5.3.5 Wood Decomposition

Mangroves, like all trees, eventually die, fall, and come to rest on the forest Hoor where they are quickl
y colonized by fungal colonies and other organisms that either live within the forest or are imported wit
h the tides (Cragg 1993; Allen et al. 2000; Maria and Sridhar 2004). But it is the teredinid mollusks that a
re the main agents of wood decomposition, possessing symbiotic cellulolytic and nitrogen-fixing bacter
ia that assist in breaking down wood. The onset of wood boring by the mollusks does not begin until af
ter significant leaching of dissolved matter has occuned. A laboratory screening of natural resistance in
tropical hardwoods has found that several mangrove species produce leachatcs that induce mortality in
marine borers, with the leachate of all species being toxic; B. gymnorrhiza being especially so compare
d with Heritiera liltoralis, R. srylosa, and Xylocarpus granatum (Borges et al. 2008). After this initial leachi
ng stage, decomposition by marine borers speeds up. Robertson and Daniel (1989b) found that after n
early 16 years lying on the forest floor decaying, trunks of Rhizophora were riddled with a network of tu
bes produced by teredinids. Some workers (Chai 1982; Ong ct al. 1984; Hauff et a1. 2006) noted more r
apid breakdown of logs tying within some Malaysian and Micronesian forests, whereas 9-10 years after
the passage of Hurricane Andrew, 66% of coarse woody debris was decomposed on the floor of a sout
h Florida mangrove forest (Krauss et at. 2005). "

De ritus from wood decomposition can be almost as important as leaf litter consumption by crabs in so
me forests (Fig. 5.4). In mature and young Rhizophora forests in northern Australia, Robertson and Dan
iel (1989b) estimate that the flux of fallen wood and crab consumption rates of litter are nearly equivale
nt in the mature forest, whereas leaf consumption is the main dctrital pathway in the young forest. The
y found that trunks decompose rapidly (k = 0.108 year") compared with wood in terrestrial forests, but
branch wood decomposes even more rapidly (k = 0,302 year”), After nearly let, the trunks sti11 retained
20% of their original c'ubon, although the C:N ratio dropped from 1,400 to 190 during the first year of
dewmposition. Branches retained 50% of their original carbon in a 2.5 year experiment with the C:N rati
o declining from 125 to=290 (Fig. 5.4).

The rate of wood decomposition varies in relation to mangrove species, position of the wood (i.e., lying
down 0r standing), and intertidal location. Using small wood disks cut from live stems or Avicennia ger
minans. Luguncularia racemosa, and Rhizophora mangle and placing them up above tidal waters, on a
nd beneath the soul surtace. Romero et a1. (2005) studied their decomposition patterns in a South Flori
da estuary for 28 months. Decay in the air followed a simple exponental

(8)
Diets of benthic msvroinvertebrate species found in a variety of mangrove forest and
waterway worldwide as deduced by catty acid biomarkers and stable isotopes. FA = Fatty
Acid; SI=Stable Isotope; B=Both methods