An empirical model of the fate of organic carbon in a mangrove forest partly affected by anthropogenic activity

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Ecological Modelling 147 (2002) 69–83
An empirical model of the fate of organic carbon in a
mangrove forest partly affected by anthropogenic activity
John F. Machiwa a,*, Rolf O. Hallberg b
a Department of Zoology and Marine Biology, Uni�ersity of Dar es Salaam, PO Box 35064, Dar es Salaam, Tanzania
b Department of Geology and Geochemistry, Stockholm Uni�ersity, S-106 91 Stockholm, Sweden
Received 14 June 1999; received in revised form 28 April 2000; accepted 27 June 2001
Abstract
A model of biogeochemical and hydrological processes that drive organic carbon dynamics of a mangrove
ecosystem has been developed. Tidal regime parameters as well as biological factors related to macrofauna and
microbiota are described within the model. The model includes three sub-models, each representing a major form of
organic carbon in the mangrove ecosystem; litter organic carbon, particulate organic carbon and dissolved organic
carbon (DOC). Results from the model reveal that discharge of DOC to the adjacent ocean may be one of the
dominant outputs of a mangrove forest. The model confirms the observed data that DOC accounts for 80% of total
organic carbon export. In order to balance the standing crop of DOC in the marine fringe zone, the model suggested
that 40% is removed in this zone by microorganisms as well as resident and tidal migrant fauna. © 2002 Elsevier
Science B.V. All rights reserved.
Keywords: Crabs; Dissolved organic carbon; Empirical model; Litter; Mangroves; Particulate organic carbon
www.elsevier.com/locate/ecolmodel
1. Introduction
Summers and McKellar (1981) made a sensitiv-
ity analysis of carbon flows in an estuarine envi-
ronment. Their model consisted of 19
compartments within four well-defined subsys-
tems interacting through distinct fluxes. The
model took into consideration the time variable
and could be used for predictive purposes. A
model of phosphorus dynamics in a Spartina salt
marsh was developed by Pomeroy et al. (1972).
The model consisted of five compartments, the
external forcing function was the physical removal
of Spartina. Lugo and Snedaker (1974) modelled
the effects of nutrient runoff on mangrove pro-
duction, and the influence of tides on mangrove
production and export. Their model also consid-
ered the consequences of mangrove succession on
nutrient content of surrounding waters. They used
non-linear differential equations in simulation of
a three-compartment system. State variables
which were used in the model were light, tide, and
dissolved oxygen. Jacobi and Schaeffer-Novelli
(1990) developed a conceptual model on the fate
* Corresponding author. Fax: +255-5141-0038.
E-mail addresses: jmachiwa@ucc.udsm.ac.tz (J.F.
Machiwa), rolf.hallberg@geo.su.se (R.O. Hallberg).
0304-3800/02/$ - see front matter © 2002 Elsevier Science B.V. All rights reserved.
PII: S 0304 -3800 (01 )00407 -0
mailto:jmachiwa@ucc.udsm.ac.tz
mailto:rolf.hallberg@geo.su.se
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8370
of oil spills in mangroves. Detritus, inorganic and
organic particulate matter are state variables or
system features that influence oil storage in the
system. Tidal flush is the main forcing function
affecting residence time of oil constituents. Pilette
and Kincaid (1992) used a non-cyclic approach to
analyse carbon transfer in a small hypothetical
ecosytem. Models derived from empirical data
which integrate structural and functional ecosys-
tem characteristics are rare. For instance, Wort-
mann et al. (1997) modelled the vegetative spread
of sea-grass in estuarine environment, and Duarte
and Ferreira (1997) simulated macro-algae popu-
lation dynamics in a sub-tidal area. Few studies, if
any, have used a holistic ecosystem analysis to
model structures and energy flows in mangrove
systems. Most of the previous works had suffi-
cient temporal resolutions, but they were of a
limited spatial extent and the coverage was on just
few aspects of the ecosystem.
Dynamics of macrodetritus and benthic nutri-
ents in mangrove ecosystems have been investi-
gated by several workers (e.g. Lugo et al., 1976;
Boto and Bunt, 1981; Twilley, 1985; Alongi et al.,
1989; Lee, 1990; Alongi, 1996). For instance, the
influence of tidal regime and benthic organisms
on organic matter exchange has been well docu-
mented. It has also been reported that the extent
of tidal export depends on the amplitude and
frequency of tidal inundation. Golley et al. (1962)
used mass balance approach to estimate tidal
exchange of material between a mangrove stand
and adjacent marine biotopes. Cundell et al.
(1979) and Robertson (1988) concluded that the
amount of organic matter, which was available to
coastal and offshore higher trophic level, was
dependent on the sum of production, leaching,
decomposition and detrital storage in a mangrove
system. Invertebrates are an important factor in
regulating the magnitude of organic carbon ex-
port (Robertson, 1986; Lee, 1989; Robertson and
Daniel, 1989; Robertson et al., 1990; Camilleri,
1992; Emerson and McGwyne, 1992). Indeed, the
grapsid crabs are more efficient in retention of
autochthonous organic matter and litter turnover
than purely microbial decay process (Macnae,
1968; Leh and Sasekumar, 1985; Robertson, 1986,
1988). Microbiological degradation of litter pro-
duce dissolved organic carbon (DOC), that forms
a high proportion of material export from man-
grove areas (Twilley, 1985). A review by Muller
(1998) discussed the connectivity of structural and
functional characteristics of an ecosystem. For a
holistic ecosystem comprehension, the author em-
phasised analysis of ecological gradients in physi-
cal, chemical and biological compartments of the
system.
In this study, we used a modelling approach to
investigate the fate of organic carbon in a man-
grove ecosystem. We have shown that, modelling
can reliably estimate some parameters that are
difficult to quantify under field conditions and can
explain processes that can not be well constrained
by field measurements (e.g. Muller, 1998).
2. Materials and methods
2.1. Construction of the model
In ecosystem simulation, a system comprises
several compartments, in this case specific parts of
the mangrove forest like the terrestrial fringe (TF)
or the crabs. Compartments are connected via
flows whereby they act in full or partial depen-
dency on each other to contain a certain amount
of carbon. Inputs were litter fall in the mangrove
area and litter as well as particulate organic car-
bon (POC) and DOC from the ocean. The ocean
was used as a sink for all outputs from the
mangrove forest, Fig. 1. These inputs and outputs
are named variables and can be a value according
to an equation, which is calculated as the model is
run. In our case, we used annual averages accord-
ing to our observations. Knowledge of internal
processes that are connected with input and out-
put, their functions as well as their limitations is
of fundamental importance in ecological
modelling.
In order to develop a model for the fate of
organic matter in an ecological system, we first
considered a conceptual scheme of the organic
carbon dynamics in the forest (Fig. 2). The proce-
dure involved in the construction of this ecologi-
cal model includes identification of the main
compartments, and measurement of their sizes.
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–83 71
Major fluxes, their magnitudes and directions
were also determined. System variables and
boundary conditions were considered during the
field surveys. Quantitative data regarding various
aspects of matter turnover were then accumulated
over a period of 2 years (Table 1). The subsystems
were the ecologically distinct zones in the man-
grove forest:
Marine fringe (MF) zone was colonised by a
nearly pure stand of Sonneratia alba. Trees are
large and widely spaced, they harbour dense beds
of oysters (Machiwa and Hallberg, 1995). The
Fig. 1. Parent model of the fate of organic carbon indicating flows (Mg org.C year−1) to or fromsub-models and the ocean.
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8372
Fig. 2. Generalised section of Maruhubi forest showing location of the sub-areas in relation to tidal level (HST=highest spring tide;
MHT=mean high tide; MT=mean tide level; MLT=mean low tide). Vegetative structure of the forest is represented by relative
heights (not to scale) of trees and shrubs. The conceptual diagram of organic carbon dynamics is shown (A= total litter production
in each mangrove sub-area; C=grapsid crab density; L= litter standing crop; S=organic carbon content of the sediment; thick
arrows indicate direction of flow and magnitude (not to scale) of LOC, POC and DOC).
sandy/muddy substrate supports a high popula-
tion density of ocypodid crabs and other benthos.
Shoreline (SL) zone was composed of mixed
vegetation of S. alba and A�icennia marina. Trees
were relatively short, with few crabs and oysters.
Landward extent (LE) zone was situated land-
ward adjacent to the SL. Half of its area com-
prised a mixed stand of short A. marina and
Ceriops tagal plants. Another half harboured an
almost monospecific stand of densely growing C.
tagal shrubs. Relatively few ocypodid and
sesarmid crabs were found in this zone. For mod-
elling purposes, the SL and LE zones were com-
bined to form a common SL–LE compartment.
This was necessary because of the inherent
difficulties of sampling of suspended particulate
matter (SPM) and macrodetritus transport in the
inner zones of the forest.
TF zone had an almost pure stand of large A.
marina trees. Mangrove floor macrofauna in-
cluded big sesarmid crabs.
Each zone was treated as containing a homoge-
neously mixed volume of water, with tidal water
flow serving as a link for transfer of different
forms of organic carbon (org.C) between the
compartments.
Position of the mangrove zones in relation to
the amplitude and frequency of tidal inundation is
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–83 73
Table 1
Summary of the field data (mean�standard deviation) that were used to construct the empirical model of organic carbon.
SL and LE TFMarine fringe
Litterfall (g m−2 year−1) 241.4�141.5632.5�364.1 728.9�432.2
14.3�10.6 7.4�5.23.0�1.7Litter standing stock (g m−2)
Suspended particulate matter (mg l−1)
5.18�2.793.44�2.56 9.04�3.71Flood tide
Ebb tide 4.28�2.241.81�1.74 4.54�2.94
Dissol�ed organic carbon (mg l−1)
1.355�0.482Flood tide 1.920�0.5240.789�0.365
2.005�0.488 2.573�0.3791.276�0.221Ebb tide
Lateral transport, litter (g m−1)
63.9�36.214.0�15.3 16.2�23.9Flood tide
37.1�15.3 68.9�66.1Ebb tide 52.5�51.9
10.1Crab litter removal (Mg year−1) 80.2–
Depth of water (m)
1.9�0.57Spring tides 0.9�0.4 0.5�0.1
0.9�0.58Neap tides 0.5�0.5 –
95 975 160 385112 980Surface area (m2)
Estimated �olume of water (m3)
80 210214 660 80 190Spring tides
22 630Neap tide –101 680
18252375 2128Length of SL (m)
shown in Fig. 2. Compartments of the model are
related with actual mangrove regimes in
Maruhubi mangrove forest as shown in Fig. 3. A
total of eight compartments within the three sub-
models were used (Figs. 4–6). Initial value of
these compartments was zero. A steady state of
the eight compartments was usually achieved
within ten cycles, where each cycle represents 1
year.
Field data has been combined to make an
algorithm using Model Maker ver. 3 software.
For example, the change with time in the TF
compartment of subsystem 2 (Fig. 4) is described
as a differential equation.
dTF
dt =TFlitter−F1−F4−F7
=TFlitter−TF(k1+k4+k7).
The variable TFlitter is the calculated mass of
organic carbon of annual litter fall based on
observed data from the collecting nets. The rate
constants k1 and k4 have been chosen to satisfy
observed mass flows to Crabs and SL–LE, respec-
tively. k7 is chosen to satisfy observed standing
crop of TF.
Fig. 3. Map of the study area showing sub-areas of the forest:
marine fringe (MF) which is mainly colonised by S. alba ;
shoreline (SL) composed of S. alba and A. marina ; landward
extending (LE) with an almost pure stand of C. tagal as well
as a mixed stand of C. tagal and A. marina ; terrestrial fringe
(TF) dominated by A. marina.
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8374
Fig. 4. Litter sub-model showing the compartments and sinks of litter (rectangular boxes): MF; combined SL and LE; and TF; crab
consumption; and degradation. Fluxes of litter in the forest sub-areas are shown. Model and observed (in parentheses) values are
given in Mg org.C year−1.
2.2. Estimation of mangro�e leaf remo�al by
crabs
Grapsid crabs, especially Neosarmatium mein-
erti, were quantitatively the dominant members of
the macrofaunal community of the mangrove
floor of the LE and TF zones (Machiwa and
Hallberg, 1995). Other important crabs included
the gecarcinid, Cardisoma carnifex and few Uca
spp. Rate of litter removal by the grapsid crabs
was estimated by using a laboratory feeding ex-
periment. The set-up involved collection of live
crab specimens of varying size classes from the
forest. Crabs were then fed on senescent A.
marina leaves that were about to be shed. Half
leaves (split along the petiole and midrib) were
introduced into plastic buckets (10 l) in which the
crabs were reared; the other halves were retained
for dry weight (dw) determination.
2.3. Determination of organic carbon in the forest
Litter production was measured using 36 litter
traps made of a square wooden frame (0.25 m2 )
and a tapering net (mesh size 2 mm). Six traps
were deployed in each sub zone of the forest, and
monthly collections were made. Aboveground
standing litter biomass in the forest subsystems
was determined by collecting all litter in 1 m2
quadrants. Litter was dried to constant weight at
80 °C. A portion was finely ground (�80 mesh),
homogenised and litter organic carbon (LOC) was
determined as total organic carbon (TOC). A
Shimadzu TOC-5000 analyser (equipped with
Solid Sample Module SSM-5000A) was used.
Floating mangrove litter was collected at five
sampling sites along the ocean– forest boundary,
three sites at the MF–SL–LE boundary and four
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–83 75
sites at the SL–LE–TF boundary. The same sites
were used for water sampling to the POC and
DOC analysis. Macrodetritus was collected with a
net (2 mm mesh size) that was set perpendicular
against the direction of the tidal flow. The net was
kept above the water surface by closely fastened
buoys. Macrodetritus was dried to constant
weight and TOC was determined as above.
Water samples for SPM and DOC analysis
were collected at depths of 0.25, 0.5, 1.0, 1.5 and
2.0 m depending on the amplitude of the tide at
the specific site. Samples for POC determination
were immediately centrifuged (3500 rpm, for 10
min). SPM was washed with distilled water, freeze
dried and the weight was determined gravimetri-
cally. POC content of SPM was analysed with a
Shimadzu TOC-5000 analyser.
Samples for DOC analysis were filtered through
a 0.45 �m membrane filter (Schleicher &
Schuell®). DOC was determined as non-purgeable
organic carbon (NPOC) with a Shimadzu TOC-
5000 analyser coupled to an autosampler (ASI-
5000). The methods are described in details in
Machiwa and Hallberg (1995) and Machiwa
(1999).
2.4. Computation of the field measurements
Maruhubi forest system is relatively open to
tidal flushing. Mass balance studies are limited by
the accuracy of estimation of rates of discharge.
Per tidal cycle POC and DOC fluxes were calcu-
lated by multiplying average concentration of
each zone with estimated net exchange of water
between the zones. Values were integrated over a
complete tidal cycle (about 12 h) to obtain net
Fig. 5. POC sub-model showing compartments and sinks (MF; combined SL and LE; TF; and sedimentation). Fluxes of POC
include input of POC from the ocean and standing stocks of POC in the forest zones (MF–POC; SL–LE–POC; and TF–POC).
POC to DOC is a POC sink that is further degraded into DOCin the sediment. Model and observed (in parentheses) values are
given in Mg org.C year−1.
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8376
Fig. 6. DOC sub-model showing the fate of DOC in the forest zones. Compartments are the Ocean; MF; combined SL and LE; and
TF). Fluxes and sinks of DOC (mainly removal in the MF sub-area by organisms) are shown. Model and observed (in parentheses)
values are given in Mg org.C year−1.
material transport (Spurrier and Kjerfve, 1988).
Volume of water was estimated by multiplying the
area of each forest zone with the mean depth of
water of that zone. The within forest standing
stock of DOC and POC were calculated by multi-
plying the concentration per unit volume with
total volume of water at mean water depth within
a given forest zone. Litter transport was estimated
by multiplying the mass of trapped litter (per unit
length of net), with the length of the boundary
line between given sub zones of the forest. It was
assumed that cross-sectional variability in litter
transport within given boundaries was small.
Amount of leaf foraged by a crab was deter-
mined after 24 h, as the difference between the
initial wet weight of half leaf and the wet weight
of the remaining leaf portions. Weight increase of
leaf by water absorption due to exposure of meso-
phyll tissue was checked using a control for each
half leaf. Rate of litter removal by crabs was
estimated by multiplying the average per capita
leaf consumption with the numerical abundance
of crabs in a given forest zone or in the entire
forest.
3. Results and discussion
3.1. Leaf litter remo�al by crabs
Crab size correlated well (Pearson r=0.81,
P=0.027) with the amount of leaf material in-
gested per day (Table 2). With an average number
of 21 sesarmid crabs per m2, the TF zone sup-
Table 2
Consumption of A. marina leaf by the crabs N. meinerti (size
classes between 10 and 60 mm) and C. carnifex (size classes
between 60 and 80 mm)
Size classes of crabs Rate of consumption
(Carapace width mm) (mean�SD mg dw crab−1
day−1)
10–19 (n=5) 15.7�4.9
20–29 (n=5) 22.3�8.2
30–39 (n=8) 64.5 �32.8
40–49 (n=6) 89.8�57.6
72.6�41.250–59 (n=4)
60–69 (n=5) 443.0�203.4
70–79 (n=5) 957.4�231.9
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–83 77
ported a sesarmid population of 3.36 million.
Mean carapace width for the crabs was estimated
at 30 mm, a crab of this size would consume
about 23.73�12.05 g dw of litter year−1 equiva-
lent to 10.59�5.48 g org.C year−1. Similar feed-
ing experiments have been conducted, for
instance, Leh and Sasekumar (1985) estimated
mangrove leaf consumption by Chiromantes ony-
chophorum (carapace width 11–16 mm) in the
laboratory to be 14.97�7.67 g dw year−1 per
crab. The estimate for C. eumolpe (carapace width
9.7–18.4 mm) was 12.78�3.29 g dw year−1 per
crab. Emmerson and McGwynne (1992) reported
ingestion rates in the laboratory of between 26.65
and 168.27 g dw year−1 per crab for Sesarma
meinerti de Man. Rearing of crabs in the labora-
tory may underestimate their rate of feeding. Un-
der field conditions, grapsid crab removal of litter
includes consumption and storage in their
burrows.
Analytical results showed that A. Marina dry
leaves contain �45% orgC. Relevant figures for
TF zone (e.g., field estimates of mean crab density
and laboratory estimate of crab ingestion rates)
were applied to estimate litter removal by crabs.
Calculations reveal that sesarmid and gecarcinid
crabs consume 498.23�252.95 g dw leaf litter
m−2 year−1. This amount was equivalent to
68.6% of litter production in the TF zone, the rate
of consumption in the LE zone was equivalent to
14% of litter fall.
3.2. Parent model
The conceptual framework for this model al-
lows it to be used in an environmental setting
similar to Maruhubi site. The assumptions of the
model were: the import of litter from other adja-
cent marine ecosystems was only via the ocean–
MF boundary; there was no net import of
non-mangrove litter from adjacent marine ecosys-
tems; all the litter that was taken into the burrows
by crabs was eventually consumed; the number of
crab holes m−2 closely represent the number of
crabs m−2. Sub-models were constructed using
observations in the field, i.e., organic carbon was
exported to the ocean in the form of DOC (62 Mg
org.C year−1) and macrodetritus (18 Mg org.C
year−1) only; organic carbon was imported to the
forest in the form of SPM (7 Mg org.C year−1).
Litter (69 Mg org.C year−1) is fragmented into
POC, and is exported to the POC sub-model.
POC (98 Mg org.C year−1) is degraded into DOC
in the forest sub zones and is exported to the
DOC sub-model. The sub-models are linked to
the parent model as shown in Fig. 1. Raw data of
compartments, variables, standing stocks, flows
and rate constants is available from the corre-
sponding author.
The fate of organic carbon in the mangrove
forest involved a series of degradation steps from
production to the final stage of export to the
ocean. Litter production (mainly leaves) is an
index of primary production. Leaves form the
basis for the organic carbon flux through the
mangrove ecosystem. Leaf litter from the man-
groves constitute LOC, which is the major organic
carbon input of the system. Primary production in
the ocean formed another essential input of car-
bon as POC. One of the sensitive parameters that
controlled DOC fluxes between the mangrove
ecosystem and the ocean was tidal amplitude and
flow velocity of tidal current for LOC. Hydrody-
namics affected the rate of within system organic
carbon transport and accumulation. Therefore,
changes in the fluxes significantly affected the
standing crops of organic carbon in the zones of
the mangrove forest.
3.3. Sub-model litter organic carbon
Fig. 4 shows annual input (variables), standing
crops of litter (compartments) and fluxes of litter
in the mangrove zones. Crabs remove litter from
the forest sub zones TF and SL–LE (36 and 3 Mg
year−1) and bury it in the sediment, where it is
degraded. This makes the TF zone especially rich
in organic matter. Removal of litter by grapsid
crabs was the predominant sink for litter in the
TF zone. Crabs dragged leaves down their bur-
rows as well as consuming them on the sediment
surface (Machiwa and Hallberg, 1995). These
crabs fragment leaf litter and return the nutrients
as faecal pellets which can be easily degraded by
micro-organisms, enhancing POC and DOC pools
of the forest (Robertson, 1987).
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8378
Results suggest that sesarmid crabs have a sig-
nificant quantitative impact on litter removal
(68% of litterfall) from the TF sub-area of the
forest. The TF zone had the highest amount of
litter input in the system (331.3 g. orgC m−2
year−1). This fraction of litter is available for
export only during highest spring tides. Robertson
(1991) has reported similar observation. He found
that Sesarma messa consumed or buried at least
154 g m−2 year−1 or 28% of the annual leaf fall
of 556 g m−2 year−1. His observations were
restricted to the low and mid-intertidal forests of
Rhizophora spp. that are tidally flushed twice per
day. Robertson and Daniel (1989) also estimated
that in the high intertidal mangroves dominated
by Bruguiera or Ceriops, crabs removed up to
79% of the total annual litter fall. Mean instanta-
neous standing stock of leaf litter on the floor
where crabs exist was low. About 1% of annual
litterfall is removed by in situ microbial decompo-
sition per se in intermittently flooded forests
(Robertson and Daniel, 1989). Earlier, Valk and
Attiwill (1984) estimated the processing (immedi-
ate consumption or storage) of freshly fallen litter
by the macro detritivores such as grapsid crabs as
40% of total litterfall in the daily inundated man-
grove zones. Variation in the litter removal rates
reflect the between sites differences in the tidal
regimes and food habits of the grapsids.
Imbalance between litterfall, standing crop and
litter transport was evidentin the SL–LE zone,
where litter standing crop of the model (15 Mg
org.C) suggested a higher rate of litterfall than the
observed value (Fig. 4). Model results showed
that the observed litter standing crop (10 Mg
org.C) in the SL–LE zone was underestimated by
30%. Discrepancy between the observed and
model data was because of the presence of short
scrub plants in the SL–LE zone, which were
efficient in trapping lateral flux of litter. These
shrubs also were a problem in estimation of
canopy cover and hanging of litter baskets. SL–
LE litter, was a variable that represented litter
which was accumulated at the spring high tide
mark of the SL–LE zone. This fraction of litter is
fragmented by physical factors and decomposed
in situ by benthic microbiota. The SL–LE zone
was not exporting any litter to other zones. Re-
sults from the model (Fig. 4), concluded that in
addition to the crabs, the major sink for litter in
the SL–LE zone was fragmentation by physical
factors and in situ decay (12 Mg org.C year−1).
Litter in the MF zone was mainly exported to
the ocean (18 Mg org.C year−1). In situ decay
removed 9 Mg org.C year−1, and 5 Mg org.C
year−1 was transferred to the SL–LE zone. Flows
to the degradation compartment were given val-
ues to balance the compartments in accordance
with observed values of standing crop in the
forest sub-areas. These flows, as well as 39 Mg
org.C year−1 of faecal material from crabs en-
tered the degradation compartment as POC and
were further exported to the POC sub-model.
Unlike in Florida where almost all litter is
flushed (Twilley et al., 1986), at Maruhubi the
sesarmid crabs exert a major impact on leaf litter
turnover in the landward part of the forest. Simi-
lar observations have been reported from tropical
Australia, Malaysia and South Africa (Leh and
Sasekumar, 1985; Robertson, 1986; Emmerson
and McGwynne, 1992). In support of Emmerson
and McGwynne (1992), the model results suggest
that the TF zone mangroves are ecologically im-
portant. TF zone supports a large macrofaunal
biomass that process mangrove litter, therefore, it
plays a major role in the flow of energy in
Maruhubi forest. Results of macro detritus trans-
port revealed that tidal export of litter in the TF
zone is not so effective. High litter production in
the TF zone coupled to high abundance of crabs
ensures retention of nutrients in the forest (un-
published phosphate data). This possibly creates a
large nutrient sink in the TF zone, which was
flushed to the marine environment by tidal, storm
and ground water flow mostly as DOC.
3.4. Sub-model particulate organic carbon
There was a net import of POC from the ocean
to the mangrove area, which thus was acting as a
filter for the ocean water of the Zanzibar channel,
thereby enhancing the environment for the sur-
vival of the neighbouring coral reefs. Inputs of
POC in the three zones were calculated as directly
proportional to the retention time of tidal water
in each separate zone, which has been multiplied
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–83 79
Table 3
Data derived from the model in Mg org.C year−1 unless
otherwise noted
MF SL–LE TF
9Degradation/fragmentation of litter 12 9
to POC
3Faecal POC (crabs) 36–
414 12Deposition of POC
24Transformation of POC to DOC 16 59
7Flux of DOC to overlying water 88
–22 –Removal of DOC by organisms
5Rate of sedimentation (mm year−1) 1 3
33 43 14Rate of POC mineralization (%
year−1)
be an overestimation of the real situation, because
resident and tidal migrant fauna consume part of
the POC. The model also showed that sedimenta-
tion in the MF zone was accompanied by high
rate of POC mineralization (Table 3). Observed
and model data for POC mineralization in the
forest sub-areas compares well, except for the TF
zone where the observed rate is twice the model
rate. Discrepancy between the observed and
model values for the TF zone may be explained
with the TF zone containing a more pronounced
amount of litter than the other zones, while the
material used for field observations was only
POC.
3.5. Sub-model dissol�ed organic carbon
Standing crops and net flows of DOC from the
mangrove forest zones to the ocean are shown in
this sub-model (Fig. 6). Like in the POC sub-
model, all inputs into the three zones were calcu-
lated from the retention time of tidal water in
each forest sub zone. In order to balance the
model with observed standing crops and fluxes,
additional DOC was imported from the SED
compartments of the POC model. Decay of POC
in the sediments of the mangrove zones increased
the magnitude of the flow of DOC to the ocean.
DOC was exported from the forest as a result of
in situ decay of macro-detritus and particulate
matter. The model showed an imbalance between
DOC production in the forest and export at the
MF-ocean water boundary. DOC discharge into
the ocean amounted to 62 Mg. year−1, and the
DOC mass balance was achieved by removal of
DOC from the water column by organisms in the
MF sub-area. This amounted to about 22 Mg
year−1 which was removed from the water
column when the MF zone was inundated. Possi-
ble sinks for DOC in the MF zone included
removal by macrofauna, bacterial and microalgae
utilisation and absorption of dissolved organic
nitrogen by mangrove rootlets. Muller (1998) ad-
vocates that, in an open system structures are
created and can be detected using ecological gra-
dients which build up in the system. Camilleri and
Ribi (1986) reported that flocculation of DOC
and formation of flakes, feeding of the flakes by
with the observed standing crop of POC. Accord-
ing to the model (Fig. 5), the SPM (7 Mg org.C
year−1) import to the forest from the ocean has a
high impact on the rate of sediment accretion in
the MF zone. POC was deposited in the MF zone
during the high tide flow. Most of the POC from
the autochthonous suspended matter generated in
the SL–LE (10 Mg org.C year
−1) was removed
from the water column in the TF zone by sedi-
mentation (12 Mg org.C year−1). The accumula-
tion of organic carbon in SED compartments was
used to balance the model with respect to stand-
ing crop data and flow rates between the compart-
ments of MF, SL–LE and TF. The accumulation
in the SED compartments was further enhanced
by the import of degraded litter from the litter
sub-model, which was distributed between SED
compartments in accordance with the inputs to
the degradation compartment of this sub-model
(Table 3). Material balance of the model sug-
gested that litter removed by crabs was turned
into faecal POC, which was deposited in the TF
sediments. Crab faecal material and SPM con-
tribute POC (39 Mg org.C year−1) to the TF
sediment (litter sub-model). Calculated values for
the rate of sedimentation in the forest sub-areas
(Table 3) were derived from the models rate of
accumulation of carbon in the sediment of each
specific mangrove zone and the average amount
of observed carbon in the uppermost 5 cm of the
sediment from these zones (Machiwa, 1998).
Model data for rates of sediment accretion may
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8380
tidal migrant (e.g. juvenile fish and crustaceans)
and resident macrofauna was a prominent DOC
sink in mangrove systems.
3.6. Ad�antages of the empirical model
In general, the model provides good estimates
of field conditions of organic carbon dynamics
(Table 4). For instance, the model may answer the
following questions: What would happen to the
system if clear felling of trees occurs in the MF or
TF zones?; What is the implication of clear cut-
ting trees in the TF zone to mangrove fauna?; If a
large proportion of trees in the MF zone is to be
clear cut, the export of litter to the ocean will
decrease tremendously. Dynamics of DOC and
the deposition of POC will be impacted to a
greater extent. Clear cutting of trees in the TF
zone will wipe out a large number of litter eating
crabs, litter turnover will take a longer time than
in the presence of crabs.
What would be the impact of sewagedisposal
in the TF zone? This was actually the case be-
tween 1970s and 1993 when about 5 Mg of wet
sewage (mixed with sand) per day was dumped in
the TF zone. The model gives an estimate of
annual amount of organic carbon accumulated in
the sediments of respective area. Numbers are
derived from balancing the model data of stand-
ing crops and fluxes with observation data. The
model allows simulation of the influence of hu-
man perturbation of mangrove organic carbon
budget. Sensitivity tests reveal that disposal of
sewage wastes in the form of POC in the TF zone
results in accumulation of POC in this zone only
with negligible effects in the ambient areas (com-
pare Fig. 7a and b). Alternatively, if sewage is
dumped at the SL–LE zone, the rate of degrada-
tion is high, and a small accumulation takes place
in this zone but again increased accumulation is
noted in the TF zone (Fig. 7c). Sewage disposal in
mangrove areas can, therefore, be beneficial, haz-
ardous or both, depending on a number of fac-
tors. Long term discharge of sewage can bring
intense anoxic chemical conditions that are offen-
sive to the resident and tidal migrant fauna. High
organic carbon loading causes de-oxygenation in
the sediments of the TF zone, initiating anoxic
sediment reactions. In connection with the role of
grapsid crabs in the structure and function of
mangrove systems, Smith et al. (1991), found that,
in plots where crabs were removed, sulphidic con-
ditions developed quite rapidly and the ammonia
level was high. In addition, total number of ma-
ture propagules that were produced was signifi-
cantly low at sites where crabs were removed
compared to control plots with crabs. Grapsid
crabs, therefore, can have profound benefit in
sewage contaminated mangrove areas, such as
enhancement of aeration and propagule perfor-
mance in sulphidic sediments.
The modelling approach has attempted to
achieve a holistic assessment of the behaviour of
organic carbon in the mangrove ecosystem. The
model has demonstrated that the flux of organic
Table 4
Comparison of some observed mean values and model results
of organic carbon (org.C) from macro-detritus, SPM and
DOC of the mangrove forest
ModelObserved
Litterfall in forest zones (Mg org.C
year−1)
32.2Marine fringe 32.2
SL and LE combined 10.3 14.6
52.6Terrestrial fringe 52.6
Flows of org.C within and between
the forest and the ocean (Mg org.C
year−1)
Macro-detritus:
17.817.0MF to ocean
5.25.8MF to SL and LE combined
8.08.3TF to SL and LE combined
Suspended particulate matter:
7.2Ocean to MF 7.2
6.2MF to SL and LE combined 6.1
9.8 9.6SL and LE combined to TF
Dissol�ed organic carbon:
MF to ocean 6062.0
25.4 25.4SL to MF
LE to SL 11.811.2
8.6TF to LE 7.6
Crab remo�al of litter (Mg org.C
year−1):
2.7Combined SL and LE zones 1.9
36.1Terrestrial fringe 36.2
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–83 81
Fig. 7. Sensitivity test on annual accumulation of organic carbon in the sediment with varying inputs of sewage in the form of POC.
Graph (a) represents steady state with no addition of sewage. Graph (b) represents an input of 20�15 Mg to the SL–LE zone and
(c) represents the same input into the TF zone.
J.F. Machiwa, R.O. Hallberg / Ecological Modelling 147 (2002) 69–8382
Fig. 7. (Continued)
material from the forest depends on the extent of
mangrove cover and the hydrodynamic properties
of the system. The model confirms, using field
data that a large proportion of mangrove organic
carbon is channelled into in situ utilisation by
mangroves and juveniles of fish as well as crus-
taceans, molluscs, and insects.
Considering the constraints of sampling in the
field, this model was an attempt to give site-spe-
cific description of the dynamics of organic car-
bon within the forest and between the forest and
adjacent ocean. The empirical model has gener-
ated some data that otherwise would be difficult
to retrieve by sampling within the mangrove
forest (Muller, 1998).
Acknowledgements
Anonymous reviewers are thanked for their
critical comments. SIDA/SAREC East African
Programme in Marine Science funded the project.
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	An empirical model of the fate of organic carbon in a mangrove forest partly affected by anthropogenic activit
	Introduction
	Materials and methods
	Construction of the model
	Estimation of mangrove leaf removal by crabs
	Determination of organic carbon in the forest
	Computation of the field measurements
	Results and discussion
	Leaf litter removal by crabs
	Parent model
	Sub-model litter organic carbon
	Sub-model particulate organic carbon
	Sub-model dissolved organic carbon
	Advantages of the empirical model
	Acknowledgements
	References