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Whole food webs studies – Mangroves

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Scharler UM (2011) Whole Food-Web Studies: Mangroves. In: Wolanski E and

McLusky DS (eds.) Treatise on Estuarine and Coastal Science, Vol 6, pp. 271–286.
Waltham: Academic Press.

© 2011 Elsevier Inc. All rights reserved.

 Author's personal copy

6.12 Whole Food-Web Studies: Mangroves

UM Scharler, University of KwaZulu-Natal, Durban, South Africa
© 2011 Elsevier Inc. All rights reserved.

6.12.1 Introduction 271

6.12.2 Food Web 272
6.12.2.1 Primary Food Sources 272
6.12.2.2 Who Eats Who? – Main Energy Sources and Consumers 274
6.12.2.2.1 Use of primary producers 274
6.12.2.2.2 Links among heterotrophs 276
6.12.2.3 Connections to Adjacent Ecosystems (Imports/Exports) 278
6.12.3 Ecosystem Functioning (Whole Food-Web Studies) 279
6.12.4 Carbon, Nitrogen, and Phosphorus Turnover of Mangrove Systems 283
6.12.5 Concluding Remarks 283
References 284

Abstract

Whole food-web studies of mangrove ecosystems are rare. However, several components of the flora and fauna and selected
linkages from primary food sources (primary producers and detritus) and between heterotrophs have been studied in detail.
Considerable attention has been given to carbon imports and exports from mangrove ecosystems in the form of Dissolved
Organic Carbon (DOC), Particulate Organic Carbon (POC), and CO2. The comparatively few whole food-web studies on
mangroves from different continents thus far produced fairly wide ranges (and thus few generalizations) of ecosystem level
indices, including trophic efficiencies, extent of recycling, or total energy throughput.

6.12.1 Introduction living and nonliving constituents as well as among different

Mangrove ecosystems typically span intertidal regions in trop­
ical and subtropical areas of the globe between latitudes of 30°
north and 30° south (Kathiresan and Bingham, 2001; see
Figure 1). The most northern distribution limit is found in
Japan and Bermuda, whereas the southern limits are in
Australia, New Zealand, and the east coast of South Africa
(Steinke, 1999; Kathiresan and Bingham, 2001, and references
therein). The southernmost mangroves are found in Australia
(Victoria) at 38°45′ (Hogarth, 2007). Mangrove forests estab­
lish themselves along estuaries, river deltas, along continental
margins, along the fringe of islands, or are forming islands.
They establish themselves along the tidal gradient between
mean sea level and mean high water spring tide level
(Steinke, 1999). The mangrove habitat is characterized by dif­
ferences in the extent of tidal inundation, and various physico­
chemical parameters including salinity, and oxygen and
nutrient levels (Steinke, 1999; Kathiresan and Bingham,
2001). Due to their intertidal position, mangrove ecosystems
include a variety of fauna that span terrestrial (e.g., insects),
semi-terrestrial (e.g., crabs and mollusks), and aquatic organ­
isms (e.g., root fouling organisms and fish). As such, they are
characterized by three-dimensional habitat niches above and
below sea level. The terrestrial and aquatic habitat is interlinked
in mangrove ecosystems, and energy and nutrients move
between them through tidal action, nutrient, and other chem­
ical diffusion and cycling among the biotic and abiotic
constituents. Mangrove ecosystems can thus support a diverse
fauna and flora, and the opportunity for linkages among the
habitats is well established in the literature.
Mangrove ecosystems provide numerous services to
humans, ranging from food resources to building material to
protection from wave action. In order to comprehensively
understand the services and their functioning, the investigation
of entire food webs that encompass information on species,
communities, the abiotic environment, and their interactions
are important.
Traditionally, there has been a focus on mangrove trees and
crabs in mangrove ecosystem-related studies, and on commer­
cially exploited species (e.g., prawns and trees). Thereafter, a
shift of focus to other primary producers, notably microalgae
and cyanobacteria, was apparent; the focus was also on
imported primary producers such as phytoplankton from adja­
cent estuaries and lagoons. In terms of fauna, there has been a
shift to gather information on other benthic invertebrates.
Insects were studied especially in terms of loss of production
of mangrove trees and as ecosystem engineers. Once isotope
studies were used in mangrove ecology, the interrelationship
between certain fauna and primary producers was elucidated,
as was the relative importance of several primary producer
groups as food sources.
Of the nutrients, carbon flow studies were those that
embraced a community or ecosystem view and describe
organic carbon transfers in mangrove ecosystems. They focus
on fixation by primary producers, on imports and exports of
dissolved and particulate carbon from the entire system, con­
sumption by crabs, decomposition of mangrove litter, and
sediment pathways of carbon.

271
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
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272 Whole Food-Web Studies: Mangroves
Figure 1 Overview of mangrove distribution across the globe.
Previous so-called ecosystem-level studies were restricted to
parts of the ecosystem, such as carbon turnover by mangrove
trees scaled up to an entire forest, or the entire globe, or carbon
imports and exports of an entire system (see, e.g. Alongi, 2009).
Studies that take the entire food web from primary producers to
top consumers, including abiotic food sources, into account are
few, and most have put the adjacent estuary, lagoon, or reef
area that are fringed with mangroves as primary focus.
However, there have been a few whole food-web studies spe­
cifically on mangrove ecosystems that include energy and
nutrient flows between species and species groups, namely on
the mangrove system in South Florida (Ulanowicz et al.,
1999a), the Sundarbans in India (Ray et al., 2000), Twin Cays
in Belize (Scharler et al., in preparation), the Caete estuary in
Brazil (Wolff et al., 2000), and the Golfo de Nicoya, Costa Rica
(Wolff et al., 1998). Gribble, (2005), for example, produced a
linked mangrove, lagoon seagrass, and coral reef system model
of the Great Barrier Reef, Australia, with the focus not on the
mangroves themselves, but on target fisheries in the region. In
essence, the various ecosystem-level studies include various
scales of the ecosystem. Some include the mangrove ecosystem
proper, putting the boundaries at its edge, whereas others
include adjacent ecosystems of estuaries, creeks, and seagrass
or coral systems.
6.12.2 Food Web
Whole food-web studies in mangroves are, as in other ecosys­
tems, rarer as compared to studies on individual organisms or
groups, and feeding or behavioral links between those. The main
focus of studies in mangrove ecosystems has often been that of
mangrove trees, its most conspicuous primary producer, and
habitat provider for various trophic levels. In this section, the
most important food sources in terms of (1) the first trophic level
(primary producers and detritus), (2) the remainder of the food
web, as well as (3) linkages between and within these groups are
elucidated. This serves to give an overview of the main energy
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
sources, the main energy consumers, and the inter-linkages with
adjacent habitats. The narrative is focused on the processing of
energy or carbon, and the main processors within the mangrove
community. It is not intended to give a comprehensive overview
of individual geographic localities, or species.
6.12.2.1 Primary Food Sources
Primary food sources in mangroves include the mangrove trees,
micro- and macroalgae, microbial mats and imported auto­
trophs (e.g., phytoplankton), as well as detritus from within
and from adjacent ecosystems. Mangrove trees feature the larg­
est biomass of the primary producers, and they are responsible
for making mangrove ecosystems net autotrophic (Alongi,
2009). However, several primary producers are important
food sources to higher trophic levels, recycle nutrients, and
capture atmospheric carbon and nitrogen. The main focus of
basal energy resources in mangrove ecosystems has historically
been on the amount of leaf litter produced that sustains her­
bivorous crabs or adjacent ecosystems. Although mangrove
leaves have low nutritional content (high C/N ratios), they
are often cited as important carbon sources for primary con­
sumers (Camilleri, 1992; Cannicci et al., 2008).
However, several studies have highlighted the importance
of algal food sources and imported plant detritus as a trophic
link to benthic invertebrate communities (Bouillon et al.,
2002a; Kristensen et al., 2008). Benthic microalgae achieve
higher biomass in light gaps, and growth is limited by light
and tannins (Alongi, 1994). Benthic microalgae are thus
expected to contribute more to higher trophic levels in forests
where sufficient light reaches the forest floor, and moisture and
nutrient availability are adequate. However, their overall con­
tribution to the mangrove food web has mostly received little
attention. An example of significant nitrogen contribution of
N-fixers to mangrove ecosystems is that of Twin Cays, Belize,
where the interior of the island is populated by dwarfed
Rhizophora mangle (Feller et al., 2003) that provide sufficient
light gaps for other primary producers to grow (Figure 2). The
 Author's personal copy
Figure 2 Zone of Rhizophora mangle dwarf trees in the interior of Twin Cays, Belize.
nutrient pool is supplemented by nitrogen-fixing cyanobacteria
in microbial mats who supply nitrogen to this nitrogen-limited
environment (Lee and Joye, 2006), which in turn can be used
by benthic algae and mangrove trees. In areas where light
availability is reduced due to dense mangrove tree stands,
microbial mats were found to compete with mangrove trees
for nitrogen via denitrification (Lee and Joye, 2006). Since
microbial mats can make up to 80–90% of the organic carbon
of sediments (Wooller et al., 2003), this primary food source
can be of high significance to the mangrove food web. Mann
and Steinke (1993), who investigated nitrogen fixation by
cyanobacteria in a mangrove in South Africa (Beachwood at
Mngeni estuary, see Figure 3), similarly found a high contribu­
tion of nitrogen to the mangrove ecosystem via this pathway,
which was calculated at about 24% of the annual nitrogen
requirements of the mangrove system.
Phytoplankton can be imported during high tides and be
consumed once deposited. Its contribution to the mangrove
system varies with geomorphology (habitat availability for
phytoplankton and mangrove area inundated during high
tides), currents and nutrient levels (Kristensen et al., 2008).
Similarly, plant material can be imported from beyond the
terrestrial edge of the mangrove ecosystem and contribute to
the detritus food web. The terrestrial carbon contribution to
Figure 3 The Mgeni estuary mouth, with mangroves. Durban, South Africa.
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
Whole Food-Web Studies: Mangroves 273
mangrove ecosystems has not received the same amount of
attention compared to imports from estuaries and the sea.
Mangroves are efficient traps for debris due to their root system,
and associated macroalgae growing on roots.
Lichen as primary producers and potential food sources
have not been studied in any great detail in mangrove ecosys­
tems, and the only ecological study published to date describes
unusually negative δ15N values in lichen and mangrove leaves
on Twin Cays, Belize (Fogel et al., 2008). On this mangrove
island, a nutrient-limitation gradient and concomitant tree
height gradient are apparent (e.g., Feller et al., 2003). By ana­
lyzing δ15N values from NH4+/NH3− in pore water, rainwater,
and atmospheric ammonia, lichen and microbial mats were
analyzed as a proxy of organisms that use atmospheric nitro­
gen, in order to establish whether mangroves are able to utilize
this source and so provide an explanation of their highly neg­
ative δ15N values (Fogel et al., 2008). Fogel et al. (2008) were
able to establish that these values were not a result of fractio­
nations during pore-water nutrient uptake through the analysis
of roots, stems, and leaves, but rather that leaves are able to use
atmospheric nitrogen in nutrient-limited conditions. In the
interior of Twin Cays, R. mangle trees exhibit dwarf growth
due to severe phosphorus limitation that prevents effective
functioning of the hydraulic system and thus utilization of
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274 Whole Food-Web Studies: Mangroves
pore-water N and other nutrients (Lovelock et al., 2006a,
2006b). Atmospheric N therefore supplements the production
and maintenance of mangrove trees under such nitrogen-limit­
ing conditions via leaf uptake (Fogel et al., 2008).
The importance of primary food sources other than leaf
litter from mangrove trees is highlighted through above exam­
ples. The exact contribution of each source to higher trophic
levels can be highly variable within and between different
mangrove ecosystems. Global averages of the proportional
contribution of mangrove ecosystem primary producers
might be misleading information when applied back to indi­
vidual systems, with knock-on effects for their management.
Kristensen et al. (2008) summarize the production of var­
ious primary producers in the mangrove system, which
constitutes trophic level I of the mangrove food web. There
have been many studies on mangrove productivity, and these
have been criticized for only including litter fall as a measure
of productivity, thereby ignoring wood and above- and
belowground root productivity (see Kristensen et al., 2008).
First inclusions of wood and root production in overall man­
grove primary production (PP) estimates significantly
increased overall mangrove PP estimates, for example, from
38 mol-C m−2 yr−1 of litter fall to 105 mol-C m−2 yr−1 (both
global averages; Twilley et al., 1992). A global average of
mangrove root production has been estimated at 44 mol-
C m−2 yr−1 (Kristensen et al., 2008), thus increasing overall
mangrove tree primary productivity fourfold compared to
leaf litter productivity only (Table 1). The global averages
are based on a variable number of observations, and further
studies are needed to increase the confidence in estimates on a
global scale (see Kristensen et al., 2008). Data are overall too
scarce and locally variable to estimate a global average for
other primary producers in mangrove ecosystems. Table 1
therefore includes two examples of mangrove ecosystems
that have been studied using ecological network analysis
(ENA), which uses, among other data, estimates of net PP of
the various primary producer groups. From these data, it is
equally apparent how variable data are, and a range of values
might be more appropriate than a mean of the relatively few
measurements available.
Another set of global averages is available from Alongi
(2009), who estimated a net PP of ecosystem production of
about 150 Tg-C yr−1. The same caution on the relatively scarce
data availability of sufficient representative mangrove ecosys­
tems applies here, as well as for the individuality of mangrove
ecosystems for the calculated values that might not be repre­
sentative of all mangrove systems.
In summary, mangrove trees have undoubtedly the biggest
biomass in mangrove ecosystems. In addition to providing
Table 1 Comparison of net productivity of various primary producers in mangrove ecosystems
Ecosystem Trees
Global average 149 mol-C m−2 yr−1
Global average 1930 g-C m−2 yr−1
Sundarbans, India
South Florida mangroves 410 g-C m−2 yr−1
Twin Cays, Belize 2193 g-C m−2 yr−1
Data from Kristensen et al. (2008), Alongi (2009), Ray (2008), Ulanowicz et al. (1999a), and Scharler et al. (in preparation).
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
habitat, they are of high importance in providing biomass to
other organisms in the food web, as well as biomass (e.g., leaf
litter) and organic and inorganic carbon to adjacent ecosystems
via export as leaf litter, leachates from leaf litter and respiration.
However, primary producers other than mangrove trees have
enjoyed increased attention over the past years. In particular,
the ability to fix nitrogen in nutrient poor areas by cyanobac­
teria and lichen in mangroves has been studied in a greater
number of studies and has highlighted the importance of such
organisms to the remainder of the food web. The uptake of
atmospheric nitrogen via leaves has been the subject of an
ecological isotope study in mangroves (Fogel et al., 2008),
and has revealed an important pathway of nutrient gain in
nutrient poor soil conditions.
6.12.2.2 Who Eats Who? – Main Energy Sources and
Consumers
In this chapter, the different food sources of heterotrophs are
described to elucidate the trophic importance of each food
source and that of consumers in mangrove ecosystems. There
are many resident and transient fauna, which highlights the
importance of mangrove systems to fauna inhabiting sur­
rounding ecosystems and using the same as main or seasonal
feeding grounds. On an ecosystem level, this is quantified as
imports and exports to and from a mangrove ecosystem.
6.12.2.2.1 Use of primary producers
The consumption of primary producers has received consider­
able attention in mangrove ecosystems. As mentioned above,
the main focus in mangrove studies has mostly been on
mangrove trees, and their contribution to higher trophic levels
(e.g., crabs and mollusks) via leaf litter has been considered as
one of the main paths of energy transfer. The production of
mangrove litter was deemed of high importance by Odum and
Heald (1972), to the extent that mangrove litter was recognized
to provide a major outwelling pathway of energy to adjacent
ecosystems, thus supplementing these system’s energy supply.
Later studies have not always found evidence to support this
hypothesis, and due to an increased focus on primary producers
other than trees, and on the nutritional quality of these sources,
the functional role of mangrove litter as an intertidal food source
and contributions to neighboring ecosystems has become some­
what clearer (e.g., Bouillon et al., 2002b; Alongi, 2009).
Crabs have had the limelight of studies on the invertebrate
fauna in mangrove ecosystems. Their roles as litter consumers
and particle transformers have received considerable attention,
but their role as prey to birds and reptiles, and to predators
from adjacent systems during inundation of intertidal areas has
Lichen Macroalgae Microbial mats Benthic microalgae
110–118 mol-C m−2 yr−1 7–73 mol-C m−2 yr−1
9315 kcal m−2 yr−1
291 g-C m−2 yr−1
0.04 g-C m−2 yr−1 142 g-C m−2 yr−1 16 g-C m−2 yr−1
 Author's personal copy
received little attention. As described in Alongi (2009), the
chain-like usage of mangrove litter as proposed by Odum and
Heald (1972) has been replaced by an understanding of the
wider role that crabs play in connection with mangrove litter.
The role of crabs in leaf litter removal is well documented
(Steinke et al. 1993; see studies cited in Bouillon et al. 2004b
and Kristensen et al. 2008). Burrowing leaves, which give
microbes a chance for decomposition instead of probable
export, enlarge the mangrove leaf-driven microbial pathway
of nutrient recycling and thus retention within the mangrove
ecosystem. Furthermore, crabs egest a large part of the con­
sumed litter (~50% for sesarmid crabs; Lee, 1997; Thongtham
and Kristensen, 2005) in the form of smaller particles that, in
turn, can be used by other detritivores and microbes. The
availability of this not otherwise readily available food source
is thus increased for many detritivores and is a major energy
source enhancement in an ecosystem with such a large supply
(in terms of weight and volume) of leaf litter whose nutritional
availability largely depends on microbial decomposition. The
transformation by crabs therefore sustains populations of
smaller detritivores, and their impact is accentuated by meas­
urements that, for example, sesarmid crabs can consume
between 30% and 80% of leaf litter in the system (Robertson,
1991). This recycling of leaf litter via breakdown and consump­
tion of egested leaf litter has also been described as a
coprophagous food chain (Lee, 1997). Mangrove leaves thus
still provide a major path of sustenance to the mangrove eco­
system. However, the indirect dependencies on litter by
organisms other than direct litter consumers constitute major
links within these systems (Figure 4). It is not only that the
Litterfall
Remineralization
Breakdown
Consumption
of litter
Breakdown
Consumption of litter
Figure 4 Mangrove trees as a major direct and especially indirect food
source. Conceptual pathway is from trees to leaf litter to leaf litter con­
sumers to breakdown of litter to availability for smaller consumers to
breakdown of leaf litter to remineralizers.
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
Whole Food-Web Studies: Mangroves 275
actual leaf litter is made available through breaking down of
bigger into smaller particles, but knock-on effects such as the
increase in meiofauna feeding on bacteria and microphyto­
benthos that subsequently develop on smaller particles have
been noted as well (Zhou, 2001). Kristensen et al. (2008)
similarly stated the possibility of consumers impacting carbon
dynamics in mangrove ecosystems due to their relatively high
productivity, selective feeding, and improving the availability
of unassimilated food for further consumption.
The bulk of leaves that is consumed is in the form of leaf
litter, whereas a few species also exploit green leaves on trees
(e.g., Aratus pisonii in the neotropics; Alongi, 2009). During leaf
senescence, nutrient resorption takes place and green leaves
may be nutritionally (in terms of N and P content) more
palatable than yellow senesced leaves, although less so than
leaf litter having entered the decomposition stage during which
the microbial degradation again enriches the nutrient content
of leaf litter.
Sesarmid crabs show a high dependency on leaf litter, and
high potential for its removal. Their dependency on this direct
trophic source has been estimated from isotope data as
between 30% and 60%, and their potential of leaf litter
removal as 30–160% of leaf litter fall (Kristensen et al.,
2008). During periods of reduced litter fall relative to the
amount of litter consumers, the consumption requirements
for leaves might thus not be satisfied (Nordhaus et al., 2006;
Kristensen et al., 2008). Next to crabs, gastropods can have a
considerable impact on leaf litter removal (Slim et al., 1997;
Fratini et al., 2008) and have been shown to feed on a wider
range of mangrove tree species and tidal range than sesarmid
crabs (Fratini et al., 2008).
Although microbes are most often viewed as decomposers
and remineralisers, they are of course also consumers in their
own right. Bacteria and fungi are directly dependent on vari­
ous forms of detritus as food sources, and both indirectly and
directly on detritus producers such as primary producers (dead
plant material) and heterotrophs (egestion and carrion).
The re-formation of detritus into forms that are accessible
(e.g., nutrients to primary producers) and more palatable to
heterotrophs (e.g., increased nutrient content of detritus
through selectively accumulating proportionally more
nutrients compared to carbon during decomposition) is an
important function in any ecosystem. In mangrove systems
that have such a high supply of a nutritionally poor food
source (leaf litter), this function is of high significance. The
initial losses of leaf litter are compounds that leach
(e.g. organic carbon), for which microbes have high conver­
sion efficiency. The decomposition of particulate material is
performed by aerobic and anaerobic prokaryotes, and oomy­
cetes (Alongi, 2009), whereas true fungi (ascomycetes) are not
prominent in litter degradation in mangroves (Newell, 1996).
Senescent leaves are degraded at a rate of 0.001–0.1 day−1
(Kristensen et al., 2008), underlining a high-throughput rate
of this material through bacteria and fungi as consumers, as
well as their substantial role in increasing the nutritional
quality (through their attachment to the litter/fragments)
thereof for further consumption. Since microbes are attaching
to surfaces, litter shredders (e.g., crabs and other macroben­
thos) and microbes build a positive feedback loop whereby
shredders increase the surface for microbe attachment, and
microbes increase the nutritional quality of the litter (Hyde
 Author's personal copy
276 Whole Food-Web Studies: Mangroves
and Lee, 1995). More positive feedback exists between
microbes and primary producers, since although they might
compete for the same nutrients, microbes are able to increase
the availability of nutrients to primary producers (Holguin
et al., 2001; Alongi, 2009).
In food-web studies, fungi are usually lumped into one
group, if considered at all, but are highly diverse. In a South
African study, 20–25 species of fungi were identified from
Avicennia marina and Brugueria gymnorrhiza leaves during the
decomposition process (Steinke et al., 1990), whereas 55 spe­
cies were obtained from mangrove wood (Steinke and Jones,
1990). At present, the trophic importance of fungi in mangrove
ecosystems is assessed through rates of litter decomposition,
their diversity and rarely (see e.g. Kohlmeyer and Bebout,
1986) as food sources.
Bacteria were found to be rather indiscriminative of their
carbon sources, specifically in systems with a Total Organic
Carbon (TOC) content of >1 wt.% (Bouillon and Boschker,
2006). Where TOC content was <1 wt.%, bacteria utilized iso­
topically enriched carbon sources, which may be root exudates
or of microphytobenthos origin (Bouillon and Boschker, 2006).
Next to leaf litter consumption, that of propagules and
seedlings has received considerable attention in the literature
(e.g., Robertson, 1991; Lin and Sternberg, 1995; McKee, 1995;
Farnsworth and Ellison, 1997; Sousa and Mitchell, 1999; Feller,
2002). Crabs and insects are involved in these direct trophic
links, and influence propagule dispersion, growth, and recruit­
ment success.
Studies on crabs utilizing various other primary producers,
such as microalgae, epiphytes, bacteria and fungi in microbial
mats, and sediments, have received attention in the recent past
(e.g., Bouillon et al., 2004b). The proportional importance of
these food sources can vary for the same species in different
locations, and different studies on the feeding relations
through isotope signatures sometimes find different feeding
relations for the same consumer genus. As an example, the
following items have all been reported to constitute a major
part of the diet of Metopograpsus sp.: microphytobenthos, littor­
inids, mangrove leaves, or macroalgae (Reid, 1986; Dahdouh-
Guebas et al., 1999; Bouillon et al., 2002a). According to food
availability, species can thus have different priority items in
their diet in different localities. Microalgae as autochthonous
carbon sources in mangrove ecosystems are recognized for their
importance as food sources, as are allochthonous resources
such as imported microalgae and detritus (Dye and Lasiak,
1987; Bouillon et al., 2002a). Many macrobenthic species
have been shown to selectively feed on certain microalgae
(e.g., diatoms and dinoflagellates) or macroalgae (see sum­
mary in Alongi 2009). Fiddler crab species can be selective on
the type of microphytobenthos, for example, for diatoms or
cyanobacteria (Bouillon et al., 2002a). In some systems,
limited overlap of primary producer resources used in benthic
invertebrates has been inferred from stable isotope signatures
(e.g., Bouillon et al., 2002a). Bouillon et al. (2002a), for exam­
ple, showed that δ13C values of mangrove leaves and benthic
invertebrates (crabs, gastropods, and bivalves) hardly overlap
in mangrove forests of the Coringa Wildlife Sanctuary (Andhra
Pradesh, India). In this study, sesarmid crabs and some gastro­
pods derived a major part of their carbon sources from
mangrove tree production (Bouillon et al., 2002a); other
benthic invertebrates were not closely dependent on mangrove
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
leaves even for their carbon requirements and thus use different
primary producer resources. The selectivity of macrobenthos
for certain primary producers and/or detritus has thus been
established.
Benthic mollusks, for example, of the genus Littoraria, uti­
lize epiphytes on tree stems (Bouillon et al., 2002a). The diet of
Littorina angulifera includes lichen, microbial mats, fungi, and
green Rhizophora leaves (Kohlmeyer and Bebout, 1986).
Numerous species of insects feed on and live within parts of
mangrove trees. Leaf miners, stem miners, wood borers, stem
girdlers on mangrove trees, and seedlings all contribute to
herbivory (direct loss of mangrove tree biomass) and indirect
loss of canopy production and seedling recruitment
(Farnsworth and Ellison, 1991; Feller, 1995; Feller and
Mathis, 1997; Feller and McKee, 1999). In addition, there are
numerous species of ants, bees, mosquitoes, termites, flies, etc.,
that have not been studied in any great details in many man­
grove ecosystems, and whose impact on the mangrove system
in a trophic sense has not been evaluated. However, several
species have been studied in terms of abundance and life
history traits (see several references in Nagelkerken et al.
2008). From a trophic point of view, Nagelkerken et al.
(2008) have divided the insect fauna into herbivorous insects,
saproxylic and saprophagous insects feeding on dead and
decaying organic matter, and parasitic and predatory insects.
6.12.2.2.2 Links among heterotrophs
The main focus of most published isotope-related studies in
mangrove ecosystems are related to the primary producers
group, and primary producers and detritus as food sources.
Interrelationships among heterotrophs, on the other hand,
are poorly documented. Equally, the wider diet of species
perceived to be herbivores is insufficiently investigated. One
paradox has always been why leaf litter is such a sought after
food source, since its nutritional content is not very high (Skov
and Hartnoll, 2002). Current knowledge shows that crabs sup­
plement their diet not only with other primary producers that
are richer in nutrients, but probably also by consuming other
heterotrophs, such as invertebrates (Figure 5), for example,
bivalves, gastropods, anomurans, other crabs or carrion, and
insects (Beever et al., 1979; Dahdouh-Guebas et al., 1999;
Thongtham and Kristensen, 2005; Erickson et al., 2008; Lee,
2008; Thongtham et al., 2008).
Among crabs, there are several feeding guilds present. Some
are herbivorous, detritivores, or feed specifically on microalgae,
whereas others are scavengers or predators (Kathiresan and
Bingham, 2001). Scylla serrata, for instance, is a predatory
crab feeding mainly on heterotrophs and is usually regarded
as a top predator in the mangrove community (Bouillon et al.,
2002a).
Since shrimp catches and shrimp farms are very often asso­
ciated with mangroves and are a prominent economic feature,
they are mentioned here for their dependence on mangroves as
a nursery ground for juveniles, coupled with a food supply
originating from both the mangroves themselves and terrestrial
runoff stimulating nearshore productivity (Kathiresan and
Bingham, 2001).
Some of the major gaps that exist in mangrove food-web
studies are, similar to other ecosystems, information on the
small communities such as meiofauna and heterotrophic
microfauna (Bouillon et al., 2002a). Meiofauna has been less
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Figure 5 Aratus pisonii supplementing its vegetarian diet. Photo credit: I.C. Feller.
extensively studied compared to the larger epibenthos (crabs
and molluscs), and within the meiofauna group especially
nematodes and harpacticoids have been studied in greater
detail. Food-web interactions have only been sparsely
described in mangrove ecosystems. One example from Gazi
Bay, Kenya, describes the meiofauna community as isolated,
and predator–prey interactions between meiofauna and epi­
benthos as minor (Schrijvers et al., 1995). Similarly, the
major components of the macrobenthic infauna have been
described as a trophic dead end in the same system
(Schrijvers et al., 1998). These interactions describe direct feed­
ing interactions but disregard the feedback loops that exist via
the detrital pathway (e.g., egestion and carrion). It is also not
apparent from the published literature how important feeding
relations are within the meio- and macrobenthic community
themselves (Lee, 2008). Furthermore, meiofauna has been
described as an important food source for shrimp and fish in
mangrove systems (Coull et al., 1995; Dittel et al., 1997).
Knowledge on this abundant group of organisms in terms of
food web interactions is lacking for mangrove systems
(Nagelkerken et al., 2008).
Fish are mostly residents of adjacent creeks, estuaries,
seagrass beds, and bays, whereas mangrove creeks and subtidal
prop root systems can act as permanent habitats for larvae and
juvenile fish providing protection from large predators
(e.g., Kathiresan and Bingham, 2001). During high tide, they
are able to utilize the food sources of the mangrove system
proper and consume epibenthic invertebrates, primary pro­
ducers and detritus. The extent to which fish can access food
sources of the mangrove system depends on accessibility of the
habitat, that is, length and frequency, as well as extent of tidal
inundation (Nagelkerken et al., 2008). Fish are thus able to
access the bulk of the mangrove system only once the man­
groves are inundated, whereas during low tide, mangrove
ecosystem food sources are available to fish from overhanging
prop roots and exported detritus.
Amphibians have not been studied in mangrove ecosystems
in any great detail. A recent assessment on terrestrial mangrove
vertebrates (Luther and Greenberg, 2009) lists only frog species
endemic to mangroves. No trophic studies are available in the
published literature for amphibians utilizing mangroves.
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Whole Food-Web Studies: Mangroves 277
Reptiles, on the other hand, are conspicuous and far more
numerous in mangrove ecosystems. Snakes, crocodiles, alliga­
tors, lizards, and turtles live in and utilize mangrove food
sources either as resident or as transient fauna. The smaller
reptiles, in turn, are important food sources for birds. The diet
of ground snakes consists of crabs, shrimp, and fish found on
mudflats, among roots and in tidal channels (Luther and
Greenberg, 2009). Snakes living on trees include birds, mam­
mals, and lizards in their diet (Luther and Greenberg, 2009).
However, mammals endemic to mangroves are few (six spe­
cies), feed mainly on leaves, and also include insectivorous bats
(Luther and Greenberg, 2009).
Luther and Greenberg (2009) found that just over half of
the bird species endemic to mangroves feed on insects, almost a
third on crabs, 16% on nectar, and 4% on fish. Birds utilize the
three-dimensional habitat of mangrove ecosystems and forage
from the canopy down to the mudflats, and include aerial
insectivores (Luther and Greenberg, 2009).
Of the vertebrates restricted to mangroves, 32% were found
to primarily depend on food sources only available in man­
grove ecosystems, and forage mainly on crabs, and other
invertebrates and small vertebrates (Luther and Greenberg,
2009). There are many more transient vertebrates utilizing
mangroves for food resources. However, the above discourse
gives an overview of the most important food sources to terres­
trial vertebrates in mangrove systems that are important links
in food webs.
Symbiotic relationships are, when recognized, often not
described in a quantitative fashion in mangrove systems. One
such relationship from mangrove systems has been described
between peritrich ciliates and chemoautotrophic bacteria (Ott
et al., 1998). Facultative mutualism has been described
between root-fouling sponges and mangrove trees (Ellison
et al., 1996), and between zooxanthellae of the upside-down
mangrove jellyfish Cassiopeia xamachana in mangrove ecosys­
tems (Verde and McCloskey, 1998). These mutualistic
relationships involve trophic transfers and energy or nutrient
gain by at least one of the partners, but have not been given
considerable attention. Although there are calculations for sin­
gle species under certain circumstances and for certain
locations, for example, zooxanthellae can satisfy 169% of the
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278 Whole Food-Web Studies: Mangroves
carbon demand of Cassiopeia (Verde and McCloskey, 1998),
the overall importance of such relationships to the mangrove
food web is as yet unclear.
6.12.2.3 Connections to Adjacent Ecosystems (Imports/
Exports)
Ecosystems do not exist in isolation, and mangrove ecosystems
are, as any other, connected to other ecosystems. These con­
nections can be expressed as imports and exports from and to
adjacent systems, from the air, rivers, sea, and through transient
feeders visiting the mangrove system.
One of the important effects of mangrove whole food-web
production is the contribution, or export, of mangrove material
to adjacent ecosystems, notably estuaries, lagoons, seagrass beds,
and coral reefs. The exchange of material with other ecosystems
is dependent on the amount produced in the mangrove ecosys­
tem, and the agents for exchange are tidal action and animal
movement between the systems. Some mangrove ecosystems
export material and nutrients, whereas others might retain their
production (Alongi, 2009). A global average of mangrove net
primary productivity and an estimate for export resulted in an
approximation that mangroves can provide 10–11% of the total
terrestrial carbon input to oceans (Alongi, 2009). CO2 emission
of mangroves has been estimated at about 24% of coastal waters
globally (Alongi, 2009), and mangroves are thus important
contributors of CO2 to the atmosphere. For both inorganic and
organic carbon, mangroves contribute disproportionally to their
spatial extent (Alongi, 2009). The importance of mangrove eco­
systems therefore not only lies in creating a productive and
diverse ecosystem that can sustain itself, but, through its exis­
tence, may also sustain adjacent ecosystems by providing
energy/material and habitat.
Tidal flow is one of the main agents of importing and
exporting material to and from mangrove ecosystems.
Inorganic and organic dissolved substances, particulates, leaf
litter, propagules, bacteria, microalgae, and larvae are so
exchanged between the mangrove system, creeks, estuaries,
seagrass, and coral reef systems. The export and import of
organic matter and microalgae has received considerable atten­
tion, while others, including the exchange of eggs and larvae,
are not well documented (Lee, 2008). Tidal range, habitat
morphology, and tidal flow velocity can differ widely between
mangrove ecosystems and influence the extent of time avail­
able for feeding by visiting aquatic species. Additional factors
that influence the importance of the mangrove habitat avail­
ability for aquatic visitors are frequency of tidal inundation, the
availability of food providing habitats nearby, and type and
amount of predator and prey species present (Sheaves, 2005).
Species involved in the import and export of material in man­
grove systems are represented in the food web, and part of their
energy flow is depicted as import or export from the food web.
Besides energy, nutrients are also exchanged between the
mangrove system and its neighbors. Eggs and larvae have a
considerable lower C/N ratio than mangrove litter and this
export therefore constitutes one of high quality to nearshore
environments (Lee, 2008). Imports of larvae ready for settle­
ment in the mangroves equally constitute a high nutritional
quality import.
Compared to biotic migrations (e.g., for feeding) and imports
and exports of biota, especially in terms of quantities, the export
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and import of dissolved and particulate organic matter have been
explored in more detail. Several studies investigated the uptake
and export of inorganic and organic nutrients from mangrove
systems labeling them both as importers and exporters of various
inorganic and organic nutrients (e.g., Salcedo and Medeiros,
1995; Davis et al., 2001; Dittmar and Lara, 2001; Bouillon
et al., 2008b; Kristensen et al., 2008; Alongi, 2009, and references
therein), emphasizing the individuality of mangrove systems
and their nutrient regimes. According to Kristensen et al.
(2008), a global average seems to emerge that mangroves are a
net source of detritus to coastal waters. The contribution of
mangroves to other ecosystems is often expressed in terms of
carbon, for example, Jennerjahn and Ittekot (2002) estimated an
organic carbon contribution to coastal waters of 46 Tg-C yr−1 (or
11% of terrestrial carbon input to the ocean). Dittmar et al.
(2006) stated that while mangroves occupy less than 0.1% of
the continent’s surface, they produce more than 10% of the
terrestrial carbon input to oceans. DOC can be a considerable
part of the total organic carbon export, for example, 80% in a
Zanzibar mangrove system (Machiwa and Hallberg, 2002).
Whether the same pattern can be derived for various dissolved
inorganic and organic nutrients other than carbon awaits further
investigation. As an example, de Boer (2000) investigated the
contribution of nutrients from mangroves and seagrass beds to
their adjacent intertidal system at Inhaca island, Mozambique,
and found that on an annual basis mangroves supply the bulk
of carbon (330 t-C, 6 t-N, and 0.6 t-P), and seagrass beds the bulk
of nutrients (490 t-C, 30 t-N, and 2 t-P). This study points out
that mangroves can sustain productivity in adjacent ecosystems,
but due to the low-nutrient content of the major export product
(leaf litter), the importance of the export might only be realized
in conjunction with nutrient supplies from elsewhere.
Other studies have found that exported carbon has not had
a significant effect on offshore systems, either because partic­
ulates are trapped in the vicinity of the mangrove system, and/
or because the main fraction exported is that of DOC
(Kristensen et al., 2008). However, these exports can be impor­
tant for nearby ecosystems, such as seagrass beds, where a
mangrove contribution to the benthic mineralization in sea-
grass beds was estimated between 16% and 74% (Bouillon
et al., 2004a). Bouillon et al. (2008a) stated that the major
form of carbon exported to adjacent systems is in the form of
dissolved inorganic carbon (DIC) through tidal export.
Another route of export from mangrove systems are the
transient fauna that export mangrove fauna and flora after
consumption, or import food sources from other ecosystems
as egestion supplementing the detritus pool. They include rep­
resentatives of the major groups discussed in previous sections
above, live and forage in several habitats, and are numerous in
mangrove systems aided by the three-dimensional character of
both terrestrial and aquatic habitat. Export occurs through
transient fauna such as birds or fish that consume epifauna,
reptiles, and fish.
It is unclear to what quantities mangrove ecosystems
actually depend on carbon and nutrient imports from adjacent
ecosystems. Qualitative information as to the importance of
imported material resulting mainly from isotope studies points
to the significance of imported material for, for example,
benthic invertebrates (Bouillon et al., 2002b) or sediments
(Bouillon et al., 2003). Other organisms that take part in
importing their food sources are the root fouling organisms
 Author's personal copy
such as sponges, tunicates, and bivalves, that grow on sub­
merged roots and filter water from the creek, estuary, or
lagoon (Nagelkerken et al., 2008).
6.12.3 Ecosystem Functioning (Whole Food-Web
Studies)
Although isotope studies have proved to be invaluable in trac­
ing feeding links, they have rarely been used to describe entire
food webs of mangrove systems. A similar situation is present in
terms of a holistic description of the food web with quantified
trophic links. The quantification of the actual components can
show a clearer picture of trophic connectivity between source
and consumer, as well as aid in establishing a comprehensive
description of ecosystem budgets of energy or nutrient through­
put and the opportunity of calculating the sustainability of
exploitation of its various components in a quantified way.
Ecosystem models are very data intensive, and above it was
shown that for many components of mangrove ecosystems,
adequate quantitative data are not available. One of the major
gaps is in the information on secondary productivity of man­
grove fauna, especially when compared to the rather extensive
studies on mangrove trees (Lee, 2008; Alongi, 2009). Therefore,
ecosystem models have been criticized for the accuracy of their
results (Nagelkerken et al., 2008). However, first attempts at
analyzing quantified food webs of mangrove ecosystems as
trophic flow networks have resulted in interesting insights
into ecosystem functioning, which are described below.
Whole food-web studies on ecosystems have been com­
pleted on networks describing quantified feeding interactions
between species or species groups. Such networks are data
intensive for the reason that data requirements include all
trophic flows (consumption, production, respiration, and eges­
tion) and biomass of all species included in the models. Due to
the high data requirement, quantified ecosystem trophic flow
networks have been established on systems that had been
subjected to numerous studies on their components, such as
the Sundarbans (Ray, 2008), South Florida mangroves
(Ulanowicz et al., 1999a), and Twin Cays Belize (Scharler
et al., in preparation). Other trophic flow models are in exis­
tence for estuaries or lagoons with fringing mangroves that thus
include large water bodies (Wolff et al., 1998, 2000).
Furthermore, there are a several trophic flow models focusing
on estuaries and lagoons (Wolff et al., 1996; Manickchand
et al., 1998; Lin et al., 1999; Ray et al., 2000; Vega-Cendejas
and Arreguín-Sánchez, 2001; Cruz-Escalona et al., 2007).
Although the estuaries and lagoons feature fringing mangroves,
the mangrove trees and associated flora and fauna are not
included as nodes in these models.
The very first whole food-web study of mangroves reported
in the literature is that of Golley et al. (1962), who investigated
energy flow through a Puerto Rican mangrove forest. They
reported measurements on the biomass of the flora, crabs,
snails, insects and arthropods, and vertebrates such as birds
and fish. Measurements of metabolism resulted in carbon
fluxes of c. 13.3 g-C m2 d−1 from primary producers and soil,
whereas the fauna was responsible for only 0.082 g-C m2 d−1.
Golley et al. (1962) concluded that animals therefore play a
minor role in the ecosystem. Subsequent to Golley et al.’s
study, the pioneering work of Odum and Heald (1972)
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Whole Food-Web Studies: Mangroves 279
elucidated trophic interactions between components of a man­
grove estuary in South Florida as well as stimulated further
research on the energetic contribution of mangroves to adja­
cent marine/estuarine ecosystems. Alongi (2009) furthermore
cited the study of Lugo et al. (1976) and Pandey and Khanna
(1998), who dynamically simulated energy flow through a
mangrove system. The main drivers of system functioning
were identified as tidal action affecting detritus export, and
terrestrial runoff to influence nutrient regimes in the
mangroves.
In the late 1990s, further studies were conducted that took
the entire mangrove food web into account (Wolff et al., 1998;
Ulanowicz et al., 1999b). As mentioned before, numerous stud­
ies have been conducted on selected primary producers,
heterotrophs, or abiotic components, and linkages have been
investigated between individual groups. This information has,
however, mostly not been summarized in comprehensive eco­
system budgets or models, except those described in this section.
The whole food-web studies which are presented in the
literature aim to be inclusive of all trophic levels. In most
cases, bacteria and fungi are not included, due to the scarcity
of quantitative data. Food webs are often depicted as digraphs,
where species or species groups are represented as nodes, and
feeding relations between them as a directed trophic flow from
source to consumer, or to detritus. The information on the
number of flows, and amount of material flowing along links
is used to characterize the trophic flow network for several
properties that arise on the species, community and ecosystem
level. The trophic flow networks are built on the principle of
conservation of mass, on information on the material through­
put through each node, losses to respiration, and links between
nodes. Information is generally taken from the literature where
not measured, and several software packages are available for
the construction (e.g., Vézina and Platt, 1988; Fath et al., 2007;
Ulanowicz and Scharler, 2008; Ecopath with Ecosim (EwE))
and analysis for trophic flow models, for example, WAND
(Allesina and Bondavalli, 2004) or EwE.
Most trophic flow models of ecosystems, and also of man­
grove systems, are constructed using a flow currency of energy
or carbon. Few concentrate on flows of other nutrients, for
example, nitrogen or phosphorus, mainly because data are
scarcer. Exceptions are models that simultaneously describe
the carbon, nitrogen, and phosphorus flows. Such models
have been built by Ulanowicz and Baird (1999) for the meso­
haline region of Chesapeake Bay, by Baird et al. (2008) of the
Sylt-Rømø Bight, Germany, and also for a mangrove system in
Twin Cays, Belize (Scharler et al., in preparation).
The trophic flow models for mangrove systems have been
analyzed for various descriptors and indicators, which are
shortly described below while comparing the various mangrove
systems. Size of an ecosystem can be expressed in terms of
energy or material throughput, and ecosystems can be directly
compared if throughput is referenced to area (e.g., throughput
per m2). Ecosystems with higher throughput values are more
active in terms of processing the trophic flow currency of energy
or nutrients. As with all models, it is important to account for
the way the model was built when comparing results of different
modelling exercises. If, for example, the South Florida and Twin
Cays mangroves are compared (see Table 2), then it is immedi­
ately apparent that there is much more carbon processed in the
healthy mangrove stands on Twin Cays (fringe and transition
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Table 2 Ecosystem properties of various mangrove ecosystems

South Florida South Florida Twin Cays – Twin Cays –

Golfo de Nicoya, Caeté estuary, Sundarban – Sundarban – mangroves – wet mangroves – dry Twin Cays – fringe transition dwarf mangroves,
Parameter Costa Rica Brazil virgin, India reclaimed, India season, USA season, USA mangroves, Belize mangroves, Belize Belize

Units of biomass/ g m−2/g m−2yr−1 g m−2/ kcal m−2/ kcal m−2/ g-C m−2/ g-C m−2/ g-C m−2/ g-C m−2/ g-C m−2/
flows g-m−2yr−1 kcal m−2 yr−1 kcal m−2 yr−1 g-C m−2 yr−1 g-C m−2 yr−1 g-C m−2 yr−1 g-C m−2 yr−1 g-C m−2 yr−1
Mean transfer 14.9 9.8 26.5 21.7 14.4 6.1 7.4 9.5
efficiency (%)
Transfer efficiency 8.8 5.9 62.8 58.6 39.8 21.5 24.3 21.5
TL I–II (%)
Transfer efficiency 8.8 26.6 41.6 5.5 2.0 0.02 0.01
TL I–II (%) –
grazing
TST 3 049 10 559 539 040 136 570 3 342 3 349 20 699 30 365 4 274
FCI (%) 5.5 17.9 21.3 8.3 9.6 17.2 9.7 9.3 6.5
A/C (%) 26.1 27.4 37 29 31.9 33.1 42.2 50.3 44.8
R/C (%) 56.0 19.6 33.5 28.9 29.0 27.7 31.6 25.5
I/C (%) 0 13.8 12.8 11.7 11.7 15.5 8.4 16.9
E/C (%) 2.7 12.2 5.4 4.4 7.2 7.1 3.2 4.8
D/C (%) 15.1 17.3 19.2 23.1 19.0 7.4 6.5 8.0
Connectance 0.30 0.53 2.1 2.1 1.9 1.9 1.8
Areal coverage (% of 1 45 Majority of study Only adjacent to Majority of study Majority of study 100 100 70
total system) area creeks area area
Total system 76 99 79 79 33 22 6
biomass made up
by mangroves (%)
Total system PP 1 60 50 50 82 98 53
made up by
mangroves (%)
Reference Wolff et al. Wolff et al. Ray (2008) Ulanowicz et al. (1999a) Scharler et al. (in preparation)
(1998) (2000)

Golfo de Nicoya and the Caeté estuary include large water bodies, whereas the remainder are mangrove islands or areas. TL, trophic level; TST, total system throughput; FCI, Finn cycling index; A, ascendency; C, development capacity; R, redundancy; I, imports,
E, exports; D , dissipation; PP, primary productivity.

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 Author's personal copy
zones) as compared to the South Florida mangroves. This is
mostly a result of the depth of sediment (and its associated
microbes and other fauna) that was chosen as 10 cm for South
Florida, but 30 cm for Twin Cays. In such cases, it is more
reasonable to concentrate on relative descriptors, for example,
ratios, which are not affected by these differences. The virgin and
reclaimed Sundarban mangroves, on the other hand, when re­
calculating kcal into carbon (10 kcal = 1 g-C; McLusky, 1989),
have a similar total system throughput compared to fringe and
transition mangroves of Twin Cays (Table 2). It is unknown at
what depth the soil food web was included or excluded in the
Sundarban study (Ray, 2008).
The relative importance of primary producers as food sour­
ces in mangrove systems has been discussed above. The
mangrove tree biomass is generally the highest of all other
living components. Mangrove trees provide habitat, food, litter,
and detritus, whereas other primary producers may be more
important in supplementing nutrients rather than energy. By
using input–output analysis and tracing units of flows through
the ecosystem, one can calculate the dependency of a node in
the food web on another, via direct and all indirect pathways.
In expanding the current knowledge on the use and importance
of various primary producers in mangrove systems, one can, for
example, calculate the trophic dependence of all nodes in the
ecosystem on the individual primary producers, and so gauge
the importance of the particular PP to the entire ecosystem.
As an example, Table 3 shows the dependency of the entire
food web on the various primary producer nodes for their
carbon requirements. The method to calculate dependencies
is described in Ulanowicz (2004). Dependencies are calculated
from a n � n adjacency transfer matrix that depicts all direct
quantitative transfers between nodes (e.g., from prey to preda­
tor, from consumers to detritus, etc.). This matrix is used to
calculate the amount of trophic transfer of indirect interactions,
that is, those over path lengths of 2, 3, 4, etc. If one is interested
to know, to what extent one or more nodes on the food web
depend on a particular other node (e.g., a primary producer),
that the intake of the node can be backtracked via all pathways
of all lengths. The result is a dependency value that gives an
indication of the importance of a particular compartment to
the sustenance of another.
In the Sundarbans, the dependency of commercially impor­
tant nodes (including carnivores and detritivores) on the three
Table 3 Dependencies of commercially important compartments in the Sundarbans networks on the primary producers nodes. Sums of
dependencies (%) of all nodes on primary producers on Twin Cays in terms of carbon
Sundarban
virgin a
Benthic algae 9.9 (1.6)
Phytoplankton 4.1 (3.6)
Macrophytes 82.0 (3.8)
Mangrove trees (Rhizophora mangle, Avicennia marina,
Laguncularia racemosa)
Lichen
Microbial mats
Macroalgae
a
Calculated from data given in Ray (2008). Data are mean% (� SD) of dependencies of the four commercially important nodes (invertebrates, fish) in terms of energy (kcal).
b
Scharler et al. (in preparation).
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Whole Food-Web Studies: Mangroves 281
different primary producers nodes (benthic algae, phytoplank­
ton, and macrophytes including mangroves) was calculated
(Ray, 2008). The reliance on macrophytes was 9 times higher
compared to that on benthic algae, and 20 times higher to that
on phytoplankton in the virgin forest. In the reclaimed forest,
the same nodes were half as dependent on macrophytes com­
pared to the virgin forest, and not even twice as much on
benthic algae. The importance of the phytoplankton was also
higher in the reclaimed compared to the pristine forest
(Table 3). These data are a result of the different availability
of primary food resources relative to each other, and can be an
important indicator of changes in the food-web structure and
the impacts of unsustainable use of mangrove ecosystem
resources.
The Twin Cays networks (Scharler et al., in preparation)
have been analyzed in the same way, and the dependencies of
the entire food web on the various primary producers nodes
were calculated (Table 3). It is apparent that mangrove trees are
more important to sustain the mangrove ecosystem in the
healthy stands of the fringe and transition zone as compared
to in the nutrient, and tree growth-limited, dwarf zone. The
reliance on microbial mats is small where there are not enough
light gaps for adequate growth (transition zone), and smaller
availability of macroalgae in the drier transition zone is equally
a reflection of availability. An interesting result is the fairly high
dependency on lichen overall, and the much higher impor­
tance of microbial mats in the dwarf zone which has the most
light gaps to sustain a higher biomass and productivity of
microbial mats.
Other indicators of ecosystem function are the number of
trophic levels and the associated transfer efficiencies, which are
calculated from the proportional feeding activities of each spe­
cies group or node in the food web (e.g., see Ulanowicz, 2004).
The proportional amount of feeding activity of each node in
the system on a specific trophic level is added to give the gross
amount of activity on a specific trophic level. The activity on
each trophic level can be compared over temporal and spatial
extents, or evaluated after an impact to the system. On the
contrary, the feeding activity of each node that is apportioned
among the trophic levels can be added up in order to arrive at
an integrated, or effective, trophic level for each node. Except
for species at trophic level I (primary producers, detritus), and
pure grazers and detritivores (trophic level II), the effective
Sundarban Twin Cays Twin Cays Twin Cays
reclaimed a fringeb transition b dwarf b
25.5 (9.5)
17.4 (14.3)
43.0 (10.0)
41.9 51.0 17.9
6.0 8.0 3.2
0.1 0.03 1.1
5.5 0.4 9.0
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282 Whole Food-Web Studies: Mangroves
trophic level of a node is mostly found between two trophic
levels and not specifically on an integer trophic level. Temporal
changes in food availability or variations of effective trophic
levels of the same species in different geographic locations can
so be calculated. The number of trophic levels is in general
limited due to constraints on energy availability (e.g., Pimm
and Lawton, 1977), and the amount transferred between tro­
phic levels higher than 5 is in general minimal (Ulanowicz,
2004). The efficiency of material passed on from one trophic
level to the next is calculated as the percentage of the flow into a
trophic level that is passed on to the next trophic level. The
mangrove networks listed in Table 2 feature a transfer effi­
ciency (TE) of between 6% and 26%. The TE in the Twin Cays
mangroves is low probably because of the inclusion of peat to a
depth of 30 cm. The peat on Twin Cays accumulates and a large
part of the detritus are thus not passed on to higher trophic
levels. In the Sundarbans, the ecosystem of the virgin forest
stand has a slightly higher TE compared to the reclaimed stand
(26.5 vs. 21.7). The Sundarbans feature slightly higher TEs
(Table 2) compared to a range of TEs of entire food webs that
have been reported to lie between 8% and 14% (Christensen
and Pauly, 1993).
Of interest is to compare the TE between trophic levels I and
II, since it gives a clue about basic food availability (primary
producers and detritus) and on how efficiently PP and detritus
(both on trophic level I) are taken up into the system to fuel
higher trophic levels. Should both PP and detritus be rare, the
trophic efficiency from trophic level I to II will be high com­
pared to a situation of overabundance of first-level resources.
TEs are often high from the first to second trophic level com­
pared to TEs along subsequent trophic levels, but do not
necessarily decrease steadily from lower to higher trophic lev­
els. Transfer efficiencies from TL I to TL II ranged from 6% to
63% (Table 2). It was overall lowest in the estuary and lagoon
(Caéte estuary, Golfo de Nicoya), and highest in the
Sundarbans, where the virgin forest system had a slightly higher
TE (63% vs. 59%) than the reclaimed forest. The TE for grazing
is substantially lower in all systems except in the Golfo de
Nicoya where it is about the same as the combined grazing
and detritivory TE from TL I to TL II. In the South Florida
mangroves and Twin Cays, grazing TEs are very low due to
the high biomass and production of mangroves trees that is
not directly consumed (Table 2). TEs for more palatable
and less abundant primary producers are higher than those
for trees.
In case resources are rare, recycling of nutrients and energy
takes on an important role in order to sustain maintenance and
productivity of all trophic levels. The Finn cycling index (FCI)
describes the proportion of the total systems throughput the
material that is cycled within the ecosystem. In the mangrove
ecosystems analyzed quantitatively, the percent recycled ranges
from about 5% to 21%, which is relatively low. This indicates
that the majority of resources is not utilized within the man­
grove systems, and are either buried (including peat formation)
or exported from the system (Table 2). Although export did
occur from all systems, the ecosystems were more reliant on
imports than exports, except the Golfo de Nicoya for which no
imports are listed (E/C, I/C in Table 2, see description of
indices below). The reliance on imports to and exports from
the system can is calculated from the number of pathways
entering/leaving the system and the actual amount imported
Treatise on Estuarine and Coastal Science, 2011, Vol.6, 271-286, DOI: 10.1016/B978-0-12-374711-2.00625-2
and exported along each pathway. Import pathways can be
those that supplement mangrove detritus, allochthonous food
sources available once the high tide has receded, or mangrove
residents foraging partly outside the system boundary. Exports
include, for example, tidal export of detritus and nutrients,
larval releases, or transient species removing system resources.
Ecosystem indices have been used in order to describe the
patterns of energy and material flow along the links realized in
the ecosystem. These indices give information on the develop­
mental state of the ecosystem, on its resilience gained through
parallel trophic pathways, its reliance on imports and exports
to and from the system, as well as on the respiratory loss from
the system (e.g., Ulanowicz, 2004; Scharler, 2008). The indices
are calculated from information theory, using conditional
probabilities for trophic transfer events that are calculated
from flow diversity (a priori, from number of paths and distri­
bution of flows along the pathways) and actual output from a
node a time step earlier (conditional). The present develop­
ment of the ecosystem can be expressed as the development
capacity (C) which describes the potential of the ecosystem to
develop with its current total system throughput (TST) and
flow structure. It is calculated from the flow diversity
(Shannon’s index) and scaled to the respective ecosystem by
multiplying by the TST. Representing the constraints on the
flows in the system, or its order, is the average mutual informa­
tion (AMI). The AMI is higher when flows are few, and when
the bulk of energy or material flows along very few of the
realised links. It is scaled to the ecosystem in question by
multiplying by the TST. A ratio of A/C, which essentially cancels
out TST, and with it ecosystem size, is often used for compar­
ison between ecosystems (e.g., Christian et al., 2005). This ratio
gives an indication of the percentage of constrained flows,
which may be equated with the degree of specialization of
trophic flows. These ecosystems with a high trophic flow spe­
cialization feature a more efficient processing of energy, but at
the same time nodes are reliant on few food sources and thus a
reduced number of transfer pathways whose disturbance might
have serious consequences. In mangrove systems, A/C ratios
ranged from 26% to 50% (Table 2). Interestingly again, the
virgin Sundarbans have a higher A/C and thus feature more
specialised flows compared to the reclaimed forest.
The existence of parallel, or redundant, pathways in food
webs are promoting resilience in the ecosystem, because the
loss of one of many parallel pathways can be easily absorbed
than the loss of the only existing pathway between two nodes.
This kind of overhead of the system is thus necessary for its
existence (e.g., Ulanowicz, 2004). The more parallel pathways
exist, the higher becomes the amount of uncertainty of along
which pathway a unit of flow will be transferred. This can be
expressed as part of the overhead of the ecosystem and, as
ascendancy, can be noted as a percentage of C. R/C ratios
range from 20% to 32% in the Sundarbans, South Florida
and Twin Cays mangroves, whereas it was high (56%) in the
Golfo de Nicoya (Table 2). The virgin Sundarban forest had a
lower redundancy compared to its reclaimed counterpart, indi­
cating a higher specialization of flows and loss of parallel
pathways.
The number of pathways and the flow distribution along
the links are also used to calculate connectivity between species
of the ecosystem. Connectance values are low if number of
links are few and the flow distribution along the links skewed
 Author's personal copy
toward few links transporting the bulk of material or energy
(Ulanowicz and Wolff, 1991; Bersier et al., 2002). Empirical
systems have been shown to fall in a range below a connectance
value of 3 (Ulanowicz, 1997). The South Florida and Twin Cays
mangroves have a connectivity similar to each other of around
2 (1.8–2.1), whereas the estuarine and lagoonal system show a
much lower connectivity of 0.5 and 0.3, respectively.
It has been noted that real-world ecosystems exist with a
balance of organization and overhead that keeps them in a
well-identifiable range of existence, a so-called ‘window of
vitality’ (Ulanowicz, 2009; Ulanowicz et al., 2009), similar to
a balance in too much or too little connectivity. In terms of A/C,
the mangrove systems in Table 2 fall within ranges of other
ecosystems (e.g., estuaries, shelf; Christian et al., 2005). The
low A/C ratio of the lagoonal system seems to be a tradeoff with
a high R/C value, implying many parallel pathways and thus
less streamlined processing of material. The comparison of the
virgin (R/C = 19.6) and reclaimed (R/C = 33.5) Sundarban
mangrove systems illustrates nicely how a system can change
in its functioning after a majority of their resource (in this case
wood) has been unsustainably harvested.
In addition to characterizing the food webs of the mangrove
systems, some authors have explored the use of ecosystem
models to elucidate resource use in mangrove systems (Wolff
et al., 1998, 2000; Wolff, 2006). In the Nicoya gulf, the shrimp
fishery exerts high pressure on the ecosystem in that it affects
the processing of detritus from trophic level I through to pred­
ators, for which shrimp act as intermediate processors (Wolff
et al., 1998). In the Caéte estuary, crabs are the main resource
harvested, and the impact of the fishery, as well as the crab’s
trophic role within the system is elucidated by analyzing tro­
phic flow models.
Whole food-web studies, whether in the form of ENA or
isotope studies, elucidate quantitative and/or qualitative feed­
ing links. The quantification of links allows for an analysis into
the structure and functioning of the ecosystem, and gives infor­
mation on how individual species are embedded in a trophic
network. Information on how ecosystems process energy tells
about its efficiency, its resilience, its reliance on imports, and
how well connected the system is. The obvious path toward the
future is to incorporate temporal resolution in order to mean­
ingfully project future scenarios of ecosystem behavior, and
impacts of harvesting of mangrove ecosystem resources.
Insights gained from whole ecosystem models may be useful
in exploring possibilities of ecosystem restoration by elucidat­
ing the intricate dependencies of nodes on one another in the
food web.
6.12.4 Carbon, Nitrogen, and Phosphorus Turnover
of Mangrove Systems
Mangroves grow in both nutrient-poor and nutrient-rich hab­
itats. In nutrient-poor habitats, the limiting nutrients are
conserved, whereas they are exported under conditions of
nutrient oversupply (Alongi, 2009). Mangrove ecosystems can
be both net importers or net exporters for dissolved nitrogen
and phosphorus components. Overall, there have not been
many studies exploring the nutrient exchanges and nitrogen
and phosphorus cycling within mangrove ecosystems. Wafar
et al. (1997) modeled litter fall dynamics, and the resulting
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Whole Food-Web Studies: Mangroves 283
carbon, nitrogen, and phosphorus contributions to adjacent
estuarine water. One of the main findings was that mangrove
tree production mainly contributed carbon to the adjacent
estuary to facilitate the microbial loop, but did not contribute
to the remainder of the food chain.
The decomposition of leaf litter has been studied in some
detail in terms of carbon, nitrogen, and phosphorus dynamics
(Davis et al., 2002). Nitrogen and phosphorus resorption by
leaves during senescence (Feller et al., 1999), as well as the
limitations of the two nutrients to mangrove tree growth have,
for example, been studied in Twin Cays, Belize (Feller et al.,
2003), the Indian River lagoon, FL, USA (Feller et al., 2007),
and Richards Bay, South Africa (Naidoo, 2009). In terms of
whole ecosystem budgets of carbon, nitrogen, and phosphorus,
ecosystem models were built for Twin Cays, Belize, in order to
investigate the different patterns of C, N, and P transfers, as well
as analyze trophic networks with different flow currencies
(Scharler et al., in preparation). One of the interesting findings
of this study was how the constraints on nutrient limitations
are expressed in a balanced trophic flow network in a nutrient-
limiting environment, and how dependencies of nodes on the
various primary producers shift in magnitude for carbon, nitro­
gen, and phosphorus across a tree height/nutrient limitation
gradient. The nutrient limitation of nodes changed along the
nutrient limitation gradient that exists on Twin Cays from the
fringe of the island to its interior. Dependency coefficients of
the food web on the various primary producers showed that the
mangrove trees were overly important in terms of supplying
carbon to the ecosystem. Intertidal macroalgae played an
important role in terms of nitrogen supplies to higher trophic
levels, and microbial mats increased in importance as nitrogen
and phosphorus sources according to their biomass distribu­
tion. Lichen, although slow growing and not a direct food
source to many, also play an important role in supplementing
carbon, nitrogen, and phosphorus to the ecosystem, albeit only
minor compared to mangrove trees and macroalgae (Scharler
et al., in preparation).
6.12.5 Concluding Remarks
The biogeographical distribution of mangroves has been into
two major regions globally, namely the Indo-West Pacific
region and the Atlantic- East Pacific region (Duke et al.,
1998). Although the mangrove gastropod and brachyuran
crab species richness go hand in hand with that of mangrove
tree species (Lee, 1998; Ellison, 2008), there is no information
whether the ecosystems function differently in species-rich or
species-poor regions. The global distribution of mangrove spe­
cies may provide us with a natural laboratory to investigate
high- versus low-diversity mangrove ecosystems, and their
functioning.
Although many attempts have been made to put monetary
value on ecosystems, including those of mangroves (references
in Gilman et al. (2008)), their ultimate value for humans lies in
the fact that ecosystems sustain human life as much as that
of the flora and fauna within the ecosystem and adjacent
systems. The importance of preserving intact ecosystems and
rehabilitating degraded ones can therefore be directly linked to
the long-term sustenance of human existence. The difficulty in
providing accurate long-term predictions of the consequences
 Author's personal copy
284 Whole Food-Web Studies: Mangroves
of habitat loss or degradation often lies in the lack of avail­
ability of long-term data. Similarly, despite a wealth of
knowledge accumulated thus far on mangrove ecosystems, a
few data gaps have been identified that could serve the accuracy
of long-term predictions, including (Gilman et al., 2008), but
not limited to, long-term changes on soil elevation caused by
changes in groundwater input, effects of increased frequency of
extreme high water events, effect of changes in rainfall patterns
on mangroves, and that of elevated CO2 levels. Resource use for
a worldwide growing population is a topic of high importance,
but their consequences on the entire system with adequate
replication across the globe still has to be forthcoming (see
examples in Hogarth (2007), Dahdouh-Guebas and Koedam
(2008), Ellison (2008), and Alongi (2009)). Although the
importance of mangroves as nursery area and feeding grounds
for fish and certain invertebrates is the main theme of many
scientific studies, it is as yet unclear what exactly the losses
would be if these functions are not anymore fulfilled following
habitat loss or degradation. This can include a quantitative
assessment of organisms utilizing mangroves, of the food sour­
ces provided, and of the loss of biomass to nearshore
environments and economic activities. In order to assess a
national and global impact, adequate replicate studies are
required. A start to this has been made by characterizing the
quantitative relationship between mangrove areas and fishery
catches summarized by Baran (1999, as cited in Manson et al.
(2005)). Whole food-web studies, including knock-on effects
on humans harvesting for subsistence or economic gain, have
to be integrated for a clearer picture of the short-term and long-
term value of mangrove ecosystems.
Although mangroves have a global distribution within their
preferred temperature range, not all regions are studied
adequately. As examples, the mangroves of West Africa, or
many Pacific or Caribbean islands do not appear in the peer-
reviewed scientific literature to any great extent, but are
undoubtedly important for the livelihood of a diverse fauna,
flora, adjacent ecosystems, and people in the form of subsis­
tence use or commercially (e.g., fisheries and shrimp farms).
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Relevant Websites
http://www.ecopath.org – Ecopath with Ecosim.