Dual isotope study of food sources of a fish assemblage in the red river mangrove ecosystem, vietnam

Hydrobiologia
DOI 10.1007/s10750-013-1737-9

BIODIVERSITY IN ASIAN COASTAL WATERS

Dual isotope study of food sources of a fish assemblage
in the Red River mangrove ecosystem, Vietnam
Nguyen Tai Tue • Hideki Hamaoka • Tran Dang Quy •
Mai Trong Nhuan • Atsushi Sogabe • Nguyen Thanh Nam
Koji Omori

•

Received: 24 February 2013 / Accepted: 27 October 2013
Ĩ Springer Science+Business Media Dordrecht 2013

Abstract The food source utilization and trophic
relationship of the fish assemblage in the Red River
mangrove ecosystem, Vietnam were examined using
dual isotope analysis. The carbon and nitrogen stable
isotope signatures of 23 fish species ranged from
-24.0 to -15.7% and from 8.8 to 15.5%, respectively.
Cluster analysis based on the d13C and d15N signatures
clearly separated the mangrove fish into five feeding
groups, representing detritivores, omnivores, piscivores, zoobenthivores, and zooplanktivores, which
Guest editors: M. Tokeshi & H. T. Yap / Biodiversity in
Changing Coastal Waters of Tropical and Subtropical Asia
N. T. Tue
Graduate School of Science and Engineering, Ehime
University, 2-5 Bunkyo-cho, Matsuyama, Japan
N. T. Tue (&) Á H. Hamaoka Á K. Omori

Center for Marine Environmental Studies, Ehime
University, 2-5 Bunkyo-cho, Matsuyama 790-8577, Japan
e-mail:
T. D. Quy Á M. T. Nhuan
Faculty of Geology, VNU University of Science, 334
Nguyen Trai, Thanh Xuan, Hanoi, Vietnam
A. Sogabe
Research Center for Marine Biology, Asamushi, Tohoku
University, 9 Sakamoto, Asamushi, Aomori 039-3501,
Japan
N. T. Nam
Faculty of Biology, VNU University of Science, 334
Nguyen Trai, Thanh Xuan, Hanoi, Vietnam

concurred with the dietary information. The results
suggested that mangrove carbon contributed a small
proportion in the diets of the mangrove fish, with
dominant food sources coming from benthic invertebrates, including ocypodid and grapsid crabs, penaeid
shrimps, bivalves, gastropods, and polychaetes. The
d15N values showed that the food web structure may be
divided into different trophic levels (TLs). The lowest
TLs associated with Liza macrolepis, Mugil cephalus,
and Periophthalmus modestus; 18 fish species had TLs
between 3.0 and 3.8; and Pennahia argentata had the
highest TL (c. 4.0).
Keywords Mangrove ecosystem Á Stable
isotopes Á Fish Á Food sources Á Trophic level Á
Vietnam

Introduction

Mangrove ecosystems have often been considered as
hot spots of fish diversity (Nagelkerken et al., 2008).
The hypotheses of the high diversity of the fish in the
mangrove ecosystem include reduced predation,
increased living space, and dominated food supply
(Nagelkerken et al., 2008). The last of these hypotheses stated that the mangrove ecosystem produces
greater food densities such as mangrove detritus,
benthic microalgae (BMA), sediment organic matter,
infauna, and invertebrates that form the basal food
sources of the fish in the mangrove ecosystem.

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Hydrobiologia

The linkage between the mangroves and the fish has
been the focus of numerous studies (e.g., Odum &
Heald, 1972; Blaber, 2007; Layman, 2007; Nagelkerken et al., 2008). Based on the stomach content
analysis, Odum & Heald (1972) demonstrated that the
mangrove detritus was a predominant food source of
the fish in the estuarine habitats. Nevertheless, isotopic
studies have failed to confirm the contribution of the
mangrove detritus in the diets of the fish in the
estuarine food web (Rodelli et al., 1984), apparently
because the refractory mangrove detritus is not easily
digested by the gut system of the fish (Fry & Ewel,
2003). Subsequently, numerous studies have focused
on determining the functional relationship between the
mangroves and the fish through examining the food

source utilization (Sheaves & Molony, 2000; Nanjo
et al., 2008), and the trophic relationship (Abrantes &
Sheaves, 2009; Giarrizzo et al., 2011). The results
would be useful for ecosystem-based fishery management and mangrove conservation practices (Nagelkerken et al., 2008).
The stable isotope ratios of carbon (d13C) and of
nitrogen (d15N) are useful in determining the timeaveraged relative importance of the ingested food
sources and the relative trophic level (TL) of a
consumer (Michener & Lajtha, 2007). The mean
(±1SD) trophic enrichment factor (TEF) between an
animal and its diet for d13C and d15N is 0.4 ± 1.3 and
3.4 ± 1%, respectively (Post, 2002). Therefore, the
d13C values can be used to trace the carbon utilization
by an organism when the stable isotope signatures of
the food sources are different (Bouillon et al., 2008).
In addition, the d15N values can be used to estimate the
relative TL of the organism (Zanden & Rasmussen,
1999; Post, 2002).
The d13C and d15N values have been frequently used
to examine the food sources (Sheaves & Molony,
2000) and the TL of the fish (Abrantes & Sheaves,
2009) in the mangrove ecosystem, and the ecological
connectivity between mangrove forests and other
coastal ecosystems (Layman, 2007). The isotopic
studies have shown that the contribution of the
mangrove carbon in the diets of the fish varies by
landscape characteristics (Thimdee et al., 2004; Lugendo et al., 2007) and tidal water levels (Sheaves &
Molony, 2000) of the mangrove ecosystem. However,
the application of the stable isotope methods in
understanding ecological functions of the mangrove
ecosystem in Vietnam has been few, and there remains

123

a significant gap in knowledge concerning the importance of horizontal and vertical trophic dynamics of the
fish assemblage within and between adjacent systems.
These problems certainly constrain our understanding
of the importance of the mangroves to fisheries, the
valuation of ecological services of mangroves, and the
planning and implementation effective conservation.
In the present study, we analyzed the stable isotope
signatures of carbon (d13C) and nitrogen (d15N) of 183
individuals from 23 fish species, and used the isotopic
data of primary production (mangroves, BMA, and
marine phytoplankton), mangrove creek particulate
organic matter (POM), sediments, and major groups of
the benthic invertebrates for testing the hypothesis of
whether the mangrove carbon was a major food source
of the fish assemblage in the Red River mangrove
ecosystem of Vietnam. To test our hypothesis, two
objectives were investigated: (1) to determine the
utilization of food sources by the fish assemblage and
(2) to determine the relative trophic relationship of the
fish assemblage in the Red River mangrove ecosystem
of Vietnam.

Materials and methods
Study area
The present study was conducted in the Red River
Delta Biosphere Reserve (RRBR) in northern Vietnam. The RRBR has two primary mangrove forests,
the Xuan Thuy National Park and the Tien Hai Natural

Reserve (Fig. 1) (). The characteristics of the mangrove forests are earlier described in Tue et al. (2011, 2012a, c). Briefly, the
mangrove forests are predominated by Sonneratia
caseolaris (L.) Engl., Bruguiera gymnorrhiza (L.)
Lamk., Kandelia candel (L.) Druce, and Aegiceras
corniculatum (L.) Blanco, and consist of several major
creek systems (Fig. 1), which remain inundated
throughout the tidal regimes. Moreover, mangroves
are an important source of the POM (Tue et al.,
2012b), and important sinks to organic carbon and fine
sediment particles (Tue et al., 2012d). As a result, the
mangrove forests are thought to provide productive
food sources for the benthic invertebrates (Tue et al.,
2012c) and the fish in the estuarine habitats (Cuong &
Khoa, 2004). The mangrove forests also play important roles in the filtering and containment of various


Hydrobiologia

pollutants (i.e., trace elements; Tue et al., 2012a), as
well as a physical buffer against erosion and surge
from major storm events. Moreover, the mangrove
forests are of great importance as major feeding,
breeding, and stopover grounds for migratory birds,
including several highly threatened species Platalea
minor (Temminck & Schlegel, 1849), Larus ichthyaetus (Pallas, 1773), Tringa orchropus (Linnaeus,
1758), and Egretta eulophotes (Swinhoe, 1860)
(Nhuan et al., 2009).
Field sampling
Fish samples were collected by a gill net during spring
and ebb tides in two major tidal creeks of the Xuan

Thuy National Park and the Tien Hai Nature Reserve
(Fig. 1) in January–February 2008. The sampling was
designed to collect most predominant fish species and
those of high economic values (Cuong & Khoa, 2004;

Than, 2004). Fish samples were placed in labeled
polyethylene bags, immediately stored in ice, and
transported to the laboratory where they were frozen at
-20°C until processing and analysis.
Sample preparation and analysis
In the laboratory, the fish samples were first rinsed
with distilled water, wiped with paper towel, then
identified to species level, measured for total body
length, and categorized into feeding groups based on
the literature (Balan, 1967; Koslow, 1981; Elliott
et al., 2007; Platell et al., 2007; Baeck et al., 2008;
Nanjo et al., 2008; Salameh et al., 2010; Froese &
Pauly, 2011). The list of the mangrove fish observed in
the RRBR and their feeding ecology is shown in
Table 1. These feeding groups consisted of detritivores (detritus and/or microphytobenthos feeders),
omnivores
(filamentous
algae,
macrophytes,

Fig. 1 Sampling sites
within the Red River
mangrove ecosystem,
Vietnam

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Hydrobiologia
Table 1 The list of fishes observed in the Red River mangrove ecosystem, Vietnam
Order
Taxa

Major food items

Feeding
ecology

References

Anguilliformes
Moringua sp.

NA

Aulopiformes
Harpadon nehereus (Hamilton, 1822)
Muraenesox cinereus (Forsska˚l, 1775)

Nekton and fishes

PV

Froese & Pauly (2011)

Fishes and crustaceans

PV

Froese & Pauly (2011)

Escualosa thoracata (Valenciennes, 1847)

Zooplankton (copepods, crab zoea,
larvae of bivalves, and fish eggs) and
phytoplankton

ZP

Froese & Pauly (2011)

Coilia mystus (Linnaeus, 1758)

Zooplankton and phytoplankton

ZP

Koslow (1981)

Acanthopagrus latus (Houttuyn, 1782)

Mangrove detritus, sesarmid crabs,
small gastropods, worms,
crustaceans, and mollusks

ZB

Platell et al. (2007)

Bostrychus sinensis (Lacepe`de, 1801)

Crustaceans and small fishes

PV

Froese & Pauly (2011)

Clupeiformes

Perciformes

Butis butis (Hamilton, 1822)

Small fishes and crustaceans

PV

Froese & Pauly (2011)

Gerres limbatus (Cuvier, 1830)
Glossogobius biocellatus
(Valenciennes, 1837)

Small benthic animals
Fishes, detritus, and gammaridean

amphipods

ZB
PV

Froese & Pauly (2011)
Nanjo et al. (2008)

Gobiomorphus sp.

NA

Leiognathus bindus (Valenciennes, 1835)

Copepods, phytoplankton, detritus,
and zoobenthos

ZP

Balan (1967)

Liza macrolepis (Smith, 1846)

Algae, diatoms, forams, benthic
polychaete, crustaceans, mollusks,
organic matter, and detritus;
copepods and floating algae

DV

Froese & Pauly (2011)

Lutjanus russellii (Bleeker, 1849)

Crabs, shrimps, fishes, crustaceans,
and insects

PV

Nanjo et al. (2008)

Mugil cephalus (Linnaeus, 1758)

Zooplankton as larvae; detritus,
microalgae, and benthic organisms

DV

Nanjo et al. (2008)

Oxyeleotris marmorata (Bleeker, 1852)

Small fishes, shrimps, aquatic insects,
mollusks, and crabs

PV

Froese & Pauly (2011)

Parapercis sp.

NA

ZB

Pennahia argentata (Houttuyn, 1782)

Small fishes and invertebrates

PV

Froese & Pauly (2011)

Periophthalmus modestus (Cantor, 1842)

Gammarids, crabs, and other
crustaceans

OV

Baeck et al. (2008)

Sillago sihama (Forsska˚l, 1775)

Polychaete worms, small prawns
(penaeus), shrimps, and amphipods

ZB

Froese & Pauly (2011)

Terapon theraps (Cuvier, 1829)

Animals

ZB

Froese & Pauly (2011)

Trypauchen vagina (Bloch & Schneider, 1801)

Small invertebrates and crustaceans

ZB

Salameh et al. (2010)

NA

NA

Scorpaeniformes
Onigocia sp.

General feeding ecology and reference are shown for each fish species
NA Not available, DV detritivores, OV omnivores, PV piscivores, ZB zoobenthivores, and ZP zooplanktivores

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Hydrobiologia

periphyton, epifauna and infauna feeders), zooplanktivores (zooplankton, hydroids, planktonic crustacean,
and fish eggs/larval feeders), zoobenthivores (benthic
invertebrate feeders), and piscivores (finfish and
nektonic invertebrate feeders) (Elliott et al., 2007).
The processing of fish for the stable isotope analysis
involved the extraction of white muscle tissue from the
anterior dorsal region. The white tissue is more
isotopically homogenous than other tissues (Michener
& Lajtha, 2007). The fish tissues were then placed in
Eppendorf tubes, dried in an electric oven at 60°C for
24 h, and ground to fine powder by an agate mortar
and pestle. The lipids were extracted from the fish
tissues prior to the stable isotope analysis following
methods described in Tue et al. (2012c). Briefly, the
pulverized fish tissues were placed in the Eppendorf
tubes, immersed in a 2:1 chloroform:methanol (by
volume) solution, and left at room temperature for
24 h to extract the lipids. The samples were then
rinsed with distilled water, and dried in an electric
oven at 60°C for 24 h.
For all samples, 1.0 ± 0.1 mg of the pulverized fish
tissues was packed in a tin capsule. The carbon and
nitrogen stable isotope signatures were measured
using an isotope ratio mass spectrometer (ANCAGSL; Sercon Inc, UK) and expressed in d notion as
parts per thousand (permil, %) as shown in Eq. (1):
ÂÀ
 Á
Ã

d13 C or d15 N ¼ Rsample Rstd À 1 Â 1000
ð1Þ
where R is isotope ratios 13C/12C or 15N/14N. Rsample is
the isotope ratio of the sample, and Rstd is the isotope
ratio of a standard referenced to Pee Dee Belemnite
limestone carbonate (PDB) for d13C, and to atmospheric nitrogen for d15N. During analysis processes,
13
15
L-histidine (d C = -11.4% and d N = -7.6%)
was used for quantifying the analyzed results. Analytical errors were 0.1% for d13C and 0.2% for d15N,
respectively.

Background data for potential food sources
of the mangrove fish
The ranges of the d13C and d15N values of the
mangrove leaves, the marine phytoplankton, the
BMA, the POM, the sediments, and the benthic
invertebrates are shown in Fig. 2. The respective
means of the d13C values increased in the order of the
mangrove leaves, mangrove sediments, the tidal flat,

Fig. 2 Dual isotope plot of mean d13C and d15N signatures (±1
SD) of the different food sources, and the fish in the Red River
mangrove ecosystem, Vietnam. Acronyms of fish taxa are
shown in Table 2, and DV, OV, PV, ZB, and ZP denotes the
detritivores, omnivores, piscivores, zoobenthivores, and zooplanktivores, respectively. Mang, Mang sed, Adj sed, POM,
Phyto, and BMA denotes mangrove leaves, mangrove sediments, adjacent habitat sediments, creek particulate organic
matter, marine phytoplankton, and benthic microalgae, respectively. The stable isotope data of mangrove leaves, POM, and
phytoplankton; benthic microalgae and invertebrates; and
mangrove, creek bank, tidal flat and bottom sediments are

presented in Tue et al. (2012a, b, c), respectively

the creek bank and creek bottom sediments, the POM,
the marine phytoplankton, and the BMA (Tue et al.,
2012b, c, d).
The benthic invertebrates (e.g., grapsid crabs) have
been shown to be important food sources for the
mangrove fish (Sheaves & Molony, 2000). The ranges
of the d13C and d15N values of the major benthic
invertebrate groups in the mangrove ecosystem of the
RRBR are shown in Fig. 2. Tue et al. (2012c) reported
that the gastropods, bivalves, grapsid crabs, and
polychaetes inhabiting the mangrove forests directly
relied on the mangrove detritus. The ocypodid crabs
inhabiting the land–water ecotone showed preference
for the BMA and other food sources (i.e., bacteria,
ciliate protozoa, and nematodes) over the mangrove
detritus. The diets of tidal flat bivalve Ensis magnus
(Ensis Schumacher, 1817) was a mixture of the marine
phytoplankton and the BMA. The penaeid prawns

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Hydrobiologia

were opportunistic omnivorous, feeding on the BMA,
the marine phytoplankton, the POM, and juvenile
invertebrates (i.e., crabs, gastropods, and bivalves),
with the latter being predominant (Tue et al., 2012c).

Estimation of the relative trophic level
and contribution of the food sources in diets
of the mangrove fish
The diversity of the food sources generates difficulties
in establishing an isotopic baseline for estimating the
relative TL of the mangrove fish (Layman, 2007).
Instead, the d15N values of the primary consumers
(invertebrates potentially eaten by fish) were used as
an index of nitrogen isotope compositions entering the
base of the food web. This method reduces the
temporal and spatial variations in the d15N values of
the primary producers (Post, 2002), and provides a
more temporally integrated measurement of the relative TL of the mangrove fish (Zanden & Rasmussen,
1999). In the present study, the relative TL of the
mangrove fish was estimated from the d15Nbase values
of the bivalve E. magnus based on the Eq. (2) (Post,
2002). The d15N values of the E. magnus were used as
the isotopic baseline, because this species is a true
suspension feeder, feeding on the marine phytoplankton and the BMA (Tue et al., 2012c).

TL ¼ ðd15 Nfish d15 Nbase ị 3:4 ỵ 2
2ị
where TL is the relative trophic level of the mangrove
fish; d15Nfish and d15Nbase are the nitrogen stable
isotope values of the mangrove fish and the bivalve
E. magnus, respectively; the mean trophic enrichment
factor between the mangrove fish and the bivalve
E. magnus for d15N is 3.4; and the TL of the bivalve
E. magnus is 2.

The contribution of the mangroves, the marine
phytoplankton, the BMA, the POM, the sediment
organic matters, grapsid crabs, ocypodid crabs,
E. magnus, gastropods, and polychaetes to the diets
of the mangrove fish was estimated using a Stable
Isotope Analysis in R (SIAR) package (Parnell et al.,
2010) on R software (R Core Team, 2012). The SIAR
package is based on a Bayesian framework that can be
used to find a solution for an isotope mixing model
(Parnell et al., 2010). The SIAR package requires the
d13C and d15N values of the mangrove fish, the mean
and SD of the d13C and d15N values for the food

123

sources, and the mean and SD of the trophic enrichment factors. In the present study, the mean trophic
enrichment factors (±1SD) for d13C and d15N were
0.4 ± 1.3 and 3.4 ± 1.0%, respectively (Post, 2002).
The stable isotope values of the sediments from
mangrove forests, and the adjacent habitats (tidal flats,
bank and bottom creeks) were pooled, representing the
sediment organic carbon source. The isotope mixing
model was run 5 9 106 iterations with an elimination
of the first 5 9 104. The contributions of the food
sources in the diets of the mangrove fish were reported
as means and lower and upper ranges (5th and 95th
percentiles).
Statistical analysis
The d13C and d15N values of the mangrove fish were
used to perform hierarchical cluster analysis, which

can be used to categorize the mangrove fish into
feeding groups based on their similarity (Mazumder
et al., 2011) and their dietary information (Table 1).
The distance metric was based on the Euclidean
distance completed linkage method. The statistical
analysis was performed using the SPSS statistical
software package 17 (SPSS 17.0).

Results
Stable isotope values of the mangrove fish
The d13C and d15N values of the mangrove fish ranged
from -24.0 to -15.7% and from 8.8 to 15.5%,
respectively (Table 2; Fig. 2). The lowest and highest
d13C values were expressed in Periophthalmus modestus and Lutjanus russellii, respectively (Fig. 2). Pennahia argentata showed the highest mean d15N values,
while the lowest mean d15N values were expressed in
Mugil cephalus and Liza macrolepis (Fig. 2).
Feeding groups and the contribution of different
food sources to diets of the mangrove fish
Five groups of the mangrove fish were categorized at a
similar index level of 15 (Fig. 3). Based on the dietary
information (Table 1), the mangrove fish were classified into five feeding groups, consisting of detritivores, omnivores, piscivores, zoobenthivores, and
zooplanktivores. Detritivorous fish were M. cephalus


Hydrobiologia
Table 2 d13C and d15N values of the fish collected from the Red River mangrove ecosystem, Vietnam
Order
Taxa

ACR

n

L (cm)

d13C (%)

d15N (%)

24.9

-20.8 ± 0.5

11.3 ± 0.3

3.11

24.8 ± 3.0

-17.1 ± 0.3

13.0 ± 0.3

3.6 ± 0.1

-19.6 ± 1.1

12.4 ± 0.7

3.45 ± 0.2

-18.7 ± 0.1

13.0 ± 0.4

3.63 ± 0.13

-20.1 ± 0.3

13.4 ± 0.1

3.73 ± 0.04

18.2 ± 3.1

-20.8 ± 1.1

12.3 ± 0.7

3.42 ± 0.2

(13.3 - 22.5)
8.7 ± 1.0

-20.0 ± 0.3

11.5 ± 0.2

3.17 ± 0.06

-20.4 ± 0.6

11.9 ± 0.2

3.30 ± 0.05

-19.1 ± 0.7

13.3 ± 0.7

3.69 ± 0.21

-20.3 ± 0.8

11.3 ± 0.4

3.11 ± 0.13

-19.5 ± 1.3

11.7 ± 0.7

3.23 ± 0.2

-19.5 ± 1.5

13.7 ± 0.1

3.81 ± 0.03

-18.6 ± 1.2

10.6 ± 0.9

2.91 ± 0.25

11 ± 0.7
(10.2 - 11.7)

-17.2 ± 1.1

12.0 ± 0.2

3.34 ± 0.05

-17.4 ± 0.8

10.5 ± 0.8

2.88 ± 0.24

-19.8 ± 1.3

11.9 ± 0.7

3.28 ± 0.21

-19.5 ± 0.8

12.4 ± 0.4

3.44 ± 0.11

-17.3 ± 0.5

14.2 ± 0.5

3.97 ± 0.15

-21.8 ± 1.7

10.7 ± 0.8

2.95 ± 0.22

-17.9 ± 0.2

13.4 ± 0.2

3.74 ± 0.05

Trophic level

Anguilliformes
Moringua sp.

Mor

2

Hn

6

Aulopiformes
Harpadon nehereus

(20.7 - 28.6)
Muraenesox cinereus

Mc

3

30.9 ± 7.6
(23.5 - 41.4)

Clupeiformes
Escualosa thoracata

Et

3

5.3 ± 0.5
(4.7 - 5.7)

Coilia mystus

Cm

5

12.9 ± 1.6
(11.9 - 15.8)

Perciformes
Acanthopagrus latus

Al

12

Bostrychus sinensis

Bs

6

Butis butis

Bb

4

(7.7 - 10)
7.1 ± 0.6
(6.7 - 8.1)
Gerres limbatus

Gl

10

10.8 ± 1.6
(8.9 - 13.9)

Glossogobius biocellatus

Gb

19

11.6 ± 4.6

Gobiomorphus sp.

Gob

4

23.8 ± 2.9

(5.0 - 26.5)
(20.7 - 26.6)
Leiognathus bindus

Lb

3

8.2 ± 0.6
(7.4 - 8.6)

Liza macrolepis

Lm

5

18.1 ± 5.5
(13.8 - 27.3)

Lutjanus russellii

Lr

3

Mugil cephalus

Mcl

18

15.8 ± 3.1

Oxyeleotris marmorata

Om

28

8.2 ± 4.8

(11.1 - 21.3)
(3.5 - 18)
Parapercis sp.

Ps

11

12.2 ± 2.6
(7.0 - 16.4)

Pennahia argentata

Pa

8

24.5 ± 1.4

Periophthalmus modestus

Pm

10

3.6 ± 1.7

(23.4 - 26.8)
(1.8 - 6.6)
Sillago sihama

Ss

5

8.4 ± 0.7
(7.4 - 9.1)

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Table 2 continued
Order
Taxa

ACR

Terapon theraps

Tt

Trypauchen vagina

Tv

L (cm)

d13C (%)

d15N (%)

Trophic level

3

11.7 ± 1.0

-18.8 ± 0.4

13.2 ± 0.6

3.67 ± 0.17

7

14.2 ± 4.0

-20.4 ± 1.3

10.9 ± 1.5

3.00 ± 0.43

-19.0 ± 0.8

11.6 ± 0.4

3.21 ± 0.11

n

(10.6 - 12.4)
(8.2 - 18.7)
Scorpaeniformes
Onigocia sp.

On

8

11.5 ± 4.5
(8.1 - 19.4)

ACR acronym; n is number of the samples; mean, and mean ± 1SD values are given where n = 2, and C3, respectively; L total body
length (mean ± 1SD (min - max)); Trophic levels of the mangrove fishes are estimated by the d15N values

and L. macrolepis. The P. modestus could be distinguishable with other fish groups and fed on the
filamentous algae, small invertebrates, and infauna
(Table 1), representing the omnivorous fishes. The
piscivorous fishes were P. argentata, Sillago sihama,
Harpadon nehereus, and L. russellii, and may consume other fish and the invertebrates (Table 1). The
zoobenthivorous fishes consisted of Acanthopagrus
latus, Butis butis, Bostrychus sinensis, Gobiomorphus
sp., Glossogobius biocellatus, Moringua sp., Muraenesox cinereus, Oxyeleotris marmorata, Onigocia sp.,

Parapercis sp., and Trypauchen vagina whose prey
included invertebrates (polychaetes, crabs, and mollusks) and prawns (Table 1). The zooplanktivorous
fishes were Escualosa thoracata, Coilia mystus,
Leiognathus bindus, Gerres limbatus, and Terapon
theraps, feeding predominantly on copepods, crab
zoera, bivalve larvae, and fish eggs (Table 1).
The isotope mixing model results showed that the
mangrove carbon was a minor contributor to the diets
of the mangrove fish (Table 3). The major carbon food
sources of the mangrove fish were the benthic
invertebrates, consisting of the panaeid prawns, the
ocypodid and grapsid crabs, gastropods, the E. magnus, and polychaetes (Table 3).

3.97 ± 0.15), and followed by L. bindus (mean
3.81 ± 0.03).

The relative trophic level of the mangrove fish

Discussion

The mean relative TL (±SD) of the mangrove fish
ranged between 2.88 ± 0.24 and 3.97 ± 0.15 (Fig. 2;
Table 2). The relative TLs for M. cephalus, L. macrolepis, and P. modestus were below 3.0. The relative
TLs of 18 fish species ranged between 3.0 and 3.8. The
highest TL was observed from P. argentata (mean

The mangrove leaves, the marine phytoplankton, the
BMA, the POM, and the sediments had different d13C
signatures, but all had low d15N values. The d15N
values of the mangrove fish concurrently increased

with the TLs in the food web (Fig. 2). The d13C values
were, therefore, a good indicator of the origin of the

123

Fig. 3 Results of hierarchical cluster analysis of 23 fish species
based on d13C and d15N signatures. DV, OV, PV, ZB, and ZP
denotes the detritivores, omnivores, piscivores, zoobenthivores,
and zooplanktivores, respectively


3.2 (0–26.7)

4.7 (0–27)

Pennahia
argentata

Sillago sihama

7.5 (0–33.2)

6.2 (0–33.6)

7.9 (0–34.3)

6 (0–37.7)

7.9 (0–37.7)

2.9 (0–18.4)

3.5 (0–22.3)

4.8 (0–25.3)

8.4 (0–31.7)

8.5 (0–42.1)

7 (0–35.3)

5.6 (0–24.7)

6.3 (0–37)

5.6 (0–27.7)

3.3 (0–22.2)

8.6 (0–33.6)

8.7 (0–34.5)

3.1 (0–2.9)

8.6 (0–39.5)

7.9 (0–35.4)

6.6 (0–33.9)

7.8 (0–36.4)

6.1 (0–35)

Phytoplankton

6 (0–37.1)

4.5 (0–27.3)

7.2 (0–35.2)

4.7 (0–30)

6.1 (0–30.1)

2.1 (0–20.4)

2.6 (0–18.8)

3.1 (0–18.5)

7.4 (0–35.1)

7.6 (0–35)

5.6 (0–31.7)

3.9 (0–21.6)

4.8 (0–28.4)

3.9 (0–21.6)

2.8 (0–23.3)

7.6 (0–35.3)

7.9 (0–32.2)

2.9 (0–22.9)

7.5 (0–34.6)

5.4 (0–30)

3.1 (0–22.9)

6 (0–32.7)

5.7 (0–32.5)

POM

7.5 (0–36)

6.2 (0–33.1)

7.6 (0–34.3)

5.8 (0–10)

7.6 (0–36.6)

2.5 (0–20)

3 (0–18.5)

4.5 (0–25.8)

8.3 (0–36.2)

8.3 (0–36.2)

6.6 (0–34.7)

4.8 (0–22.8)

5.8 (0–35.8)

4.8 (0–29.9)

2.6 (0–21.9)

8.7 (0–36.3)

8.7 (0–36)

3 (0–31)

8.6 (0–32.8)

8.2 (0–43.6)

10.8 (0–36.7)

7.6 (0–32.6)

5 (0–25.3)

BMA

6 (0–35.6)

4.5 (0–32.7)

7.5 (0–35.5)

5 (0–32.3)

6 (0–28.3)

2.4 (0–16.3)

3 (0–18)

3 (0–20.4)

7.1 (0–30.4)

7.6 (0–31.2)

5.8 (0–33.1)

4.5 (0–23.5)

5.1 (0–29.3)

4.2 (0–26.6)

3.6 (0–25.6)

7.4 (0–37.4)

7.7 (0–33.1)

2.3 (0–17.9)

7.3 (0–41.4)

4.7 (0–26.1)

2.1 (0–21.6)

6 (0–30.5)

7.6 (0–37.4)

SOM

10.7 (0–41)

11 (0–50.6)

9.8 (0–39.7)

10.3 (0–46.6)

11.5 (0–48)

6.3 (0–37.2)

8.4 (0–32)

8.6 (0–43.7)

10.3 (0–44.1)

10 (0–37.2)

10.8 (0–48.5)

6.7 (0–27.9)

10 (0–43.2)

8.3 (0–38.8)

7.5 (0–38.7)

14.3 (0–48.5)

10 (0–36)

7.7 (0–45)

10 (0–42.9)

10.6 (0–42.7)

11.1 (0–44.4)

11.3 (0–46.1)

9.5 (0–37)

Grapsid
crabs

14.8 (0–64)

19.6 (0–77.7)

11.3 (0–58.2)

15.7 (0–64.8)

13.6 (0–52.6)

22.4 (0–55.6)

20.6 (0–59.5)

26 (0–61.6)

11.8 (0–53)

11.1 (0–41.6)

14.2 (0–53.8)

20.1 (0–50.5)

14.8 (0–57.5)

18.6 (0–52.9)

13.1 (0–46.6)

11.8 (0–55.2)

11 (0–52.6)

22.9 (0–61.4)

11.8 (0–47.4)

16.1 (0–49.3)

41.7 (0–75.5)

14.3 (0–53.5)

10.5 (0–37.4)

Ocypodid
crabs

10 (0–42.3)

9.6 (0–51)

9.8 (0–41.8)

9.6 (0–40.7)

10.7 (0–54.5)

6.4 (0–30.9)

8.2 (0–32.4)

7.6 (0–40.3)

10 (0–39.4)

9.8 (0–37.8)

10.2 (0–53.4)

6.7 (0–28.6)

9.8 (0–46.7)

8.5 (0–43.6)

8.2 (0–44.4)

9.8 (0–38.9)

9.7 (0–39.8)

7.1 (0–41.2)

9.9 (0–44.1)

10 (0–46.2)

7 (0–39.4)

10.7 (0–53.1)

10.2 (0–39.8)

Gastropods

9.2 (0–39.7)

8.3 (0–41.2)

9.5 (0–41.1)

8.8 (0–46.7)

9.7 (0–46.7)

7.7 (0–38.3)

8 (0–43.3)

8 (0–41.2)

9.5 (0–36.4)

9.6 (0–41.6)

9.5 (0–38)

10.9 (0–44.7)

9.8 (0–47.7)

10.6 (0–47.7)

8 (0–42.4)

9.3 (0–35.8)

9.3 (0–35.5)

6.2 (0–34.8)

9.3 (0–38.6)

9.8 (0–46.2)

4.5 (0–37.7)

9.5 (0–40.8)

10.3 (0–43)

E. magnus

14.9 (0–67.3)

19.6 (0–73.4)

12.6 (0–54.1)

20.8 (0–73)

13.9 (0–52.6)

37 (1–67)

32.4 (0–63.7)

27.1 (0–62.2)

12.1 (0–59.3)

11.5 (0–45.5)

16 (0–60.1)

25.3 (0–52.5)

19.1 (0–56.3)

24.3 (0–57.2)

29.5 (0–69)

11.5 (0–46.7)

11 (0–50.5)

38.5 (0–78.9)

11.7 (0–52.6)

17 (0–67.6)

9.4 (0–45)

13.8 (0–51.6)

13.9 (0–44)

Prawns

8.4 (0–45.7)

7.1 (0–55)

10.3 (0–41.2)

9.7 (0–55.6)

8.6 (0–38.4)

8.6 (0–27)

8.1 (0–28.6)

5 (0–33.9)

8.9 (0–38.3)

9.4 (0–42.1)

10 (0–48)

8.7 (0–24.2)

10.8 (0–46.6)

8.5 (0–35)

18.9 (0–47.5)

8.5 (0–48.2)

8.9 (0–38)

5.3 (0–26.8)

8.6 (0–35.3)

6.8 (0–35.2)

1.9 (0–22.6)

8.3 (0–33.7)

15.9 (0–40.7)

Polychaetes

BMA, POM, and SOM denotes the organic carbon sources of benthic microalgae, particulate organic matter, and sediment organic matter; DV, OV, PV, ZB, and ZP denotes the detritivores, omnivores,
piscivores, zoobenthivores, and zooplanktivores, respectively

6.4 (0–30.5)

Lutjanus russellii

3.7 (0–28.2)

2 (0–13)

Oxyeleotris
marmorata

PV

2 (0–17.8)

Onigocia sp.

Harpadon
nehereus

6.2 (0–30.2)

Muraenesox
cinereus

16 (0–11.3)

6.4 (0–31.5)

Moringua sp.

4.4 (0–24.5)

4.4 (0–28.5)

Gobiomorphus
sp.

Trypauchen
vagina

2.8 (0–15.3)

Glossogobius
biocellatus

Parapercis sp.

3.6 (0–24.3)

Butis butis

2.3 (0–20)

Acanthopagrus
latus

2.7 (0–18.8)

6.4 (0–32.5)

Terapon theraps

Bostrychus
sinensis

6.9 (0–34.2)

Leiognathus
bindus

ZB

1.5 (0–13.7)

Gerres limbatus

3.4 (0–21)

6.4 (0–32)

Escualosa
thoracata

ZP

4.5 (0–28)

Coilia mystus

DV

Liza macrolepis

5.3 (0–25)

1.7 (0–16.9)

OV

Periophthalmus
modestus

Mangroves

Mugil cephalus

Group

Dietary source
Species

Table 3 The proportional contribution of the food sources in the diets of the mangrove fish based on the Bayesian stable isotope mixing model

Hydrobiologia

123


Hydrobiologia

food sources (Bouillon et al., 2008), while d15N values
were indicative of the relative TLs (Michener &
Lajtha, 2007). The wide variations in the d13C and
d15N values of the mangrove fish (Fig. 2; Table 2)

indicated that they utilized heterogeneous diets.
Moreover, the fish tissues were much more enriched
in 13C composition relative to the mangrove leaves
(Fig. 2), suggesting that the fish had little reliance on
the mangrove carbon sources (Table 3). This pattern
was consistent with findings in the mangrove ecosystems in the Tanzanian coastal waters (Lugendo et al.,
2007) and Gazi Bay, Kenya (Nyunja et al., 2009).
Among fish taxa analyzed, the detritivorous fishes
had the lowest d15N values (Fig. 2) and high BMA
proportion in their diets (Table 3). The results indicated
that they fed on lower trophic order sources, such as the
BMA, the sediment organic matter, and the POM
(Tables 1, 3; Fig. 2). This finding was consistent with
the observation of Lin et al. (2007), who showed that the
preferred food sources of the L. macrolepis and other
detritivorous fishes were the BMA and the POM.
Moreover, the d13C values of the detritivorous fish in the
present study were much higher than those of the BMA,
the POM, and the sediments (Fig. 2), suggesting that
they also fed on other 13C-enriched food sources such as
the benthic invertebrates. The mixing model results
showed that the ocypodid crabs contributed up to 41.7%
in the diet of M. cephalus (Table 3). The benthic
invertebrates could be incidentally ingested while the
detritivorous fishes were feeding on the detritus, placing
them at higher TLs than the secondary consumers in the
mangrove food web (Nanjo et al., 2008).
The d13C values of the P. modestus were higher
than those of polychaetes, the POM, the sediments,
and overlapped with the d13C values of E. magnus and

gastropods (Fig. 2). The mixing model results showed
that the major food sources of the P. modestus were
polychaetes and other invertebrates (Table 3). This is
consistent with Baeck et al.’s (2008) observation that
the major food items of the Periophthalmus species
were gammarid amphipods, crabs, other crustaceans,
and benthic organisms.
The zooplanktivorous fishes C. mystus, E. thoracata, G. limbatus, L. bindus, and T. theraps were
closely positioned in the food web (Fig. 2) and clustered
in the same group (Fig. 3), indicating that they had
similar feeding behaviors. The mixing model results
showed that the major prey items of the zooplankton
fishes were the grapsid and ocypodid crabs, the penaeid

123

prawns, gastropods, and bivalves (Table 3). The diets of
the zooplanktivorous fishes in the present study were in
reasonable agreement with information on their feeding
ecology from the literature (Balan, 1967; Koslow,
1981). In which, the anchovy C. mystus and sardine
E. thoracata are suspension feeders, feeding on a
diversity of available zooplankton, fish eggs, and the
invertebrate larvae, rather than selecting specific species
(Koslow, 1981). In addition, L. bindus is reported to
feed on copepods, bivalve larvae, crustaceans, and
marine phytoplankton (Balan, 1967).
Despite the wide feeding preferences of the
zoobenthivorous fishes (Nanjo et al., 2008; Froese &
Pauly, 2011), their d13C and d15N values varied

slightly (Table 2; Fig. 2), indicating that they could
feed on similar food sources, consisting of the penaeid
prawns, the ocypodid and grapsid crabs, and the
bivalve (E. magnus) (Table 3). The food sources of
the zoobenthivorous fishes were consistent with the
dietary information from the literature (Platell et al.,
2007; Froese & Pauly, 2011). For example, the
A. latus collected from the mangrove ecosystem from
Shark Bay (Australia) fed predominantly on the
sesarmid crabs, small gastropods, and the mangrove
materials (Platell et al., 2007). The present study
showed that the d13C values of the A. latus were
higher than those of the bivalve E. magnus, and
overlapped with the d13C values of the gastropods and
grapsid crabs (Fig. 2). In addition, the bivalve
E. magnus, ocypodid crabs, polychaetes, and prawns
were predominant food items of the A. latus (Table 3).
The low contribution of the mangrove detritus in their
diets could be interpreted by either the selective
feeding mechanisms or assimilation efficiency of the
A. latus. The A. latus could predominantly ingest the
benthic invertebrates selectively and reject the mangrove detritus. In that case both the benthic invertebrates and the mangrove detritus were simultaneously
ingested by the fish, yet the mangrove detritus was too
refractory for assimilation (Fry & Ewel, 2003).
The d13C values of the piscivorous fishes were
overlapped, and higher than those of other fish groups
from 1.3 to 4.1% (Table 2; Fig. 2); hence, they may not
extensively feed upon other fishes. The mixing model
results showed that the grapsid and ocypodid crabs, and
the penaeid prawns were their major food sources

(Table 3). Furthermore, the benthic invertebrates in the
mangrove ecosystem of the RRBR are known to
consume the mangrove detritus, the BMA, marine


Hydrobiologia

phytoplankton, the POM, and the sediment organic
carbon (Tue et al., 2012c). The high contribution of the
benthic invertebrates in the diets of the piscivorous
fishes suggested that the carbon pathways from the basal
food sources to the piscivorous fishes at/or near the top
of the food chain may be shortened in the mangrove
ecosystem (Sheaves & Molony, 2000). The pattern
suggested that the piscivorous fishes may appear to be a
major mechanism of carbon transport from the mangrove ecosystem to adjacent coastal waters (Sheaves &
Molony, 2000), and the mangrove forests were important nursery and feeding grounds of the fish (Layman,
2007). However, further studies need to investigate the
extent to which the piscivorous fishes prey upon the
benthic invertebrates using a combination of stomach
content and stable isotope analyses, which would
provide a more detailed picture of energy transfer
within a mangrove ecosystem.
The food web structure of the mangrove ecosystem
of the RRBR presented four TLs that were similar to
the mangrove ecosystems of North Queensland
(Abrantes & Sheaves, 2009) and Gazi Bay (Nyunja
et al., 2009). The food web structure consisted of
primary producers (mangroves, phytoplankton, and
the BMA), the POM, and the sedimentary organic

matters, which were the basal food sources; the
primary consumers were the benthic invertebrates,
including of polychaetes, bivalves, gastropods, the
ocypodid and grapsid crabs, and the penaeid prawns;
the secondary consumers included M. cephalus,
L. macrolepis, and P. modestus; the tertiary consumers included zooplanktivorous, zoobenthivorous, and
piscivorous fishes; and the piscivorous fish P. argentata was positioned at the apex of the food web. In the
present study, almost all mangrove fishes had
TLs [ 3.0, and were one TL higher than that of the
primary consumers. Moreover, the invertebrate species utilized the food sources from the basal food
sources (Tue et al., 2012c). The food web structure
clearly showed different carbon pathways from the
basal food sources to the primary consumers, to the
secondary consumers, and then to the piscivorous
fishes at/or near the top of the mangrove food web.

Conclusions
The d13C and d15N signatures were applied to identify
the carbon utilization and trophic relationship of the

fish assemblage in the Red River mangrove ecosystem, Vietnam. The results showed that the fish
assemblage had less reliance on the mangrove carbon.
The major food sources of the mangrove fish were the
benthic invertebrates, including the penaeid prawns,
the ocypodid and grapsid crabs, bivalves, gastropods,
and polychaetes. Five feeding groups of the mangrove
fish were identified in the cluster analysis, consisting
of detritivores, omnivores, zooplanktivores, zoobenthivores, and piscivores. The food web structure
showed that the carbon energy was transferred from
the basal food sources to the piscivorous fishes at/or

near the top of the food chain by different trophic
pathways. These results highlight the need for conservation of mangroves and the preferred habitats of
the benthic invertebrates in the mangrove ecosystem.
The present study has provided baseline information on the food source utilization and the trophic
relationship of the mangrove fish, which will be a
useful database for future studies to assess the changes
in the food sources and the TLs of the fish assemblage
in relation to the mangrove and coastal ecosystem
management (Wainright et al., 1993).
Acknowledgments The authors are grateful to staff of VNU
University of Science, and the Xuan Thuy National Park and the
Tien Hai Nature Reserve, Vietnam for their help with sampling.
We express our sincere thanks to anonymous reviewers—Prof.
Tokeshi and Dr. Todd W. Miller for their critical reviews and
comments which significantly improved the manuscript. This
work was partially supported by the ‘‘Global COE Program’’
from the Ministry of Education, Culture, Sports, Science and
Technology, Japan and the Vietnam’s National Foundation for
Science and Technology Development (NAFOSTED) (No
105.09.82.09). The Grant-in-Aid for Scientific Research for
Postdoctoral Fellows by the Japan Society for the Promotion of
Science (No. 24-02386 for NTT) is also acknowledged.

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