Ecological Modelling 137 (2001) 119 133

www.elsevier.com/locate/ecolmodel

Energy fluxes in a mangrove ecosystem from a coastal

lagoon in Yucatan Peninsula, Mexico
M.E. Vega-Cendejas a,*, F. Arregun-Sanchez b
a

Centro de In6estigacion y de Estudios, Unidad Merida, A6anzados del IPN, A.P. 73 Cordemex, Merida, 97310 Yucatan, Mexico
b
Centro Interdisciplinario de Ciencias Marinas, A.P. 592, La Paz, Baja California Sur, Mexico 23000
Received 7 December 1999; received in revised form 9 August 2000; accepted 4 September 2000

Abstract
Energy fluxes in a mangrove ecosystem were evaluated with Ecopath model through a predator/prey matrix with
19 functional groups including primary producers and three levels of carnivores. Some input data (biomass of the fish
groups, zooplankton and benthic communities) were obtained from the field and by stomach content analysis of
dominant fish species (32) while others were taken from previous studies. Within fish, nine functional groups were
obtained through trophic similarity analysis, being microcrustaceans an important prey in five of them. Results
showed that a great proportion of the primary production is exported to adjacent ecosystem while within the system
only 4% is grazed and 7% goes to detritus, with a detritivory/herbivory ratio of 2.0. Within the mangrove, detritus
plays an important role with 64% of the flows being utilized and transferred to juvenile fish by microcrustaceans.
Mixed trophic impacts showed that detritus and low trophic levels had a positive influence on most groups, while a
negative one occurred with increasing biomass at high trophic compartments (other fish and piscivorous). Small EE
for fish groups indicated a low predation rate to these groups, while greater P/B and Q/B suggest that mangrove is
a high productive system with characteristic properties of a transition between mature and immature stage. 2001
Elsevier Science B.V. All rights reserved.
Keywords: Ecopath model; Mangrove ecosystem; Energy fluxes; Yucatan Peninsula

1. Introduction
Mangrove wetlands are one of the most productive aquatic ecosystems covering 240 105
km2 of subtropical and tropical coastline
* Corresponding author. Tel.: + 52-99-812960, ext. 286; fax:
+52-99-812324.
E-mail addresses: maruvega@kin.cieamer.conacty.mx (M.E.
Vega-Cendejas), farregui@vmredipn.ipn.mx (F. ArregunSanchez).

characterised by high number of primary producers, diversity of microhabitats, complex multispecies interactions and by intensive exchange of
organic matter and organisms within and outside
the ecosystem (Day et al., 1989; Twilley et al.,
1992). These halophytic species are of great energetic importance because they provide food (via
detritus) to both estuarine and ocean consumers,
serve as habitat for early stages, juveniles and
adult of estuarine and marine organisms and play

0304-3800/01/$ - see front matter 2001 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 3 8 0 0 ( 0 0 ) 0 0 4 2 1 - X

120

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

an important role in the regulation of estuarine

chemical cycles (Mitch and Gosselink, 1993).
To understand mangrove ecosystem dynamics,
a study of multispecies interactions is needed including trophic fluxes, assimilation efficiencies and
energy transfer and dissipation (Beddington,
1984; Steele, 1984; Baird and Ulanowicz, 1993).
They are reflected on diversity, abundance, distribution and persistency of the biological components which finally are regulated by primary
productivity (Oksanen et al., 1981; Oksanen,
1983), environmental variability (Pimm and
Kitching, 1987) and a combination of both
(Persson et al., 1992). Models, defined as solid
descriptions that emphasise some aspects of the
systems in order to understand how they work
(Christensen and Pauly, 1992a, 1996), are ecosystem representations that permit to understand
their complexity in energy terms, to identify their
level of production, to compare energy transfer
between ecosystems, and to evaluate the functional reaction to natural and/or anthropogenic
impacts.
Knowledge of trophic interactions in aquatic
ecosystem has considerably improved through the
design of mass-balance processes (Christensen and
Pauly, 1993). In energy terms, this kind of analysis is important because it allows the computation
of the fish biomass that can be sustained by
primary production (Halfon et al., 1996). However, in spite of mangrove importance for providing shelter and feeding grounds to marine and
freshwater fish species, there exist few ecological
models compared with other wetlands ecosystems
(Mitch and Gosselink, 1993). Lugo et al. (1976)
based on energy and material flows approach
showed that reduction in upland run-off caused a
decrease in its productivity, and that the time
required to reach steady-state levels of mangrove
biomass was similar to the average frequency of
tropical hurricanes during 20 years. Adams (1976)
characterised a fish community by its functional
role considering consumption, production and
metabolism data for the dominant species. Chavez
et al. (1993) carried out some investigations in
Celestun coastal lagon, Yucatan, using Ecopath II
and Vega et al. (1993) for the beach seine fishery
on Campeche Bank. However, no models describ-

ing energy fluxes in a mangrove ecosystem are

presently been represented. In this sense, the objective of this study is the construction of a mangrove ecosystem trophic model in order to
quantify its structure and function, to determine
its flows of energy and the role of the fish community in transferring energy from the mangrove
areas to adjacent ecosystems.

2. Materials and methods

2.1. Study area

Celestun Lagoon is a tropical ecosystem located
in the Gulf of Mexico on the northeast of the
Yucatan Peninsula (2045% 2058% N and 9015%
9025% W), (Fig. 1). Parallel to the coastline, this
narrow (0.5 2.4 km wide) and shallow (0.5 3.0
m) lagoon is connected with the sea by a permanent 410 m wide mouth at its southern part
(Herrera-Silveira, 1996). Weather is warm (mean
annual temperature \26C), semi-arid (794.7
mm annual precipitation) and 80% of relative
humidity (Garca and Mosino, 1992). There are
no rivers, so the freshwater inputs come from
underground seeps located in the northern part of
the lagoon and from heavy rains during the rainy
season (July October). The water temperature
shows small variations with the lowest values in
February during north winds (22.4C) and highest
in June (31.4C). Salinity shows spatial variations
with 35% in the mouth to 06% in the head.
Along the coast, there is a 150 m long fringe of
Rizophora mangle; while inside the lagoon, the
dominant species are Laguncularia racemosa in
the head; R. mangle and A6icennia germinans in
the mixing zone and A. germinans in the mouth
(Sanchez-Arguelles, 1994).

2.2. Ecopath model

Trophic interactions and energy fluxes were
evaluated using Ecopath model for biomass estimations and consumption of different species
groups within aquatic ecosystems (Christensen
and Pauly, 1992b; after Polovina and Ow, 1983
and Polovina, 1985). The model considers that all

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

inputs are equal to the outputs for each species

group through a series of simultaneous lineal
equations, which for each functional group is
expressed as:
n

Bi (P/B)i EEi % Bj (Qj /Bj ) DCji EXi

i=1

= 0,
where Bi is the biomass for group/specie i, (P/B)i
the production/biomass ratio, EEi the ecotrophic

121

efficiency, which is part of production that goes

out of the system through predation and exports
(including catches); DCji the fraction of the prey
(i ) in the diet of the predator ( j ), Qj /Bj the
consumption/biomass ratio for predator ( j ), and
EXi the exportation for the prey i. Considering
this equation for n groups, a system of lineal
equations are developed where at least three of
the four parameters of each group (B, P/B, Q/B
and EE) must be known while the other one is

Fig. 1. Study area on the northwestern coast of Yucatan Peninsula showing sampling sites, freshwater seeps and mangrove
distribution.

122

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

estimated by the model. Input for migration (if

considered), and groups diets are also required.
Ecopath also links some concepts of the ecosystem properties developed by theoretical ecologists
(Odum, 1969; Ulanowicz, 1986), such as several
flow indices: (a) the total system ascendence, considered a measure of the average mutual information and used for describing ecosystem flow
characteristics (Christensen, 1994a); (b) the total
system throughput, that is the sum of all flows
(Ulanowicz and Norden, 1990); (c) the Finns
cycling index (Finn, 1980) which considers the
fraction of the ecosystem throughput that is recycled; and (d) the path length, defined as the
average number of groups that an inflow or
outflow passes through. Additionally, the fractional trophic levels of each group and the aggregation of the entire system into discrete trophic
levels sensu Lindeman (1942) are considered
(Ulanowicz, 1995), as well as determination of
mixed trophic impacts, efficiency with which organic matter is transferred from lower to higher
trophic levels (transfer efficiencies) and other important physiological information for species
groups and the ecosystem such as Omnivory index, food intake, respiration and assimilation.

2.2.1. Functional groups

To describe the ecosystem, a total of 19 functional groupings was used. Ten of them included
fish and the others invertebrates (zooplankton,
insects, micro and macro-crustaceans, molluscs,
polychaetes), benthic producers (phytoplankton,
macrophytes) and detritus (Table 1). Fish groups
were determined by Principal Component Analysis considering stomach contents in 32 dominant
species during 2 years of field research. Five fish
guilds (Root, 1967) were formed: microcrustacean, piscivorous, omnivorous, phyto and
zooplankton feeders. Within the microcrustacean
feeders group, five subgroups were separated depending on their prey preferences such as phytoplankton, zooplankton and molluscs making 63%
of the total fish species. other fish group was
referring to fishes not included in the other ecological groups (Table 2).

2.3. Sources of data

Sources and derivation of input parameters are
given in Table 3. Fish diets were determined by
stomach content analysis and for invertebrates by
Odum and Heald (1972). Considering that mangrove roots are a critical habitat for different fish
species (Robertson and Duke, 1987; Thayer et al.,
1987; Morton, 1990; Tzeng et al., 1992), catch was
estimated as zero for fish groups with the exception of gray snapper (Lutjanus griseus), which has
a national economical importance and is fished in
the area. In this case, catch data was obtained
from Ministry of Fisheries (SEPESCA, 1994).

2.4. Model balancing

Since this is a steady state model, biomass
remains unchanged and all parameters were normalised to unit surface area using wet weight for
biomass and fishery catch (g m 2), while flows
and rates were expressed on an annual basis. The
criterion used for balancing the model was
ecotrophic efficiency (EE)51. In the first attempt
EE was greater than one for fish compartments,
so inorder to correct it and because most of the
individuals of these groups are juveniles with high
production rates and low biomass, several assumptions including a P/B and a growth efficiency (GE) of 3.0 and 4.0 for fish groups,
respectively were introduced. These values are
very similar to the ones considered by Christensen
(1998) for small ecological groups (P/Q= 2.5).
Other inputs to adjust the zooplankton and microcrustaceans biomasses were P/B values of 13
and 15 considering previous studies (Moller et al.
(1985), Vega et al. 1993). The balanced model was
adjusted using the Ecoranger routine which is a
statistical procedure for selecting the best fitting
model using as criterion the minimization of
residuals after 3000 positive runs.

3. Results

3.1. Input data and estimated parameters

Given and estimated input data are shown in

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.07
0.00
0.20
0.02
0.00
0.11
0.57
0.04
0.00
1.00

Phytoplankton feeders
Zooplankton feeders
Microcrubphytoplankton feeders
Microcrubzoocphytoplankton feeders
Microcrubzooplankton feeders
Microcrumolluscs feeders
Microcrustaceans feeders
Omnivorous
Piscivorous
Other fishes
Zooplankton
Insects
Microcrustaceans
Macrocrustaceans
Molluscs
Polychaeta
Phytoplankton
Plant matter
Detritus
Totals

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.07
0.82
0.00
0.11
0.00
0.00
0.00
0.00
0.00
0.00

Predators

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.07
0.02
0.68
0.00
0.00
0.00
0.19
0.03
0.00

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.02
0.24
0.01
0.54
0.01
0.01
0.00
0.16
0.01
0.00

Values show the proportion of each prey in the diet of each predator.
Microcru, Microcrustaceans.
c
Zoo, Zooplankton.

1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.

Prey

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.31
0.00
0.64
0.00
0.00
0.03
0.00
0.03
0.00

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.03
0.01
0.00
0.33
0.09
0.36
0.01
0.00
0.04
0.13

Table 1
Predatorprey matrix for the mangrove ecosystem in Celestun Lagoon, Yucatan, Mexicoa

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.07
0.02
0.01
0.77
0.05
0.00
0.05
0.01
0.03
0.00

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.10
0.00
0.37
0.00
0.00
0.00
0.08
0.45
0.00

1.00

0.01
0.00
0.01
0.11
0.00
0.05
0.16
0.02
0.07
0.12
0.02
0.02
0.24
0.07
0.00
0.02
0.00
0.07
0.00

1.00

0.00
0.00
0.00
0.00
0.01
0.00
0.03
0.00
0.03
0.17
0.11
0.05
0.25
0.04
0.04
0.01
0.13
0.08
0.06

10

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.00
0.00
0.00
0.00
0.00
0.28
0.00
0.72

11

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.00
0.00
0.00
0.00
0.15
0.34
0.51

12

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.04
0.27
0.00
0.68

13

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.06
0.00
0.00
0.12
0.00
0.29
0.00
0.11
0.00
0.43

14

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.22
0.00
0.00
0.00
0.00
0.00
0.32
0.23
0.23

15

1.00

0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.05
0.19
0.76

16

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

123

124

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

Table 2
Descriptions of functional groups of the mangrove ecosystem in Celestun Lagoon, Yucatan, Mexico
Phytoplankton feeders
Zooplankton feeders
Microcruphytoplankton feeders
Microcruphyto
zooplankton feeders
Microcruzooplankton
feeders
Microcrumolluscs
feeders
Omnivorous
Microcrustacean
feeders
Piscivorous
Other fishes
Phytoplankton
Zooplankton
Microcrustaceans
Macrocrustaceans
Molluscs
Insects
Polychaeta
Benthic producers
Detritus

Harengula jaguana, Etrumeus teres, Mugil curema, Eucinostomus melanopterus.

Fundulus persimilis.
Species that consume benthic microcrustaceans and phytoplankton (Garmanella pulchra, Lucania par6a,
Sardinella ancho6ia, Opsanus beta).
Species that take benthic microcrustacean, phyto and zooplankton as food (Anchoa hepsetus, A.
mitchilli, Menidia colei, Floridichthys carpio).
Fish species that consume benthic microcrustaceans and zooplankton (Diapterus rhombeus,
Rhomboplites aurorubens).
Species that take benthic microcrustaceans and molluscs during feeding (Sphoeroides testudineus,
Cichlasoma urophthlamus).
Fish species that consume plant and animal sources (Opisthonema oglinum, Diapterus olisthostomus).
Fish species that consume benthic microcrustaceans (Eucinostomus gula, E. argenteus, Bairdiella
chrysoura, B. ronchus, Micropogonias furnieri, M. undulatus, Achirus lineatus, Lagodon rhomboides).
Synodus foetens, Strongylura marina, S. timucu, S. notata, Lutjanus griseus.
Fishes not identified or which species are not within the other guilds like livebearers (Poecilidae) and
gobies (Gobidae).
Chlorophyceae and Cyanophyceae.
Consider fish and crustacean eggs and larvaes, copepods.
Harpacticoid copepod, Amphipoda, Ostracoda. Mysids and Isopods are grouped.
Brachyura and Penaeus sp.
Bivalvia and Gastropoda.
Diptera, Hymenoptera, Coleoptera and insect larvaes.
Nereidae
Chara sp., Batophora sp., Halodule wrightii, Thalassia testudinum.
Organic matter and organisms associated like bacteria, microbes and fungus.

Table 4. Highest P/B, Q/B and EE values corresponded to the four groups of the trophic base of
the system: zooplankton, phytoplankton, micro
and macrocrustaceans while the lowest ones were
for fishes with low predation rates. Throughout
the study period, most of the fish groups were
characterised by small sizes with low trophic levels (TL). This parameter, estimated as the
weighted average TL of their prey group plus one
(Christensen and Pauly, 1992a) ranged between
3.6 for piscivorous and 2.0 in polychaeta. A zero
Omnivory index (OI) was determined for polychaeta that feed almost on detritus (75%) and the
highest for other fishes (0.59) that feed on preys
from different trophic levels. In fish groups a high
proportion of assimilated energy (40 60%) goes
to production, while for invertebrates it varies
from 24% in molluscs to 41% for microcrustaceans (Table 5).

3.2. Trophic fluxes and interactions

Main biomass flows between functional groups
are shown in Fig. 2. Detritus and phytoplankton
displayed the highest values for biomass and production, while consumption rate and metabolic
waste (respiration) were for zooplankton (728 and
439 g m 2 per year, respectively), followed by
microcrustaceans (437 and 213 g m 2 per year).
This has to be noted, since they are the main food
supply for fish groups and show a strong relation
with primary producers including detritus. The
fluxes to detritus were between 1.4 (omnivorous)
and 199 g m 2 per year (zooplankton) and those
to cannibalism were between 0.3 for insects and
17 for other fishes (Table 6).
The ecosystem was aggregated in seven discrete
levels, though in five of them the magnitude of the
flows represented a high fraction of the flow asso-

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

ciated with top predators (Table 7). Most of them

in trophic level II (detritivores and herbivores) are

125

attributed mainly to invertebrates such as

zooplankton, polychates and insects, with fish ac-

Table 3
Sources of input parameters for the trophic model of the mangrove ecosystem in Celestun Lagoon, Mexico
Group

Biomass

Production

P/B Q/B

Phytoplankton

Vega et al., 1993

Detritus
Macrophytas
Zooplankton

Chavez et al., 1993

Herrera-Silveira, 1995
In the field (conical net, 300 m)

Estimated by Strickland and

Parson (1972)

Yanez-Arancibia and Day (1988)

Batllori, 1988

Chavez et al. (1993), Vega et al.

(1993)

Insects
Benthosa

In the field from plankton samples

Using a Van-Been dredge

Palomares et al., 1993

Estimated by Robertson (1979)

Using drop net in mangrove areas

during 2 years of bimonthly
collections

Longevity estimates were 1, 1, 3

and 1 year for polychaetes,
microcrustaceans, penaeids and
molluscs, respectively.
Equivalent to total mortality rate. Palomares and Pauly (1989)
Vega et al. (1993), Christensen and
Pauly (1993)

Fishes

Chavez et al. (1993), Palomares et

al. (1993)
Chavez et al. (1993),
Vega-Cendejas (1998)

a
Polychaetes, microcrustaceans (amphipods, tanaidaceans), penaeids (shrimps, crabs) and molluscs (gastropods and bivalves) are
included.

Table 4
Input values and estimated values (within brackets) of the mangrove ecosystem in Celestun Lagoon. Yucatan, Mexicoa
Group

Catches

P/B

Q/B

EE

GE

Piscivorous
Zooplankton feeders
Microcrustacean feeders
Other fishes
Microcrubzooplankton feeders
Micrucrubmolluscs feeders
Microcrubzooplanktonphytoplankton feeders
Microcrubphytoplankton feeders
Macrocrustaceans
Omnivorous
Phytoplankton feeders
Molluscs
Microcrustaceans
Zooplankton
Insects
Polychaetes
Phytoplankton
Macrophytas
Detritus

0.26
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00

4.04
0.09
6.73
12.31
0.20
6.37
7.01
0.22
4.05
0.38
0.59
26.50
8.64
(10.40)
0.61
9.75
7.25
153.42
2400.0

2.77
3.76
3.09
3.33
3.59
2.52
3.12
2.57
4.01
3.06
2.62
1.84
15.75
13.75
15.54
3.84
65.55
7.45
0.00

(6.13)
(8.47)
(7.09)
(8.23)
(10.97)
(8.37)
(7.45)
(8.51)
14.86
(8.97)
(5.97)
9.58
50.51
69.91
(51.93)
13.48
0.00
0.00
0.00

(0.45)
(0.31)
(0.34)
(0.71)
(0.84)
(0.08)
(0.13)
(0.53)
(0.87)
(0.38)
(0.21)
(0.83)
(0.92)
(0.62)
(0.72)
(0.64)
(0.94)
(0.10)
(0.64)

0.45
0.44
0.44
0.40
0.33
0.30
0.42
0.30
(0.27)
0.34
0.44
(0.19)
(0.31)
0.20
0.30
(0.29)
0.00
0.00
0.00

Exportation (catches) is in g m2 per year. The relation between production and consumption with biomass (P/B) and (Q/B)
are annual rates, while biomass is expressed in g m2. EE and GE are ecotrophic and growth efficiencies, both without units.
b
microcru, microcrustaceans.

126

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

Table 5
Biological statistics estimated and parameterised by ECORANGER routine for the mangrove ecosystem in Celestun Lagoona
Group

NT

OI

Piscivorous
Zooplankton feeders
Microcrustacean feeders
Other fishes
Microcrubzooplankton feeders
Microcrubmolluscs feeders
Microcrubzoophytoplankton feeders
Microcrubphytoplankton feeders
Macrocrustaceans
Omnivorous
Phytoplankton feeders
Molluscs
Microcrustaceans
Zooplankton
Insects
Polychaetes
Phytoplankton
Macrophytas
Detritus

3.57
3.09
3.09
3.04
3.00
3.00
2.89
2.83
2.59
2.49
2.42
2.22
2.04
2.01
2.01
2.00
1.00
1.00
1.00

0.42
0.07
0.12
0.59
0.03
0.25
0.18
0.20
0.45
0.27
0.28
0.17
0.04
0.01
0.01
0.00
0.00
0.00
0.44

19.79
0.60
38.16
81.05
1.76
42.65
41.77
1.49
48.15
2.72
2.79
203.09
349.23
581.39
25.34
105.15
0.00
0.00
0.00

11.18
0.33
20.70
40.94
0.72
16.06
21.82
0.56
20.70
1.16
1.53
48.66
136.19
142.95
142.95
37.44
0.00
0.00
0.00

8.61
0.64
17.40
40.1
1.59
26.59
19.95
0.93
31.92
1.56
1.26
154.47
213.13
438.49
15.87
67.70
0.00
0.00
0.00

a
Fractional trophic level (NT) and Omnivory index (OI) are without units, while assimilation (A), production (P) and respiration
(R) are expressed in g m2 per year.
b
Microcru: microcrustaceans.

counting for only 29%, while in trophic levels III

and IV, fish take more of 90% of all flows. Of the
total net primary production (15 550 g m 2) only
about 4% is grazed by herbivores, 7% goes toward
detritus and the rest is exported to adjacent
ecosystems (lagoon and coastal zone). The
ecotroffic efficiency of detritus, (Table 4) showed
that 64% of the flows are used by the ecosystem
and the rest is buried in the sediment or exported.
The proportion of these flows, considered by
Odum (1969) as a maturity measure, was of 50%
from the total throughput (4545g m 2) and considering all flows, 58% came from detritus/net
primary production (Level I), 35% from herbivores (Level II), 6, 0.7, and 0.1% from the first,
second and third consumers. The geometric mean
of transfer efficiency was 9.6% (calculated for
trophic levels IIV) with a tendency to higher
values for lower trophic levels due to the heterotrophic production (Degnbol, 1993) (Fig. 3).
From the mixed trophic impact routine
(Ulanowicz and Puccia, 1990) it was possible to
evaluate the consequences of a biomass change of

one group over the others (including competition). Detritus, macrophytas, phytoplankton and
microcrustacean had a strong positive impact on
the other components, (Fig. 4) while top predators (piscivorous) and other fishes had a negative
impact on fish groups, but a positive one on the
prey of their preys (cascade effect). Most of the
groups had a negative impact within themselves,
reflecting competition for food resources.

3.3. System properties

Some system properties have been used to evaluate the status of the ecosystem considering its
maturity (Odum, 1969). The development capacity (C) that is the upper limit for the size of the
ascendency and the system overhead reflects the
systems strength in reserve perturbations
(Ulanowicz, 1986). Results in Table 7, show that
the ecosystem under study with a size of 5138
flowbits had a great overhead. Relative ascendency defined as the ratio between the ascendency
and the development capacity had a value of 0.24.

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

Its complement to one is the relative systems

overhead, which may be taken as a measure of
system stability (Christensen, 1994b). Primary
production reached a value of 155 000 g m 2 per
year while P/R and P/B were above one. Both
relationships are considered by Odum (1971) as
energetic parameters related to maturity. The
number of unions within the model (Connectance

127

index), proportional to the number of functional

group (Nee, 1990), reached a value of 0.3 and the
Omnivory index 0.2. Those indices are a measure
of the distribution of the trophic interactions between the different trophic levels of the system the
Finns cycling index (Finn, 1980), indicated that
13% of the total throughput of the system is
recycled. Additionally the path length, which increases with maturity had a value of 4.4.

Fig. 2. Trophic interactions in the Celestun mangrove Lagoon. All the flows expressed in g m 2 per year enter a box through the
base and exit from the top. Each of the groups are placed on the Y-axis considering their trophic level. Biomass (B), Production
(P), consumption (Q), the losses by respiration, the flows to detritus and cannibalism are specified. This last flow is represented as
arrows originating from the top half upper part of a box and moving in a partial circle before entering the lower half.

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

128

Table 6
Relative flows for each functional groups are shown by discrete trophic level according to Lindeman (1942)
Group

II

III

IV

Piscivorous
Zooplankton feeders
Microcrustacean feeders
Other fishes
Microcruazooplankton feeders
Microcruamolluscs feeders
Microcruazoophytoplankton feeders
Microcruaphytoplankton feeders
Macrocrustaceans
Omnivorous
Phytoplankton feeders
Molluscs
Microcrustaceans
Zooplankton
Insects
Polychaetes
Phytoplankton
Macrophytas
Detritus

100.0
100.0
100.0

8.0

4.0
35.0
3.0
17.0
17.0
22.0
54.0
53.0
60.0
78.0
96.00
100.0
100.0
100.0

47.0
99.0
90
57.0
95.0
68.0
79.0
74.0
36.0
45.0
38.0
22.0
4.0

41.0
1.0
6.0
6.0
2.0
14.0
4.0
4.0
10.0
2.0
2.0

4.0

2.0

1.0
0.0
0.0
0.0

0.0

Microcru, microcrustaceans.

4. Discussion
Mangroves are energetic sources where about
half of the detritus produced by fallen leaves is
exported to adjacent aquatic regions mostly by
tidal flush (Jacobi and Schaeffer-Novelli, 1990).
The other half is used by juvenile stages as a
source of food by direct grazing on leaves and
indirectly by detritus consumption (Lugo and
Snedaker, 1974; Thayer et al., 1987). The importance of these biological and energetic processes
within these swamps is shown by the dependence
of detritus of two thirds of the world fisheries
(Lai, 1984). Increased cycling and storage both
tend to increase the ratio of indirect to direct
flows and contribute to network amplification and
homogenization of available energy over all
trophic levels (Patten et al., 1990). Detritus recycling or reutilization involves the subsequent
transformation of previously utilized but not dissipated energy-matter by consumers (Higashi et
al., 1993).
This paradigm established by the work of
Odum and Heald (1972, 1975) in southern Florida, has been subsequently modified to include

Table 7
Global system properties of the mangrove ecosystem in Celestun Lagoona
Attribute

Value

Total system throughput

4581

Sum of all consumption

Sum of all respiratory flows
Sum of all flows into detritus

1931
1040
1609

Net primary production

Total primary production/total
respiration
Total primary productivity/biomass

15 550
15.9
64.0

Connectance index
Omnivory index
Finns cycling index

0.3
0.2
13.4% of
throughput

Finns average path length

Capacity of the system
Overhead
Ascendency

4.4
20 803
16 665
5138

Biomass in g m2, flows in g m2 per year.

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

Fig. 3. Aggregation of the energy-flow web showing transfers

(%) through each trophic level sensu Lindeman (1942). Flows
out of the top boxes represent exports and out of lower
middle, the respiration (g m 2 per year). Flows originated
from detritus and the ones derived from primary producers are
specified.

alternative energy and carbon sources for consumers (Twilley, 1988; Robertson et al., 1992).
The energy and material cycles within ecosystems
are considered an important process (Odum,
1969). The complex biological, biochemical and
physical interactions determine the proportion of
these fluxes and the efficiency with which the
energy is assimilated, transferred and dissipated
within the ecosystem components contributing to
its autonomous behaviour (Ulanowicz, 1986).
The lower fractional trophic levels showed that
most of them are made of juveniles whose production depend direct and indirectly on primary producers
(macrophytas,
phytoplankton
and
detritus). The top predators (piscivorous) level
alues are low (3.6) compared with other close
ecosystems where the fishery is the main predator
(TL = 4.2) such as Celestun Lagoon and shallow
coastal waters (Chavez et al., 1993; Vega et al.,
1993) and the continental shelf of Campeche,
TL = 4.3 (Manickchand-Heileman et al., 1998).
The net production, which is the amount of
energy (or organic carbon) remaining after respiration was 1924 kcal m 2 per year higher than
the one in Florida mangroves (Twilley, 1988).
From the total fluxes to detritus, a major portion

129

(66%) came from primary producers (Trophic

Level I), whereas 26 and only 7% from primary
and secondary consumers, respectively.
Because most of the biomass from primary
producers and first trophic level consumers are
transferred through predation (84 and 16%, respectively), they conform the trophic base for the
mangrove ecosystem. These same results were
found by Gadke and Srtraile (1994) in Lake Constanza, where the transfer of primary production
to herbivores dominates the flow of matter within
the planktonic food web.
The relevance of the lower trophic levels in the
secondary production can be seen in the Leontief
(1951) where on the basis of fluxes and trophic
transfers, these groups (primary producers, microcrustaceans) have a positive impact on almost all
others and constitute an important link between
detritus and higher trophic levels in passing energy up to the food-web (Fig. 4). A change of
biomass or production of these basic trophic
groups will affect the other functional components by their value as food for almost all of
them. In the same sense, the Q/B ratio for piscivorous and other fish groups depend on the
biomass of the groups on which they feed (zooplanton feeders, microcrustacean and zooplankton feeders).
The estimated values of some properties, such
as the ascendency and development capacity are
tools to evaluate the organisation, maturity and
tolerance perturbations as well as for ecosystems
comparison (Mann et al., 1989; Baird et al.,
1991). According to Ulanowicz (1986) these properties tend to increase with maturity and decrease
in systems under natural or anthropogenic
stresses. However, Christensen (1995) and Aoki
(1997) stated that ascendency is not a good indicator of the degree of eutrophication and maturation, and has a negative correlation with them;
suggesting that relative ascendency should be
called a relative mutual information which provides a measure of the distribution of flows in a
system network in relation with the total flow
(Patten, 1995). Relative ascendency (25%) and the
Finn cycling index (13.4%), are lower than those
reported by Baird and Ulanowicz (1993) for four
coastal systems in Scotland, Holland and South

130

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

Africa. However, the flows diversity (4.5) is very

similar and is considered by this authors as high,
meaning a mature system with a high recycled
rate and low perturbations (Odum, 1969).
Mangrove ecosystem and its energetic characteristics are a mixture of immature and mature
properties. Between the attributes that reflect immaturity are: (a) the relation between primary
production and respiration (15.9) meaning an excess of production flowing to respiration; (b) high
P/B ratio (64.0) for all the system; and (c) the low
ratio between biomass and throughput (0.1).
Moreover, high primary production (15 500 g
m 2 per year) and small size of the individuals
are often associated with immature systems. On
the other side, detritus-based food webs, high fish
and flow diversities are typically related to maturity (Table 6). The above properties suggest that
communities associated to mangrove are a transi-

tion between immature and mature systems characterised by high productivity, biomass and
species diversity.
System recovery time, that is the time required
for all functional groups to return to baseline, is
used as a measure of stability and is negatively
correlated with the Finns cycling (Vasconcellos et
al., 1997; Perez-Espana and Arregun-Sanchez,
1999). Systems with a high capacity to recycle
detritus show greater ability to recover from. In
this study, the Finns cycling index was high
(13.4), so we can conclude that high recycling,
basically detritus, is a chief positive feedback
mechanism that contributes to the maintenance of
the ecosystem stability by preventing overshoots
and destructive oscillations from external impacts.
The energy flows described here using Ecopath
constitute a preliminary approach to the knowledge of how energy from a mangrove ecosystem

Fig. 4. Mixed trophic impacts for the mangrove ecosystem analyzed by Leontief (1951). Positive and negative effects on the biomass
of each compartment are represented over and below the line, respectively. Group values with not significative impacts are specified.
Micro, microcrustaceans; Zoo, zooplankton; Phyto, phytoplankton.

M.E. Vega-Cendejas, F. Arregun-Sanchez / Ecological Modelling 137 (2001) 119133

flows to other systems through the associated fish

community. The merit of this model is that most
of the input data (biomass of functional groups)
have been taken in the field and that fish species
trophic structure has been determined from the
stomach content analysis. However, in spite that
other values (i.e. Q/B for invertebrates) come
from literature, we hope that this study will encourage new investigations in this field.

Acknowledgements
We thank Luis Capurro for his valuable suggestions and review of an early manuscript. To
Mirella Hernandez, Victor Castillo and Adrian F.
Gonzales for their help so willingly in field and
the stomach contents analysis. Particularly appreciation is owed to CONACTY who funded the
study (Project F467-N9109). FAS thanks National Politechnic Institute for partial support
through CEGEPI-9800566, COFAA and EDD.

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