Ecological Modelling 137 (2001) 119–133

Energy fluxes in a mangrove ecosystem from a coastallagoon in Yucatan Peninsula, Mexico

M.E. Vega-Cendejas a,*, F. Arreguın-Sanchez b

a Centro de In6estigacion y de Estudios, Unidad Merida, A6anzados del IPN, A.P. 73 Cordemex, Merida, 97310 Yucatan, Mexicob 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 with19 functional groups including primary producers and three levels of carnivores. Some input data (biomass of the fishgroups, zooplankton and benthic communities) were obtained from the field and by stomach content analysis ofdominant fish species (32) while others were taken from previous studies. Within fish, nine functional groups wereobtained through trophic similarity analysis, being microcrustaceans an important prey in five of them. Resultsshowed that a great proportion of the primary production is exported to adjacent ecosystem while within the systemonly 4% is grazed and 7% goes to detritus, with a detritivory/herbivory ratio of 2.0. Within the mangrove, detritusplays 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 anegative one occurred with increasing biomass at high trophic compartments (‘other fish’ and piscivorous). Small EEfor fish groups indicated a low predation rate to these groups, while greater P/B and Q/B suggest that mangrove isa high productive system with characteristic properties of a transition between mature and immature stage. © 2001Elsevier Science B.V. All rights reserved.

Keywords: Ecopath model; Mangrove ecosystem; Energy fluxes; Yucatan Peninsula

www.elsevier.com/locate/ecolmodel

1. Introduction

Mangrove wetlands are one of the most pro-ductive aquatic ecosystems covering 240×105

km2 of subtropical and tropical coastline

characterised by high number of primary produc-ers, diversity of microhabitats, complex multispe-cies interactions and by intensive exchange oforganic matter and organisms within and outsidethe ecosystem (Day et al., 1989; Twilley et al.,1992). These halophytic species are of great en-ergetic importance because they provide food (viadetritus) to both estuarine and ocean consumers,serve as habitat for early stages, juveniles andadult of estuarine and marine organisms and play

* 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. Arreguın-Sanchez).

0304-3800/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved.

PII: S 0304 -3800 (00 )00421 -X

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133120

an important role in the regulation of estuarinechemical cycles (Mitch and Gosselink, 1993).

To understand mangrove ecosystem dynamics,a study of multispecies interactions is needed in-cluding trophic fluxes, assimilation efficiencies andenergy transfer and dissipation (Beddington,1984; Steele, 1984; Baird and Ulanowicz, 1993).They are reflected on diversity, abundance, distri-bution and persistency of the biological compo-nents which finally are regulated by primaryproductivity (Oksanen et al., 1981; Oksanen,1983), environmental variability (Pimm andKitching, 1987) and a combination of both(Persson et al., 1992). Models, defined as soliddescriptions that emphasise some aspects of thesystems in order to understand how they work(Christensen and Pauly, 1992a, 1996), are ecosys-tem representations that permit to understandtheir complexity in energy terms, to identify theirlevel of production, to compare energy transferbetween ecosystems, and to evaluate the func-tional reaction to natural and/or anthropogenicimpacts.

Knowledge of trophic interactions in aquaticecosystem has considerably improved through thedesign of mass-balance processes (Christensen andPauly, 1993). In energy terms, this kind of analy-sis is important because it allows the computationof the fish biomass that can be sustained byprimary production (Halfon et al., 1996). How-ever, in spite of mangrove importance for provid-ing shelter and feeding grounds to marine andfreshwater fish species, there exist few ecologicalmodels compared with other wetlands ecosystems(Mitch and Gosselink, 1993). Lugo et al. (1976)based on energy and material flows approachshowed that reduction in upland run-off caused adecrease in its productivity, and that the timerequired to reach steady-state levels of mangrovebiomass was similar to the average frequency oftropical hurricanes during 20 years. Adams (1976)characterised a fish community by its functionalrole considering consumption, production andmetabolism data for the dominant species. Chavezet al. (1993) carried out some investigations inCelestun coastal lagon, Yucatan, using Ecopath IIand Vega et al. (1993) for the beach seine fisheryon Campeche Bank. However, no models describ-

ing energy fluxes in a mangrove ecosystem arepresently been represented. In this sense, the ob-jective of this study is the construction of a man-grove ecosystem trophic model in order toquantify its structure and function, to determineits flows of energy and the role of the fish commu-nity in transferring energy from the mangroveareas to adjacent ecosystems.

2. Materials and methods

2.1. Study area

Celestun Lagoon is a tropical ecosystem locatedin the Gulf of Mexico on the northeast of theYucatan Peninsula (20°45%–20°58% N and 90°15%–90°25% W), (Fig. 1). Parallel to the coastline, thisnarrow (0.5–2.4 km wide) and shallow (0.5–3.0m) lagoon is connected with the sea by a perma-nent 410 m wide mouth at its southern part(Herrera-Silveira, 1996). Weather is warm (meanannual temperature \26°C), semi-arid (794.7mm annual precipitation) and 80% of relativehumidity (Garcıa and Mosino, 1992). There areno rivers, so the freshwater inputs come fromunderground seeps located in the northern part ofthe lagoon and from heavy rains during the rainyseason (July–October). The water temperatureshows small variations with the lowest values inFebruary during north winds (22.4°C) and highestin June (31.4°C). Salinity shows spatial variationswith 35% in the mouth to 0–6% in the head.Along the coast, there is a 150 m long fringe ofRizophora mangle ; while inside the lagoon, thedominant species are Laguncularia racemosa inthe head; R. mangle and A6icennia germinans inthe mixing zone and A. germinans in the mouth(Sanchez-Arguelles, 1994).

2.2. Ecopath model

Trophic interactions and energy fluxes wereevaluated using Ecopath model for biomass esti-mations and consumption of different speciesgroups within aquatic ecosystems (Christensenand Pauly, 1992b; after Polovina and Ow, 1983and Polovina, 1985). The model considers that all

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133 121

inputs are equal to the outputs for each speciesgroup through a series of simultaneous linealequations, which for each functional group isexpressed as:

Bi(P/B)i · EEi− %n

i=1

· Bj · (Qj/Bj) · DCji−EXi

=0,

where Bi is the biomass for group/specie i, (P/B)i

the production/biomass ratio, EEi the ecotrophic

efficiency, which is part of production that goesout 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 theconsumption/biomass ratio for predator ( j ), andEXi the exportation for the prey i. Consideringthis equation for n groups, a system of linealequations are developed where at least three ofthe four parameters of each group (B, P/B, Q/Band 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 mangrovedistribution.

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133122

estimated by the model. Input for migration (ifconsidered), and group’s diets are also required.

Ecopath also links some concepts of the ecosys-tem properties developed by theoretical ecologists(Odum, 1969; Ulanowicz, 1986), such as severalflow indices: (a) the total system ascendence, con-sidered a measure of the average mutual informa-tion and used for describing ecosystem flowcharacteristics (Christensen, 1994a); (b) the totalsystem throughput, that is the sum of all flows(Ulanowicz and Norden, 1990); (c) the Finn’scycling index (Finn, 1980) which considers thefraction of the ecosystem throughput that is recy-cled; and (d) the path length, defined as theaverage number of groups that an inflow oroutflow passes through. Additionally, the frac-tional trophic levels of each group and the aggre-gation of the entire system into discrete trophiclevels sensu Lindeman (1942) are considered(Ulanowicz, 1995), as well as determination ofmixed trophic impacts, efficiency with which or-ganic matter is transferred from lower to highertrophic levels (transfer efficiencies) and other im-portant physiological information for speciesgroups and the ecosystem such as Omnivory in-dex, food intake, respiration and assimilation.

2.2.1. Functional groupsTo describe the ecosystem, a total of 19 func-

tional groupings was used. Ten of them includedfish and the others invertebrates (zooplankton,insects, micro and macro-crustaceans, molluscs,polychaetes), benthic producers (phytoplankton,macrophytes) and detritus (Table 1). Fish groupswere determined by Principal Component Analy-sis considering stomach contents in 32 dominantspecies during 2 years of field research. Five fishguilds (Root, 1967) were formed: microcrus-tacean, piscivorous, omnivorous, phyto andzooplankton feeders. Within the microcrustaceanfeeders group, five subgroups were separated de-pending on their prey preferences such as phyto-plankton, zooplankton and molluscs making 63%of the total fish species. ‘other fish’ group wasreferring to fishes not included in the other eco-logical groups (Table 2).

2.3. Sources of data

Sources and derivation of input parameters aregiven in Table 3. Fish diets were determined bystomach content analysis and for invertebrates byOdum and Heald (1972). Considering that man-grove roots are a critical habitat for different fishspecies (Robertson and Duke, 1987; Thayer et al.,1987; Morton, 1990; Tzeng et al., 1992), catch wasestimated as zero for fish groups with the excep-tion of gray snapper (Lutjanus griseus), which hasa national economical importance and is fished inthe area. In this case, catch data was obtainedfrom Ministry of Fisheries (SEPESCA, 1994).

2.4. Model balancing

Since this is a steady state model, biomassremains unchanged and all parameters were nor-malised to unit surface area using wet weight forbiomass and fishery catch (g m−2), while flowsand rates were expressed on an annual basis. Thecriterion used for balancing the model wasecotrophic efficiency (EE)51. In the first attemptEE was greater than one for fish compartments,so inorder to correct it and because most of theindividuals of these groups are juveniles with highproduction rates and low biomass, several as-sumptions including a P/B and a growth effi-ciency (GE) of 3.0 and 4.0 for fish groups,respectively were introduced. These values arevery similar to the ones considered by Christensen(1998) for small ecological groups (P/Q=2.5).Other inputs to adjust the zooplankton and mi-crocrustaceans biomasses were P/B values of 13and 15 considering previous studies (Moller et al.(1985), Vega et al. 1993). The balanced model wasadjusted using the Ecoranger routine which is astatistical procedure for selecting the best fittingmodel using as criterion the minimization ofresiduals after 3000 positive runs.

3. Results

3.1. Input data and estimated parameters

Given and estimated input data are shown in

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133 123

Tab

le1

Pre

dato

r–pr

eym

atri

xfo

rth

em

angr

ove

ecos

yste

min

Cel

estu

nL

agoo

n,Y

ucat

an,

Mex

icoa

Pre

yP

reda

tors

34

56

78

910

1112

1314

1516

12

0.00

0.00

0.00

0.00

0.01

1.0.

00P

hyto

plan

kton

feed

ers

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

0.00

0.00

Zoo

plan

kton

feed

ers

0.00

0.00

0.00

2.0.

000.

000.

000.

00M

icro

crub

–phy

topl

ankt

onfe

eder

s0.

000.

000.

000.

000.

010.

000.

000.

000.

000.

000.

000.

000.

000.

000.

003.

0.00

0.00

0.00

0.00

0.11

4.0.

00M

icro

crub

–zoo

c –phy

topl

ankt

onfe

eder

s0.

000.

000.

000.

000.

000.

000.

000.

000.

000.

000.

000.

000.

000.

000.

000.

010.

000.

000.

000.

000.

000.

000.

000.

000.

005.

Mic

rocr

ub–z

oopl

ankt

onfe

eder

s0.

000.

00M

icro

cru–

mol

lusc

sfe

eder

s0.

000.

000.

000.

000.

050.

000.

000.

000.

000.

000.

000.

000.

000.

000.

006.

0.00

0.00

0.00

0.00

0.16

0.03

0.00

0.00

7.0.

00M

icro

crus

tace

ans

feed

ers

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.00

0.02

0.00

0.00

0.00

0.00

0.00

Om

nivo

rous

0.00

0.00

0.00

8.0.

000.

000.

000.

00P

isci

voro

us0.

000.

000.

000.

000.

070.

030.

000.

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000.

000.

000.

000.

009.

0.02

Oth

erfis

hes

0.00

0.03

0.07

0.00

0.12

0.17

0.00

0.00

0.00

0.06

0.00

0.00

0.00

0.07

0.01

10.

0.31

0.01

0.02

0.10

0.02

0.11

0.01

0.00

0.24

0.00

Zoo

plan

kton

0.00

0.22

0.00

11.

0.07

0.82

0.07

0.01

Inse

cts

0.00

0.00

0.01

0.00

0.02

0.05

0.00

0.01

0.00

0.00

0.00

0.00

0.00

0.00

0.02

12.

0.64

0.33

0.77

0.37

0.24

0.25

0.00

0.00

13.

0.00

Mic

rocr

usta

cean

s0.

120.

000.

000.

200.

110.

680.

540.

000.

090.

050.

000.

070.

040.

000.

000.

010.

00M

acro

crus

tace

ans

0.00

0.00

0.00

14.

0.00

0.00

0.02

0.01

Mol

lusc

s0.

000.

360.

000.

000.

000.

040.

000.

000.

000.

290.

000.

000.

000.

000.

0015

.0.

030.

0116

.0.

05P

olyc

haet

a0.

000.

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040.

000.

000.

000.

110.

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000.

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010.

080.

000.

130.

280.

150.

160.

270.

000.

110.

320.

050.

1917

.P

hyto

plan

kton

0.57

0.01

Pla

ntm

atte

r0.

030.

040.

030.

450.

070.

080.

000.

340.

000.

000.

230.

190.

040.

000.

0318

.0.

000.

1319

.0.

00D

etri

tus

0.00

0.00

0.06

0.72

0.51

0.68

0.43

0.23

0.76

0.00

0.00

0.00

0.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

1.00

Tot

als

1.00

aV

alue

ssh

owth

epr

opor

tion

ofea

chpr

eyin

the

diet

ofea

chpr

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icro

cru,

Mic

rocr

usta

cean

s.c

Zoo

,Z

oopl

ankt

on.

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133124

Table 2Descriptions of functional groups of the mangrove ecosystem in Celestun Lagoon, Yucatan, Mexico

Harengula jaguana, Etrumeus teres, Mugil curema, Eucinostomus melanopterus.Phytoplankton feedersZooplankton feeders Fundulus persimilis.

Species that consume benthic microcrustaceans and phytoplankton (Garmanella pulchra, Lucania par6a,Microcru–phyto-plankton feeders Sardinella ancho6ia, Opsanus beta).

Microcru–phyto– Species that take benthic microcrustacean, phyto and zooplankton as food (Anchoa hepsetus, A.mitchilli, Menidia colei, Floridichthys carpio).zooplankton feedersFish species that consume benthic microcrustaceans and zooplankton (Diapterus rhombeus,Microcru–zooplankton

feeders Rhomboplites aurorubens).Microcru–molluscs Species that take benthic microcrustaceans and molluscs during feeding (Sphoeroides testudineus,

Cichlasoma urophthlamus).feedersFish species that consume plant and animal sources (Opisthonema oglinum, Diapterus olisthostomus).OmnivorousFish species that consume benthic microcrustaceans (Eucinostomus gula, E. argenteus, BairdiellaMicrocrustacean

feeders chrysoura, B. ronchus, Micropogonias furnieri, M. undulatus, Achirus lineatus, Lagodon rhomboides).Synodus foetens, Strongylura marina, S. timucu, S. notata, Lutjanus griseus.Piscivorous

Other fishes Fishes not identified or which species are not within the other guilds like livebearers (Poecilidae) andgobies (Gobidae).

Phytoplankton Chlorophyceae and Cyanophyceae.Zooplankton Consider fish and crustacean eggs and larvaes, copepods.

Harpacticoid copepod, Amphipoda, Ostracoda. Mysids and Isopods are grouped.MicrocrustaceansBrachyura and Penaeus sp.MacrocrustaceansBivalvia and Gastropoda.Molluscs

Insects Diptera, Hymenoptera, Coleoptera and insect larvaes.NereidaePolychaeta

Benthic producers Chara sp., Batophora sp., Halodule wrightii, Thalassia testudinum.Organic matter and organisms associated like bacteria, microbes and fungus.Detritus

Table 4. Highest P/B, Q/B and EE values corre-sponded to the four groups of the trophic base ofthe system: zooplankton, phytoplankton, microand macrocrustaceans while the lowest ones werefor fishes with low predation rates. Throughoutthe study period, most of the fish groups werecharacterised by small sizes with low trophic lev-els (TL). This parameter, estimated as theweighted average TL of their prey group plus one(Christensen and Pauly, 1992a) ranged between3.6 for piscivorous and 2.0 in polychaeta. A zeroOmnivory index (OI) was determined for poly-chaeta that feed almost on detritus (75%) and thehighest for ‘other fishes’ (0.59) that feed on preysfrom different trophic levels. In fish groups a highproportion of assimilated energy (40–60%) goesto production, while for invertebrates it variesfrom 24% in molluscs to 41% for microcrus-taceans (Table 5).

3.2. Trophic fluxes and interactions

Main biomass flows between functional groupsare shown in Fig. 2. Detritus and phytoplanktondisplayed the highest values for biomass and pro-duction, while consumption rate and metabolicwaste (respiration) were for zooplankton (728 and439 g m−2 per year, respectively), followed bymicrocrustaceans (437 and 213 g m−2 per year).This has to be noted, since they are the main foodsupply for fish groups and show a strong relationwith primary producers including detritus. Thefluxes to detritus were between 1.4 (omnivorous)and 199 g m−2 per year (zooplankton) and thoseto cannibalism were between 0.3 for insects and17 for other fishes (Table 6).

The ecosystem was aggregated in seven discretelevels, though in five of them the magnitude of theflows represented a high fraction of the flow asso-

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133 125

ciated with top predators (Table 7). Most of themin trophic level II (detritivores and herbivores) are

attributed mainly to invertebrates such aszooplankton, polychates and insects, with fish ac-

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

ProductionGroup P/B Q/BBiomass

Estimated by Strickland andPhytoplankton Chavez et al. (1993), Vega et al.Vega et al., 1993(1993)Parson (1972)

Detritus Chavez et al., 1993 – –Herrera-Silveira, 1995Macrophytas Yanez-Arancibia and Day (1988)

Batllori, 1988Zooplankton In the field (conical net, 300 m) Chavez et al. (1993), Palomares etal. (1993)

Palomares et al., 1993Insects In the field from plankton samplesBenthosa Estimated by Robertson (1979)Using a Van-Been dredge Chavez et al. (1993),

Vega-Cendejas (1998)Longevity estimates were 1, 1, 3and 1 year for polychaetes,microcrustaceans, penaeids andmolluscs, respectively.

Palomares and Pauly (1989)Fishes Using drop net in mangrove areas Equivalent to total mortality rate.Vega et al. (1993), Christensen andduring 2 years of bimonthly

collections Pauly (1993)

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

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

Group GEEEQ/BP/BBCatches

2.774.04 (0.45)0.26Piscivorous (6.13) 0.450.00 0.09 3.76 (8.47) (0.31) 0.44Zooplankton feeders0.00 6.73Microcrustacean feeders 0.443.09 (0.34)(7.09)0.00 0.40Other fishes (0.71)(8.23)3.3312.310.00Microcrub–zooplankton feeders (0.84) 0.33(10.97)3.590.20

0.30(0.08)(8.37)2.526.370.00Micrucrub–molluscs feeders(0.13) 0.427.01 3.12Microcrub–zooplankton–phytoplankton feeders (7.45)0.00(0.53) 0.300.22 2.57Microcrub–phytoplankton feeders (8.51)0.00

(0.27)(0.87)14.864.01Macrocrustaceans 4.050.00(0.38) 0.340.38 3.06Omnivorous (8.97)0.00

0.00 0.59 2.62Phytoplankton feeders (5.97) (0.21) 0.44(0.19)(0.83)9.581.84Molluscs 26.500.00

0.00 8.64 15.75Microcrustaceans 50.51 (0.92) (0.31)(0.62) 0.20Zooplankton 0.00 (10.40) 13.75 69.91

0.00 0.61 15.54Insects (51.93) (0.72) 0.30Polychaetes 0.00 9.75 3.84 13.48 (0.64) (0.29)

65.55Phytoplankton 7.25 0.00(0.94)0.000.000.00Macrophytas 7.45153.42 0.00 (0.10) 0.000.00 2400.0 0.00Detritus 0.00 (0.64) 0.00

a Exportation (catches) is in g m−2 per year. The relation between production and consumption with biomass (P/B) and (Q/B)are annual rates, while biomass is expressed in g m−2. EE and GE are ecotrophic and growth efficiencies, both without units.

b microcru, microcrustaceans.

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133126

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

OI A PNT RGroup

0.42 19.79 11.18Piscivorous 8.613.570.07 0.603.09 0.33Zooplankton feeders 0.640.12 38.16Microcrustacean feeders 20.703.09 17.400.59 81.053.04 40.94Other fishes 40.10.03 1.76 0.72Microcrub–zooplankton feeders 1.593.000.25 42.653.00 16.06Microcrub–molluscs feeders 26.590.18 41.77Microcrub–zoo–phytoplankton feeders 21.822.89 19.950.20 1.492.83 0.56Microcrub–phytoplankton feeders 0.930.45 48.15Macrocrustaceans 20.702.59 31.920.27 2.722.49 1.16Omnivorous 1.560.28 2.79Phytoplankton feeders 1.532.42 1.260.17 203.092.22 48.66Molluscs 154.47

Microcrustaceans 2.04 0.04 349.23 136.19 213.130.01 581.392.01 142.95Zooplankton 438.490.01 25.34Insects 142.952.01 15.870.00 105.152.00 37.44Polychaetes 67.700.00 0.00Phytoplankton 0.001.00 0.000.00 0.001.00 0.00Macrophytas 0.000.44 0.00Detritus 0.001.00 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 m−2 per year.

b Microcru: microcrustaceans.

counting for only 29%, while in trophic levels IIIand IV, fish take more of 90% of all flows. Of thetotal net primary production (15 550 g m−2) onlyabout 4% is grazed by herbivores, 7% goes towarddetritus and the rest is exported to adjacentecosystems (lagoon and coastal zone). Theecotroffic efficiency of detritus, (Table 4) showedthat 64% of the flows are used by the ecosystemand the rest is buried in the sediment or exported.The proportion of these flows, considered byOdum (1969) as a maturity measure, was of 50%from the total throughput (4545g m−2) and con-sidering all flows, 58% came from detritus/netprimary production (Level I), 35% from herbi-vores (Level II), 6, 0.7, and 0.1% from the first,second and third consumers. The geometric meanof transfer efficiency was 9.6% (calculated fortrophic levels II–V) with a tendency to highervalues for lower trophic levels due to the hetero-trophic production (Degnbol, 1993) (Fig. 3).

From the mixed trophic impact routine(Ulanowicz and Puccia, 1990) it was possible toevaluate the consequences of a biomass change of

one group over the others (including competi-tion). Detritus, macrophytas, phytoplankton andmicrocrustacean had a strong positive impact onthe other components, (Fig. 4) while top preda-tors (piscivorous) and ‘other fishes’ had a negativeimpact on fish groups, but a positive one on theprey of their preys (cascade effect). Most of thegroups had a negative impact within themselves,reflecting competition for food resources.

3.3. System properties

Some system properties have been used to eval-uate the status of the ecosystem considering itsmaturity (Odum, 1969). The development capac-ity (C) that is the upper limit for the size of theascendency and the system overhead reflects thesystem’s strength in reserve perturbations(Ulanowicz, 1986). Results in Table 7, show thatthe ecosystem under study with a size of 5138flowbits had a great overhead. Relative ascen-dency defined as the ratio between the ascendencyand the development capacity had a value of 0.24.

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133 127

Its complement to one is the relative systemsoverhead, which may be taken as a measure ofsystem stability (Christensen, 1994b). Primaryproduction reached a value of 155 000 g m−2 peryear while P/R and P/B were above one. Bothrelationships are considered by Odum (1971) asenergetic parameters related to maturity. Thenumber of unions within the model (Connectance

index), proportional to the number of functionalgroup (Nee, 1990), reached a value of 0.3 and theOmnivory index 0.2. Those indices are a measureof the distribution of the trophic interactions be-tween the different trophic levels of the system theFinn’s cycling index (Finn, 1980), indicated that13% of the total throughput of the system isrecycled. Additionally the path length, which in-creases 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 thebase 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 asarrows 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. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133128

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

Group III III IV V

8.0 47.0Piscivorous 41.0– 4.0–Zooplankton feeders – 99.0 1.0 –

4.0 90– 6.0Microcrustacean feeders –35.0 57.0Other fishes 6.0– 2.0

3.0 95.0– 2.0Microcrua–zooplankton feeders –17.0 68.0 14.0Microcrua–molluscs feeders 1.0–17.0 79.0– 4.0Microcrua–zoo–phytoplankton feeders 0.0

–Microcrua–phytoplankton feeders 22.0 74.0 4.0 0.0–Macrocrustaceans 54.0 36.0 10.0 0.0

53.0 45.0– 2.0Omnivorous ––Phytoplankton feeders 60.0 38.0 2.0 0.0

78.0 22.0– –Molluscs –96.00 4.0Microcrustaceans –– –

100.0 –– –Zooplankton –100.0 – –Insects ––100.0 –– –Polychaetes –

100.0Phytoplankton – – – –100.0Macrophytas – – – –

– –100.0 –Detritus –

a Microcru, microcrustaceans.

4. Discussion

Mangroves are energetic sources where abouthalf of the detritus produced by fallen leaves isexported to adjacent aquatic regions mostly bytidal flush (Jacobi and Schaeffer-Novelli, 1990).The other half is used by juvenile stages as asource of food by direct grazing on leaves andindirectly by detritus consumption (Lugo andSnedaker, 1974; Thayer et al., 1987). The impor-tance of these biological and energetic processeswithin these swamps is shown by the dependenceof detritus of two thirds of the world fisheries(Lai, 1984). Increased cycling and storage bothtend to increase the ratio of indirect to directflows and contribute to network amplification andhomogenization of available energy over alltrophic levels (Patten et al., 1990). Detritus recy-cling or reutilization involves the subsequenttransformation of previously utilized but not dis-sipated energy-matter by consumers (Higashi etal., 1993).

This paradigm established by the work ofOdum and Heald (1972, 1975) in southern Flor-ida, has been subsequently modified to include

Table 7Global system properties of the mangrove ecosystem in Ce-lestun Lagoona

Attribute Value

Total system throughput 4581

Sum of all consumption 1931Sum of all respiratory flows 1040Sum of all flows into detritus 1609

Net primary production 15 550

Total primary production/total 15.9respiration

Total primary productivity/biomass 64.0

Connectance index 0.3Omnivory index 0.2

13.4% ofFinn’s cycling indexthroughput

Finn’s average path length 4.4Capacity of the system 20 803

16 665OverheadAscendency 5138

a Biomass in g m−2, flows in g m−2 per year.

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133 129

Fig. 3. Aggregation of the energy-flow web showing transfers(%) through each trophic level sensu Lindeman (1942). Flowsout of the top boxes represent exports and out of lowermiddle, the respiration (g m−2 per year). Flows originatedfrom detritus and the ones derived from primary producers arespecified.

(66%) came from primary producers (TrophicLevel I), whereas 26 and only 7% from primaryand secondary consumers, respectively.

Because most of the biomass from primaryproducers and first trophic level consumers aretransferred through predation (84 and 16%, re-spectively), they conform the trophic base for themangrove ecosystem. These same results werefound by Gadke and Srtraile (1994) in Lake Con-stanza, where the transfer of primary productionto herbivores dominates the flow of matter withinthe planktonic food web.

The relevance of the lower trophic levels in thesecondary production can be seen in the Leontief(1951) where on the basis of fluxes and trophictransfers, these groups (primary producers, micro-crustaceans) have a positive impact on almost allothers and constitute an important link betweendetritus and higher trophic levels in passing en-ergy up to the food-web (Fig. 4). A change ofbiomass or production of these basic trophicgroups will affect the other functional compo-nents by their value as food for almost all ofthem. In the same sense, the Q/B ratio for pisciv-orous and ‘other fish’ groups depend on thebiomass of the groups on which they feed (zoo-planton feeders, microcrustacean and zooplank-ton feeders).

The estimated values of some properties, suchas the ascendency and development capacity aretools to evaluate the organisation, maturity andtolerance perturbations as well as for ecosystemscomparison (Mann et al., 1989; Baird et al.,1991). According to Ulanowicz (1986) these prop-erties tend to increase with maturity and decreasein systems under natural or anthropogenicstresses. However, Christensen (1995) and Aoki(1997) stated that ascendency is not a good indi-cator of the degree of eutrophication and matura-tion, and has a negative correlation with them;suggesting that relative ascendency should becalled a relative mutual information which pro-vides a measure of the distribution of flows in asystem network in relation with the total flow(Patten, 1995). Relative ascendency (25%) and theFinn cycling index (13.4%), are lower than thosereported by Baird and Ulanowicz (1993) for fourcoastal systems in Scotland, Holland and South

alternative energy and carbon sources for con-sumers (Twilley, 1988; Robertson et al., 1992).The energy and material cycles within ecosystemsare considered an important process (Odum,1969). The complex biological, biochemical andphysical interactions determine the proportion ofthese fluxes and the efficiency with which theenergy is assimilated, transferred and dissipatedwithin the ecosystem components contributing toits autonomous behaviour (Ulanowicz, 1986).

The lower fractional trophic levels showed thatmost of them are made of juveniles whose produc-tion depend direct and indirectly on primary pro-ducers (macrophytas, phytoplankton anddetritus). The top predators (piscivorous) levelalues are low (3.6) compared with other closeecosystems where the fishery is the main predator(TL=4.2) such as Celestun Lagoon and shallowcoastal 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 ofenergy (or organic carbon) remaining after respi-ration was 1924 kcal m−2 per year higher thanthe one in Florida mangroves (Twilley, 1988).From the total fluxes to detritus, a major portion

M.E. Vega-Cendejas, F. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133130

Africa. However, the flows diversity (4.5) is verysimilar and is considered by this authors as high,meaning a mature system with a high recycledrate and low perturbations (Odum, 1969).

Mangrove ecosystem and its energetic charac-teristics are a mixture of immature and matureproperties. Between the attributes that reflect im-maturity are: (a) the relation between primaryproduction and respiration (15.9) meaning an ex-cess of production flowing to respiration; (b) highP/B ratio (64.0) for all the system; and (c) the lowratio between biomass and throughput (0.1).Moreover, high primary production (15 500 gm−2 per year) and small size of the individualsare often associated with immature systems. Onthe other side, detritus-based food webs, high fishand flow diversities are typically related to matu-rity (Table 6). The above properties suggest thatcommunities associated to mangrove are a transi-

tion between immature and mature systems char-acterised by high productivity, biomass andspecies diversity.

System recovery time, that is the time requiredfor all functional groups to return to baseline, isused as a measure of stability and is negativelycorrelated with the Finn’s cycling (Vasconcellos etal., 1997; Perez-Espana and Arreguın-Sanchez,1999). Systems with a high capacity to recycledetritus show greater ability to recover from. Inthis study, the Finn’s cycling index was high(13.4), so we can conclude that high recycling,basically detritus, is a chief positive feedbackmechanism that contributes to the maintenance ofthe ecosystem stability by preventing overshootsand destructive oscillations from external impacts.

The energy flows described here using Ecopathconstitute a preliminary approach to the knowl-edge 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 biomassof 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. Arreguın-Sanchez / Ecological Modelling 137 (2001) 119–133 131

flows to other systems through the associated fishcommunity. The merit of this model is that mostof the input data (biomass of functional groups)have been taken in the field and that fish speciestrophic structure has been determined from thestomach content analysis. However, in spite thatother values (i.e. Q/B for invertebrates) comefrom literature, we hope that this study will en-courage new investigations in this field.

Acknowledgements

We thank Luis Capurro for his valuable sugges-tions and review of an early manuscript. ToMirella Hernandez, Victor Castillo and Adrian F.Gonzales for their help so willingly in field andthe stomach contents analysis. Particularly appre-ciation is owed to CONACTY who funded thestudy (Project F467-N9109). FAS thanks Na-tional Politechnic Institute for partial supportthrough CEGEPI-9800566, COFAA and EDD.

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