Fish community structure and dynamics in a coastal hypersaline lagoon: Rio Lagartos, Yucatan, Mexico

Abstract

Rio Lagartos, a tropical coastal lagoon in northern Yucatan Peninsula of Mexico, is characterized by high salinity during most of the year (55 psu annual average). Even though the area has been designated as a wetland of international importance because of its great biodiversity, fish species composition and distribution are unknown. To determine whether the salinity gradient was influencing fish assemblages or not, fish populations were sampled seasonally by seine and trawl from 1992 to 1993 and bimonthly during 1997. We identified 81 fish species, eight of which accounted for 53.1% considering the Importance Value Index (Floridichthys polyommus, Sphoeroides testudineus, Eucinostomus argenteus, Eucinostomus gula, Fundulus majalis, Strongylura notata, Cyprinodon artifrons and Elops saurus). Species richness and density declined from the mouth to the inner zone where extreme salinity conditions are prominent (>80) and competitive interactions decreased. However, in Coloradas basin (53 average sanity) and in the inlet of the lagoon, the highest fish density and number of species were observed. Greater habitat heterogeneity and fish immigration were considered as the best explanation. Multivariate analysis found three zones distinguished by fish occurrence, abundance and distribution. Ichthyofaunal spatial differences were attributed to selective recruitment from the Gulf of Mexico due to salinity gradient and to changing climatic periods. Estuarine and euryhaline marine species are abundant, with estuarine dependent ones entering the system according to environmental preferences. This knowledge will contribute to the management of the Special Biosphere Reserve through baseline data to evaluate environmental and anthropogenic changes.

Full text

Fish community structure and dynamics in a
coastal hypersaline lagoon: Rio Lagartos, Yucatan, Mexico
Ma. Eugenia Vega-Cendejas), Mireya Herna
´ndez de Santillana
CINVESTAV-IPN, Unidad Me
´rida, Km. 6 Antig. Carr. a Progreso, A. P. 73 Cordemex, C. P. 97310 Merida, Yucata
´n, Mexico
Received 16 May 2003; accepted 9 January 2004
Abstract
Rio Lagartos, a tropical coastal lagoon in northern Yucatan Peninsula of Mexico, is characterized by high salinity during most of
the year (55 psu annual average). Even though the area has been designated as a wetland of international importance because of its
great biodiversity, fish species composition and distribution are unknown. To determine whether the salinity gradient was
influencing fish assemblages or not, fish populations were sampled seasonally by seine and trawl from 1992 to 1993 and bimonthly
during 1997. We identified 81 fish species, eight of which accounted for 53.1% considering the Importance Value Index
(Floridichthys polyommus,Sphoeroides testudineus,Eucinostomus argenteus,Eucinostomus gula,Fundulus majalis,Strongylura notata,
Cyprinodon artifrons and Elops saurus). Species richness and density declined from the mouth to the inner zone where extreme
salinity conditions are prominent (O80) and competitive interactions decreased. However, in Coloradas basin (53 average sanity)
and in the inlet of the lagoon, the highest fish density and number of species were observed. Greater habitat heterogeneity and fish
immigration were considered as the best explanation. Multivariate analysis found three zones distinguished by fish occurrence,
abundance and distribution. Ichthyofaunal spatial differences were attributed to selective recruitment from the Gulf of Mexico due
to salinity gradient and to changing climatic periods. Estuarine and euryhaline marine species are abundant, with estuarine
dependent ones entering the system according to environmental preferences. This knowledge will contribute to the management of
the Special Biosphere Reserve through baseline data to evaluate environmental and anthropogenic changes.
Ó2004 Elsevier Ltd. All rights reserved.
Keywords: fish; community structure; assemblages; hypersaline system; spatial distribution; seasonal variations; Rio Lagartos Reserve; Yucatan
Peninsula
1. Introduction
In coastal ecosystems, salinity and temperature
variation impose patterns in the temporal and spatial
distributions of their biological communities. Reid and
Wood (1976) consider that in coastal lagoons salinity
is one of the most important influences on organisms.
The magnitude and stability of salinity are conditioned
by morphology and size of the system, tides, freshwater
input, and climatic conditions. Most estuarine fishes
can tolerate salinity fluctuations, but their adaptability
and distribution vary among species, depending on
physiological tolerances, which may influence their
distributions (Blaber, 1997). Although the osmotic
abilities of fish have been extensively studied and
physiological details are available (Rankin and Jensen,
1993; Jobling, 1995), there have been relatively few
studies on subtropical and tropical species. Such work
may help to explain their distribution pattern as related
to the synergistic relationship between temperature and
salinity tolerance which determines the temperature !
salinity envelope where a species can live (Day et al.,
1989). Because of this, Blaber (1981) and Longhurst and
Pauly (1987) postulated that fishes from tropical
estuaries are better identified not as estuarine, but as
characteristic of certain environmental conditions.
There are very few hypersaline lagoons in the world
that receive freshwater and maintain a tidal connection
with the sea (Javor, 1989). Among them, Laguna Madre
Lagoons in Texas and Tamaulipas have been extensively
)Corresponding author.
E-mail address: maruvega@mda.cinvestav.mx (Ma.E. Vega-
Cendejas).
Estuarine, Coastal and Shelf Science 60 (2004) 285e299
www.elsevier.com/locate/ECSS
0272-7714/$ - see front matter Ó2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2004.01.005

studied with respect to their fishery resources (Gunter,
1967; Meza, 1980), alterations in hydrography and
subsequent changes in their biological communities
(Hedgpeth, 1967; Quammen and Onuf, 1993; Garcia-
Gil et al., 1993; Onuf, 1994; Dunton, 1996; Street et al.,
1997; Buskey et al., 1998; Sharma et al., 1999). However,
few studies have investigated fish composition and
distribution patterns along complex physicochemical
gradients (Tolan et al., 1997). In the Yucatan Peninsula,
there is a little known hypersaline estuarine system
designated as a National Wildlife Refuge and protected
by the Mexican Federal Government since 1979 due to
its natural and wildlife resources. This coastal ecosys-
tem, called Rio Lagartos, is critical for the survival of
flamingos (Phoenicopterus ruber ruber) and is a veritable
birding paradise with migratory ducks and waterfowl in
winter months, and an exceptional biodiversity, hosting
approximately 260 species of birds. Consequently, it is in
the list of Wetlands of International importance and is
a protected Special Biosphere Reserve where limited
human activities are allowed (Frazier, 1999). The area
involved is large enough to ensure maintenance of
genetic, species, habitat, and ecosystem diversity over
time (Meffe and Carroll, 1994).
Variation in salinity can be a primary factor
influencing fish distribution patterns along estuarine
gradients (Ley et al., 1999). The importance of
community-structuring mechanisms is predicated on
spatial variation in environmental stress (Layman
et al., 2000). In this study we defined environmental
stress in terms of the influence of salinity annual
variation over fish distribution pattern along the lagoon
from marine conditions in the inlet to hypersaline waters
upstream. The combination of physicochemical varia-
bles may be used to characterize fish assemblage
patterns and trends in community composition. We
think that where hypersalinity prevails, the abiotic
factors are the principal influences on fish community
structure, while as it decreases (inlet), biotic interactions
are more important.
2. Study area
Rio Lagartos is a long (80 km) and shallow (1e3m)
coastal embayment, located along the north-east of
the Yucatan Peninsula (21(26#e21(38#Nand87(30#e
88(15#W) (Contreras, 1993). Hypersalinity arises be-
cause the system lacks rivers, has a high evaporation to
precipitation rate and small connections (2) with the
Gulf of Mexico in relation to the area of the lagoon
(9562 Ha): San Felipe a natural inlet (1 km wide) and
Rio Lagartos a man made canal (0.2 km wide) (Fig. 1).
The freshwater inputs are from ground water discharges
and rainfall. Mean salinity is 57 with a horizontal
gradient from the inner zone (salinities O90 psu) to the
seaward region (33e38 psu) (Herrera and Ramı
´rez,
1997). Average annual temperature is about 26 (C, with
minimum values in January (20 (C) and maximum in
July (31 (C). The climatic regime has three seasons: dry
(MarcheJune), rainy (JulyeOctober) and windy (north-
erly) from November to February. Strong north winds
push seawater into the lagoon reducing salinity and
water temperature, while increasing both water level and
dissolved oxygen. The lagoon is divided into three
natural basins: Rio Lagartos, Las Coloradas and El
Cuyo creating a complex circulation pattern that
minimizes tidal influence (Zamacona, 1983). It is fringed
with mangrove swamps and a sand barrier and the
bottom is covered by an algae mat (Udotea flabellum and
Halimeda incrassata), an important habitat for fish and
invertebrates. Extreme hypersalinity excludes seagrasses
from much of the lagoon, but in Coloradas basin O75%
of the bottom is covered with seagrass (Halodule wrightii
and Ruppia sp.) (Herrera and Ramı
´rez, 1997). Part of
the seaward border has been modified for salt extraction
ponds (an important industry in the region).
3. Methods
3.1. Fish collections
The fish community was sampled during each season
(dry, wet and windy) from 1992 to 1993, and bimonthly
during 1997, at 28 stations distributed throughout the
lagoon. At each sampling station, water temperature
((C), salinity (using the Practical Salinity Scale), pH and
dissolved oxygen (mg l
1
) were measured with a Yellow
Springs Instrument (Model 85) as well as two replicate
net samples were taken during daylight. Net sampling
was conducted using a 30 m long seine (2 m deep, with
a2m
2
bag and 2.5 cm mesh) in shallow areas (!1.0 m),
and a shrimp trawl (3 m mouth and 2.5 cm stretch mesh)
in areas deeper than 1 m. The seine was pulled per-
pendicular to shore for a distance of 50 m, covering an
estimated area of 586.6 m
2
during each haul. Trawl
hauls lasted 10e15 min at 2e2.5 knots, and covered an
estimated area of 2880 m
2
per tow. All fishes captured
were placed in labeled bags and preserved in 15%
formalin. In the laboratory, samples were transferred to
70% ethanol and identified to the lowest possible taxon.
Individual fish was measured (mm, standard length) and
weighed (wet weight, g) to allow biomass (%B),
numerical (%N) and frequency of occurrence (%FO)
analysis.
3.2. Data analysis
Repeated-measures one-way ANOVAS were con-
ducted to determine temporal and spatial differences in
hydrographic data, fish densities and biomass after log
286 Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

transformation to stabilize variances. A Multiple Range
test was used to determine which means were signifi-
cantly different from the others (Fisher). The Kruskalle
Wallis test was used in cases where heteroscedasticity
was detected after logðxC1Þtransformation (Sokal and
Rohlf, 1998). Distinctive areas along the salinity
gradient were identified by means of cluster analysis
on averages (Centroid Method, Euclidean distances)
(Van Tongeren, 1995).
Fish community structure was analyzed temporally
and spatially by the number (N) of individuals per area,
number of species (S), and ShannoneWeaver’ species
diversity indices (Pielou, 1966). Also the ‘‘Importance
Value Index’’ (IVI) was used as a dominance measure by
incorporating information about the relative density
(RD), frequency (RF) and biomass (RB) for each
species (IV ¼RDCRFCRB) (Brower and Zar, 1977).
The value of IV may range from 0 to 3.0 (or 300%).
Dividing IV by 3 (100%) is referred to as the importance
percentage, that gives an overall estimate of the
influence or importance of a fish species in a community.
The relationship between biotic and abiotic variables
was tested by Pearson correlation coefficient (Ludwig
and Reynolds, 1988). An index of seasonal abundance
(Yan
˜ez-Arancibia et al., 1993) was used to follow
changes in dominant species and to explore the temporal
use of the system. The index was calculated as the
average catch per month divided by the highest monthly
average catch of the species multiplied by 100. Thus, the
highest monthly catch for each species had an index of
100.
Multivariate analyses were conducted to organize
species composition data into an ecologically meaning-
ful structure, and as an effective way to examine the
relationships of species distribution to environmental
conditions (Gauch, 1982). Fish abundance and the
corresponding physicalechemical data were analyzed by
ANACOM (Community Analysis Program) (De la
Cruz, 1994) and STATGRAPHICS. Normal cluster
analyses using the Bray Curtis dissimilarity index were
used on logðxC1Þtransformed fish density data to
compare spatial fluctuations of the fish community and
to define species assemblages (Van Tongeren, 1995;
Krebs, 1999). The Bray Curtis index was chosen because
it accurately reflects similarity in species composition
and abundance and gives a higher weight to more
abundant species (Bloom, 1981). Rare species (those
occurring in only one collection and with an abundance
Fig. 1. Yucatan Peninsula showing location of the Rio Lagartos Lagoon and sampling stations.
287Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

lower than 2% from total in each month) were excluded,
since they have neither a discernible distribution nor an
abundance pattern; also, their inclusion adds little
information on the community structure (Sedberry and
Carter, 1993).
Redundancy analysis (RDA), the canonical form of
Principal Component Analysis (PCA), was used to
examine interrelations between mean densities and
environmental parameters. This technique selects the
linear combination of environmental variables with the
smallest total residual sum of squares (Ter Braak, 1995).
This descriptive multivariate method both simplifies
large data sets with little loss of information and also
identifies interrelations among variables to delimit
ecoregions.
4. Results
4.1. Variations in environmental conditions
Although there were no significant differences in
water temperature, dissolved oxygen and pH values
among sites (p>0:05), distinct seasonal variations in
these hydrographic parameters were observed (Tables 1
and 2). In contrast, salinity showed a spatial gradient
along the length of the lagoon: average salinity was 54.8
and ranged from 34.8 (inlet/station 25) to 93.3 (inner
zone/station 2; Fig. 2). On a temporal basis, mean
surface water temperature was lowest in January and
highest in July (Table 1), and all months showed signi-
ficant differences (ANOVA p!0:05). Maximum oxygen
concentrations were observed in July (6.8 mg l
1
)and
from October to January (6.4 mg l
1
) when rain and
north winds increase the tides and waves, whereas in
May we registered the lowest value (1.1 mg l
1
) because
of organic matter decomposition related with a low mix-
ing rate. Salinity remained near or above 49 throughout
the study period with the highest value in March (62)
and lowest in September (49) due to rains. Cluster
analysis on salinity, indicated that the lagoon is divided
into four homogenous groups at a distance of 0.35
(Fig. 3). The first two groups are in the inner zone
characterized by hypersalinity (O70 average values). In
groups 3 and 4 salinity decreased from 67 (Coloradas
basin) to less than 36 in the marine influenced area
(stations 23e25).
4.2. Fish species composition and spatial assemblages
Although fish assemblage consisted of many species
(81), a few were dominant. Floridichthys polyommus was
the most numerous fish species (39.5%) followed by
Table 1
Mean values of hydrological parameters (Gstandard deviation in parenthesis) in Rio Lagartos by season during 1991e1993 and 1997; n: number of
measurements; *: statistically significant differences between months (p¼0:0001)
Parameters Windy Dry season Rainy season
November January February March May June July September October
Temperature ((C)* 27.2 (1.0) 20.4 (1.2) 23.2 (0.7) 26.5 (1.7) 30.0 (1.2) 30.8 (1.5) 31.4 (1.6) 30.7 (1.6) 25.4 (0.8)
Oxygen (mg l
1
)* 6.3 (1.2) 6.4 (0.4) 4.8 (1.3) 1.9 (0.6) 1.1 (0.1) 4.8 (0.9) 6.9 (1.3) 4.7 (1.3) 6.4 (2.0)
pH 7.3 (0.2) e8.4 (0.3) 7.2 (0.1) 7.6 (0.2) 8.4 (0.3) 7.1 (0.03) e8.5 (0.3)
Salinity (psu)* 57.3 (18.4) 54.7 (22.1) 52.3 (12.4) 62.3 (27.4) 54.1 (21.0) 55.8 (20.5) 54.7 (20.5) 48.6 (20.1) 53.4 (19.3)
n28 26 15 25 20 29 18 29 29
Table 2
Results of repeated-measures ANOVA and KruskalleWallis (KeW)
analysis depending on the non-normality of the data after their
transformation to test for significant differences in environmental
variables (temperature, dissolved oxygen, pH and salinity) and for
some ecological parameters of fish community (numerical abundance
and biomass per 1000 m
2
and total species) among sampling stations
(spatial), months and basins: El Cuyo, Coloradas, Rio Lagartos and
Channel from Rio Lagartos Lagoon; *: significant difference
Variable/analysis results Source of variation
Spatial (28) Monthly (9) Basins (4)
Temperature
MS/test statistic (KeW) 3.44 189.08 0.0008
F0.22 e1.6
p1.00 0.0000* 0.21
Dissolved oxygen KeWKeWKeW
Test statistic (KeW) 19.73 105.02 1.05
p0.87 0.000* 0.59
Log pH KeWKeWKeW
Test statistic (KeW) 8.18 135.16 0.11
p0.99 0.000* 0.95
Salinity ANOVA ANOVA KeW
MS 0.16 361.9 143.3
F37.95 0.84 e
p0.000* 0.57 0.000*
Log numerical abundance KeWKeW ANOVA
MS/test statistic (KeW) 31.70 54.95 1.73
Fee 4.21
p0.20 0.000* 0.007*
Log total species ANOVA ANOVA ANOVA
MS/test statistic (KeW) 48.51 0.12 0.85
F4.15 2.23 14.85
p0.000* 0.028* 0.000*
Log biomass KeWKeW ANOVA
MS/test statistic (KeW) 27.61 79.14 0.12
Fee 0.13
p0.43 0.000* 0.94
288 Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

Eucinostomus argenteus (16.2%), whereas Sphoeroides
testudineus,Fundulus majalis,Strongylura notata,F.
polyommus and E. argenteus contributed to 54% of the
total biomass (Table 3). These five species together with
Eucinostomus gula,Cyprinodon artifrons,Elops saurus
and Eugerres plumieri have importance values summing
to 58% (Fig. 4). Species number and diversity were
related to salinity zone, with the highest values found in
areas where the lowest salinities were recorded (Rio
Lagartos and Coloradas basins), while in El Cuyo with
salinities exceeding 70 and in Channel (a narrow strip),
the lowest species number and diversity were observed
(Table 4 and Fig. 5) (ANOVA on species diversity:
F-ratio ¼3:6; critical value at 5%: 0.03). In areas near
the sea, marine conditions favoured higher species
richness with an important influx of marine species to
the lagoon, while in Coloradas, the seagrass cover pro-
vides a higher habitat heterogeneity and consequently
an optimal feeding and protection area for fish species.
Fish community structure seems to be linked to
salinity, as we found significant negative correlation of
this parameter with diversity and species number (Table
5). Also the species that are abundant in the inner zone
(Elops saurus,Cyprinodon artifrons) showed a positive
correlation with salinity, while marine zone species such
as Halichoeres radiatus,Orthopristis chrysoptera,Chrio-
dorus atherinoides and Strongylura notata prefer colder
water with higher oxygen levels (marine influence zone
and north winds). Three principal groups of stations
were identified at the 0.66 dissimilarity index level
considering fish species composition and abundance
(Fig. 6). Cluster I which consisted primarily of stations
1e10 in the inner El Cuyo basin, was dominated by the
most abundant species. Euryhaline taxa (34 spp.) were
found inhabiting this area and two estuarine species
were established exclusively or most frequently there
(90e100% of all, C. artifrons and E. saurus). Total
density and species richness, measured as the number of
species per cluster, were highest in station-cluster II (41
species), which is located in Las Coloradas (stations
11e18) and Rio Lagartos basins (stations 24e28).
Typically abundant estuarine species (e.g., Fundulus
majalis,Eucinostomus argenteus,Sphoeroides testudi-
neus,Eucinostomus gula and Menidia colei) and the
marine species (Diapterus rhombeus) are representatives
of this group. Finally, channel stations in Cluster III
(stations 19e23) located within a narrow channel
subject to continuous passing of boats between outer
and inner zones, held substantially lower densities and
diversity of fish species (Table 4).
Redundancy Analysis (RDA) indicated that salinity
and oxygen were the most important physical factors
which determined the species composition and distribu-
tion of fishes (Fig. 7). The first two axes explained
18.5% of the variance and the first two specieseenviron-
ment correlations were 0.93 and 0.83. The first axis
represents a spatial gradient from the marine influence
zone to the interior of the lagoon. Most species appear
to be eurytopic and cluster near the center of the RDA
diagram (Floridichthys polyommus,Strongylura notata).
Abundances of Elops saurus and Cyprinodon artifrons
were positively correlated with salinity and temperature.
These species were found primarily in the inner zone
where the highest values for salinity and temperature
were registered. A group of about nine species had
higher abundances in the marine zone and showed
a high positive correlation with oxygen levels (Sphoer-
oides testudineus,Lutjanus griseus,Mugil curema,
Strongylura notata,Chriodorus atherinoides,Orthopristis
chrysoptera,Lagodon rhomboides,Halichoeres radiatus,
Sphyraena barracuda).
Fig. 3. Dendrogram analysis of logðxC1Þtransformed annual mean
salinity for stations in the Rio Lagartos complex by Centroid Method
(Euclidean Distance). See Fig. 1 for station location.
Sampling stations
mg/l
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
0
20
40
60
80
100
0
2
4
6
8
El
Salinity
Cuyo Las Coloradas Rio Lagartos
Channel
Fig. 2. Mean salinity (line) and dissolved oxygen (dashed line)
determined at each station during the entire sampling period. Stations
are arranged by basin from inner El Cuyo area with higher salinity
values to the Rio Lagartos inlet area.
289Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

4.3. Temporal variation in abundance
During February, June and October, the average
numerical density and biomass showed the highest
values, corresponding with the three periods of major
hydroclimatic changes: the end of the dry season, rainy
and prevailing winds seasons. In these months different
common species achieve their peak abundances.
October represented the principal period when resident
estuarine (Floridichthys polyommus,Fundulus confluents,
Lucania parva) and marine dependent species (Ariopsis
felis,Anchoa spp.) became established. Floridichthys
polyommus was the main contributor to the abundance
peak in February and gerrids and few other species
(F. polyommus,Strongylura notata,Fundulus majalis and
Lutjanus griseus) constituted 85% of total individuals in
Table 3
Percentage of total numbers (16,441) (%N) and weight (144,198.2 g) (%W) of representative fish species in Rio Lagartos Lagoon
Family Scientific name %N %W Salinity range Basin
Cyprinodontidae Floridichthys polyommus 39.54 8.22 23.0e110.0 Cu, Co, RL, Cha
Guerreidae Eucinostomus argenteus 16.21 4.56 32.0e85.0 Cu, Co, RL, Cha
Cyprinodontidae Cyprinodon artifrons 8.33 0.19 34.0e110.0 Cu, Co, RL
Belonidae Strongylura notata 4.80 8.22 24.9e110.0 Cu, Co, RL
Tetraodontidae Sphoeroides testudineus 4.75 24.17 30.0e66.7 Cu, Co, RL, Cha
Gerreidae Eucinostomus gula 4.03 2.64 23.0e98.2 Cu, Co, RL, Cha
Atherinidae Menidia colei 3.24 0.05 24.9e89.0 Cu, Co, RL
Cyprinodontidae Lucania parva 2.90 0.20 34.6e85.0 Co, RL
Guerreidae Eugerres plumieri 2.09 4.24 23.0e98.2 Cu, Co, RL, Cha
Fundulidae Fundulus majalis 1.85 9.21 36.2e90.1 Cu, Co, RL
Guerreidae Diapterus auratus 1.83 0.53 41.4e81.0 Cu, Co, RL
Sparidae Lagodon rhomboides 1.59 2.34 23.0e61.2 Co, RL, Cha
Elopidae Elops saurus 1.43 3.94 35.0e98.2 Cu, Co, RL
Guerreidae Diapterus rhombeus 0.90 0.53 36.0e80.0 Co, RL
Fundulidae Fundulus confluentus 0.68 2.34 37.3e95.6 Cu, Co, RL
Lutjanidae Lutjanus griseus 0.65 2.08 32.0e95.5 Cu, Co, RL, Cha
Ariidae Ariopsis felis 0.46 3.49 32.0e61.2 Co, RL, Cha
Fundulidae Fundulus persimilis 0.38 0.28 35.0e89.0 Cu, Co, RL
Engraulidae Anchoa mitchilli 0.34 0.01 41.4e85.0 Cu, Co, RL
Hemiramphidae Hyporhamphus unifasciatus 0.33 2.87 32.0e64.0 Co, RL
Syngnathidae Syngnathus scovelli 0.29 0.01 32.0e75.0 Co, RL
Haemulidae Orthopristis chrysoptera 0.28 0.41 23.0e82.0 Cu, Co, RL, Cha
Mugilidae Mugil curema 0.26 0.58 32.0e55.2 Co, RL
Hemiramphidae Chriodorus atherinoides 0.25 0.32 35.0e72.2 Cu, Co, RL
Gerreidae Eucinostomus melanopterus 0.24 0.27 53.4e54.1 Co
Achiridae Achirus lineatus 0.24 0.26 23.0e65.4 Cu, Co, RL, Cha
Batrachoididae Opsanus beta 0.23 0.45 24.9e85.0 Co, RL, Cha
Cyprinodontidae Garmanella pulchra 0.22 0.01 45.4e55.0 Co
Sphyraena Sphyraena barracuda 0.18 1.67 35.0e41.4 Co, RL
Mugilidae Mugil cephalus 0.13 2.24 34.0e64.0 Co, RL
Sciaenidae Cynoscion nebulosus 0.12 0.78 39.0e62.3 Co, RL
Synodontidae Synodus foetens 0.11 0.54 23.0e65.4 Cu, Co, RL
Fundulidae Fundulus grandissimus 0.06 0.19 32.0e84.0 Cu, Co, RL
Engraulidae Anchoa hepsetus 0.06 0.01 33.0e52.0 Co, RL
Diodontidae Chilomycterus schoepfi 0.05 0.34 33.0e64.0 Co, RL, Cha
Belonidae Strongylura timucu 0.05 0.16 65.0e89.0 Co
Tetraodontidae Sphoeroides spengleri 0.04 0.11 35.0e68.0 Co, RL, Cha
Sparidae Archosargus rhomboidalis 0.04 0.42 35.0e54.1 Co, RL, Cha
Syngnathidae Syngnathus pelagicus 0.03 0.001 37.7e48.0 Co, RL
Sciaenidae Pogonias cromis 0.03 0.84 72.0e86.0 Cu, Co
Belonidae Strongylura marina 0.02 0.13 55.2 Co
Urolophidae Urolophus jamaicensis 0.03 0.72 35.6e40.0 RL
Ostraciidae Lactroprhis quadricornis 0.03 0.12 32.0e38.0 RL
Haemulidae Haemulon plumieri 0.02 0.03 32.0e98.2 Cu, Co, RL
Tetraodontidae Sphoeroides nephelus 0.02 0.07 32.0e66.7 Co, RL
Gobiidae Gobiosoma bosci 0.01 0.001 41.4e55.0 Co
Haemulidae Haemulon aurolineatum 0.01 0.003 38 Co, Cha
Monacanthidae Monacanthus ciliatus 0.01 0.002 24.9e41.4 RL
Labridae Halichoeres radiatus 0.01 0.02 40.0 RL
Salinity ranges and basins where they were captured (Cu: El Cuyo, Co: Coloradas, RL: Rio Lagartos, Cha: Channel) are also indicated. Species are
listed in descending order of numerical abundance.
290 Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

June. By contrast, in November, January and March,
low abundance values were recorded with high species
richness in January and March, while in September
a low abundance is reflected in the lowest species
number (Table 6;Fig. 8).
We found a seasonal partition use of the system, with
highest fish densities occurring in El Cuyo (average
40.3 ind. 1000 m
2
) and Coloradas (32.6 ind. 1000 m
2
)
during the dry season, while the highest values occurred
in Rio Lagartos during rains (Fig. 8). High fish
abundance recorded in El Cuyo during May, was due
to high dominance of the estuarine species Cyprinodon
artifrons that withstand salinities higher than 80 (Fig. 9).
During June, Coloradas basin showed an important
abundance peak because of the contribution of Fundulus
spp. and gerreid species. In contrast in the Rio Lagartos
basin, peak abundances in July and October tended to
be associated with more diverse community structure.
However, in the Rio Lagartos basin highest species
richness occurred in the three months of lowest fish
density (September, November, January; Fig. 8). Ingress
of relatively rare juveniles of marine species such as
Haemulon aerolineatum,Urolophus jamaicensis and
Halochoeres radiatus, accounts for this pattern.
Spatial and temporal partitioning of the lagoon is
also evident for fish species grouped by ecological
categories (Fig. 10). In El Cuyo, the contribution of
resident estuarine to the assemblage is highest in the dry
season, decreases during rains and varies during the
period when north winds dominate. This estuarine
component decreases toward Coloradas basin and near
the mouth of the lagoon (Rio Lagartos), where the
euryhaline marine component in both basins is notable.
The stenohaline marine component is only seen in the
Coloradas basin at the end of the windy season, while in
Rio Lagartos it is represented throughout the year,
being more evident during rains and north winds.
Freshwater species (Cichlasoma urophthalmus) were
recorded in the dry season in Coloradas and Rio
Lagartos, where freshwater seeps are evident.
We conclude through the spatial analysis, that the en-
vironmental variation leads to dissimilarity in seasonal
species composition. In Fig. 11 the two axes explained
38.5% of the total variance and the first two speciese
environment correlations were 0.97 and 0.84. On the
positive side of axis 1 were the species with higher
abundances during the dry season (Fundulus majalis,
Fundulus confluentus,Eucinostomus gula,Lagodon rhom-
boides,Cyprinodon artifrons), or that were found
Fig. 4. Dominant fish species collected in Rio Lagartos Lagoon during
the study period, ranked by the Importance Value measure.
Table 4
Mean density (no. per 1000 m
2
) and biomass (g per 1000 m
2
) with standard deviation (in parenthesis), number of species, diversity and dominant
species of each cluster from Fig. 6
Ecological
parameters
Stations cluster
I II III
El Cuyo Las Coloradas Rio Lagartos Channel
Density 174.4 (85.1) 557.8 (243.6) 440.8 (109.8) 61.8 (71.1)
Biomass 1748.9 (1261.6) 7330.2 (7280.7) 7638.9 (2780.5) 1364.7 (704.1)
Species number 34 40 41 21
Diversity 2.6 3.8 3.5 1.7
Dominant
species (IV)
(%) from
total
F. polyommus
(16.1)
F. majalis (13.8) F. polyommus
(15.1)
F. polyommus
(29.5)
C. artifrons
(14.1)
F. polyommus
(12.2)
S. testudineus
(9.8)
S. testudineus
(14.3)
E. argenteus
(13.3)
S. testudineus
(8.2)
E. argenteus
(9.6)
M. cephalus
(12.6)
E. saurus (11.9) E. argenteus
(6.1)
E. plumieri (8.7) L. griseus (5.1)
S. notata (5.4) S. notata (7.7)
E. gula (5.1)
291Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

exclusively during this climatic period (Garmanella
pulchra,Eucinostomus melanopterus). They were posi-
tively correlated with salinity and temperature and
negatively with oxygen. Species collected during the sea-
sons of rains and north wind were located in the lower
left and right corners. In the axes extremes the species
with highest abundance for a specific climatic period
and high correlation with the corresponding environ-
mental factor were found. Diapterus auratus,Diapterus
rhombeus and Fundulus persimilis were found only dur-
ing the windy season, and were positively correlated
with oxygen and negatively with temperature. During
rains, Floridichthys polyommus,Ariopsis felis,Menidia
colei and Lucania parva were more abundant and pos-
itively correlated with pH. Low abundance species all
year round (Urolophus jamaicensis,Pogonias cromis,
Cynoscion nebulosus) were grouped in the center of the
axes, and had low correlations to salinity, temperature
and oxygen.
5. Discussion
Rio Lagartos coastal system is characterized by
hypersalinity with a positive gradient from the lagoon
mouth to the inner zone where salinity can exceed 100.
These values are higher than the ones registered in
Laguna Madre after the construction of the Waterway
(Quammen and Onuf, 1993; Street et al., 1997).
However, its tropical nature and a complex matrix of
interacting physical factors directly and indirectly de-
termine the occurrence, distribution and seasonal
movement of fish patterns (Blaber, 1997).
Low fish diversity and richness observed in saline
lakes have been considered as a response to salinity,
habitat homogeneity and associated biotic factors such
as the ability to survive in a system with few trophic
groups and decreasing competitive interactions (Alcocer
and Williams, 1993). At the lagoon inlet, where marine
conditions prevail, we found a high species richness (41)
with a low numerical abundance, whereas in Coloradas,
with salinities near 60, both numerical abundance and
species richness were high. By contrast, in hypersaline
conditions (70e110), the number of species and
abundance declined (Table 4;Fig. 5). The bottom
covered by Halodule wrightii and Ruppia sp. in
Coloradas basin increases habitat heterogeneity and
acts as a critical habitat for most of the fish species that
were found in that area looking for food and shelter.
The same ecological function has been described by
other seagrass systems (Sogard et al., 1989; Tolan et al.
1997) and mangroves (Thayer et al., 1987; Ley et al.,
1999) where year round residents tend to dominate using
the system as a nursery and feeding area.
An inverse relation between salinity and both species
richness and abundance has been discussed by Van der
Elst et al. (1976), Hammer (1986) and Williams et al.
(1990). Both species composition and abundance re-
spond to salinity changes because of osmoregulatory
stress and/or disappearance of certain food resources,
forcing certain fish taxa out of the area (Whitfield,
1999). When a low number of species exist, the
competitive interaction decreases, extending the species
ecological niche (Colburn, 1988). The elimination of
potential competitors and predators under conditions of
high salinity allows species that are able to tolerate
hypersaline conditions broader access to food and space,
compensating for the added energetic cost of accom-
modating to the physiological stress. In the marine area,
biotic factors become more important in structuring fish
assemblages as the environmental stress of high salinity
decreases (Layman et al., 2000). According to a model
of Menge and Sutherland (1987), the impact of pre-
dation on community structure will increase as physical
harshness decreases. The results of our study are
consistent with the hypothesis that abiotic factors as
environmental stressors influence the spatial patterns in
Fig. 5. Total density (bars) and species number (line) of fish by station
and salinity zone in Rio Lagartos over the entire study period.
Table 5
Correlation matrix of overall means of physicalechemical variables,
ecological parameters and fish species (only those species with at least
one significant correlation); *p!0:05
Salinity Oxygen Temperature pH
Density (no. 1000 m
2
)0.03 0.25 0.15 0.44*
Biomass (g. 1000 m
2
)0.30 0.31 0.21 0.10
Species number 0.52* 0.17 0.38 0.27
Diversity 0.40* 0.03 0.20 0.07
Elops saurus 0.61* 0.33 0.19 0.03
Cyprinodon artifrons 0.68* 0.06 0.21 0.13
Mugil curema 0.29 0.45* 0.69* 0.09
Strongylura notata 0.03 0.42* 0.40* 0.14
Chriodorus atherinoides 0.21 0.42* 0.79* 0.17
Lutjanus griseus 0.30 0.43* 0.24 0.45*
Eucinostomus gula 0.42* 0.26 0.16 0.33
Eugerres plumieri 0.41* 0.09 0.002 0.22
Haemulon plumieri 0.39* 0.13 0.65* 0.21
Orthopristis chrysoptera 0.13 0.48* 0.59* 0.07
Lagodon rhomboides 0.46* 0.40* 0.30 0.36
Halichoeres radiatus 0.20 0.48* 0.99* 0.05
Sphyraena barracuda 0.40* 0.40* 0.24 0.55*
Sphoeroides testudineus 0.70* 0.23 0.21 0.05
292 Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

fish assemblages, which adjust constantly in response to
changing seasons and salinities gradients.
This permanently open lagoon supports an abundant
and diverse fish fauna (81 species). Hedgpeth (1967)
listed 70 fish species in the hypersaline Laguna Madre of
Texas and 30 years later, Tolan et al. (1997) reported 55
species in the lower Laguna Madre. The fish fauna
included a number of species, genera, and families
common to other lagoons in the Gulf of Mexico and the
Caribbean (Yan
˜ez-Arancibia et al., 1980; Stoner, 1986;
Thayer et al., 1987; Tolan et al., 1997). In most of these
studies, gerreids and engraulids were among the
Fig. 6. Dendrogram of dissimilarity of stations based on logðxC1Þtransformed total abundance of fish species using the Bray Curtis index.
Fig. 7. Redundancy analysis (RDA) diagram of the overall fish abundances versus environmental variables represented by arrows. Species
abbreviations are the first letter of the genus name and first four letters of the species name.
293Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

dominant taxa and potentially important in the trophic
support of fishery populations (Vega-Cendejas et al.,
1994). In Laguna Madre, Texas, and tidal creeks of salt
marshes from European localities, most of the common
species are euryhaline and typically estuarine rather than
those from marine areas (Gunter, 1967; Laffaille et al.,
2000). Local variations are attributable to differences of
collecting gear and geographic variation (Kneib, 1997).
In estuaries, salinity fluctuations limit the use by the
marine fish and in hypersaline conditions, the estuarine
group does not appear to be well adapted (Whitfield,
1999). However in our study, the dominant species are
estuarine fishes of all stages (Floridichthys polyommus,
Fundulus majalis) and young marine estuarine dependent
fishes (Strongylura notata,Lutjanus griseus,Eucinosto-
mus argenteus,Eucinostomus gula). For example, L.
griseus, an important commercial species, was found in
Coloradas basin during October and November with
sizes ranging from 3 to 19 cm (Fig. 9). It means, that the
system is used as a nursery area when salinity decreases
considerably. Adults of this species reach 23 cm when
they got mature in year 3 (Starck, 1971), and 91 as
a maximum standard length (Vega-Cendejas et al., 1997;
Hoese and Moore, 1998). The gerreids (E. argenteus,E.
gula and Eugerres plumieri) represented 22% of the total
fish catch, even though they have been reported as not
well adapted for life in salinities above 35 (Renfro,
1960). Other valued fish species that are using the system
at juvenile stages are Pogonias cromis (9.3e31.0 cm
standard length), Cynoscion nebulosus (13.8e27.0 cm),
Haemulon plumieri (4.5e9.5 cm), and Haemulon auroli-
neatum (5.6 cm). Among all these, P. cromis was the
most tolerant to salinity extremes (72e86) and it
occurred primarily in Cuyo and Coloradas basins, while
H. aurolineatum was found only in Rio Lagartos basin.
Our analyses indicate that extreme variations in
salinity influenced fish distribution patterns along the
Table 6
Monthly variations of species richness (SR), density and biomass abundance (mean Gstandard deviation in parenthesis) of fish community sampled in the hypersaline lagoon from Rio Lagartos;
*p!0:05
Dry season Rainy season Windy season
March May June July September October November January February
Density 18.1 (16.5) 23.0 (33.5) 48.4 (38.7) 28.2 (46.4) 8.0* (13.1) 41.1 (62.0) 6.1* (12.2) 11.1 (10.6) 35.8 (37.0)
Biomass 172.0 (224.2) 165.7 (181.1) 1021.9* (1015.9) 262.3 (359.9) 125.8 (197.6) 449.0 (301.8) 37.6 (81.7) 111.2 (86.9) 312.5 (202.8)
SR 7.0 (3.9) 5.1 (2.8) 5.9 (2.4) 6.3 (3.0) 4.2 (3.8) 6.1 (2.7) 6.1 (4.7) 7.0 (3.2) 5.5 (2.7)
Fig. 8. Seasonal patterns in number of individuals per 1000 m
2
for
three zones (El Cuyo, Las Coloradas and Rio Lagartos) in Rio
Lagartos Lagoon. Number of fish species recorded monthly for each
basin is indicated above the corresponding column.
294 Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

salinity gradient, which may generate favourable con-
ditions for a community of suitably adapted species of
resident forage fishes but is unfavourable for most
estuarine transient juveniles. These results are consistent
with the findings of Peterson and Ross (1991) and Ley
et al. (1999). The dominant species occurred over an
extremely wide salinity range with Floridichthys poly-
ommus and Strongylura notata found in salinities from
23 to 110, Cyprinodon artifrons from 34 to 110, Elops
saurus from 34 to 99 and Fundulus majalis from 36 to 90
(Table 2). In fact, the most abundant fish in our study,
the topminnow F. polyommus has been reported in
a freshwater lake south of Tulum, Yucatan (Duggins
et al., 1983). This species ranges from the Yucatan
Peninsula south to Belize (Greenfield and Thomerson,
1997) and is equivalent to Floridichthys carpio, the
dominant taxon in the Florida Peninsula (Hoese and
Moore, 1998; Thayer et al., 1999). High salinity
tolerance gives this species an adaptative advantage
which is reflected by their high occurrence frequency
throughout the system, particularly in the hypersaline
areas where other species are absent. However, this
abiotic structuring parameter does not eliminate intense
biological interactions that may occur among species
that can tolerate the environmental stress in this area of
the lagoon (Layman et al., 2000).
Tito de Morais and Tito de Morais (1994) established
that salinity had an important influence on juvenile
recruitment and on the composition of larval and
juvenile fish assemblages in the Chayenne River estuary
(French Guyana, South America). Salinity changes
depend mainly upon the balance between freshwater
inflow and the tidal regime, with evaporation playing
a major role in lagoon or lacustrine systems having
a high surface area to volume ratio (Whitfield, 1999). In
Yucatan Peninsula, rivers are absent and all drainage is
subterranean. Weak tidal exchange with the Gulf of
Mexico, rains and freshwater springs rising through
solution channels into lagoons, known as ojos de agua,
are the only sources that decrease salinity (Reddell,
1977). The spatial salinity gradient created a physiolog-
ical barrier for most of the species; however, a seasonal
Fig. 9. Temporal variation in abundance of three dominant species:
(A) Floridichthys polyommus, (B) Lutjanus griseus, and (C) Cyprinodon
artifrons expressed as a Seasonal Abundance Index (SAI).
Fig. 10. Temporal distribution of ecological categories of the fish
community inhabiting each basis in Rio Lagartos Lagoon: estuarine,
freshwater, euryhaline (E. marine) and stenohaline marine (S. marine).
295Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

use of the system by the large fish community was
found. Similar results have been found by Yan
˜ez-
Arancibia (1981) for lagoons on the Pacific Coast of
Mexico and Lazzari et al. (1999) in salt ponds from the
Gulf of Maine. In Rio Lagartos Lagoon, we found that
fish species composition and diversity are in part due to
immigration of transient adults and juveniles during
certain months of the year when hydrological conditions
are optimal for growth. Marine species like Urolophus
jamaicensis were found exclusively in the marine
influenced zone (36.0e40.0&), but with higher abun-
dances during October when a seasonal increase in
water level produces a major influx of marine water and
species into the lagoon.
In South African estuaries, most fish species have the
ability to adapt to low and high salinity regimes.
Although fewer than 20 species have their upper
recorded limits above 69, more than 60 species can
survive in water with a salinity of 1 (Whitfield, 1998). In
Rio Lagartos, we found 32 species living in salinity
ranges above 65 and we never registered any mortality
under hypersaline conditions. Apparently they occur
when fish are trapped in an estuary that lacks freshwater
inflow for prolonged periods (Whitfield, 1999). Wallace
(1975) in St Lucia system recorded very few dead fish at
salinities between 60 and 110 and suggested that the
lower species diversity in the most hypersaline regions
was indicative of a movement towards lower salinity
areas in the south of the system. In Rio Lagartos
dominant species with broad physiological tolerances
(Floridichthys polyommus,Lucania parva,Menidia colei,
Ariopsis felis and Eucinostomus argenteus) were present
throughout the year, but they also exhibited higher
abundances in October that were likely due to a salinity
drop because of rains. On the other hand, the dry season
assemblage was low in diversity and composed of only
the most physiologically tolerant species. Throughout
March, May and June the highest salinities (110), and
temperatures (30 (C) were registered in the inner zone,
so eurytopic marine and estuarine fish like cyprinodon-
tids and gerreids were abundant. Also the freshwater
component represented by Cichlasoma urophthalmus
was present in Coloradas basin during this climatic
period. This cichlid is highly valued for its taste and has
a local importance as a food resource. Using the
terminology of Myers (1949), this secondary freshwater
fish is relatively tolerant to salinity and some species of
the same family can stand hypersalinities 100 (Albaret,
1987; Blaber, 1997). In our results, we consider that
seeps together with water level and circulation pattern,
have a great influence on the salinity gradient. During
the dry season, tides are small and water level is low
because of a high evaporation, so that salinities in the
vicinity at the seeps (38) where this species was collected
(stations 14 and 18), were below the average for the
basin during this climatic period (55). With the arrival of
the wet season, salinities fall sufficiently to allow other
species to penetrate upstream.
Fig. 11. Redundancy analysis (RDA) diagram of the overall fish abundances versus season. Arrows indicating their direction of increase represent
environmental variables, also the climatic period for each axis is specified. Species abbreviations are the first letter of the genus name and first four
letters of the species name.
296 Ma.E. Vega-Cendejas, M. Herna
´ndez de Santillana / Estuarine, Coastal and Shelf Science 60 (2004) 285e299

The times of the year when salinity decreased and
oxygen level increased coincide with the period when
highest species richness occurs (north winds). In this
climatic period, currents and hydrographic conditions
produced by the strong winds may bring juveniles into
the lagoon. In coastal systems from high latitudes, water
temperature is related to species richness (Lazzari et al.,
1999), while in tropical environments a seasonal increase
in freshwater inflow, occurring at the start of the rainy
season, may account for an increase in abundance of
euryhaline and stenohaline marine juveniles (Ley et al.,
1999). Spatial and temporal salinity variation in the
system may reduce trophic competition between species
and between stages with similar diets and consequently
favour their growth (Laffaille et al., 2000). We found
that spatial colonization varies according to seasons,
changing the peak abundance and species composition
of the fish assemblage in relation to environmental
conditions change along the salinity gradient. Such
seasonal patterns in abundance within estuaries have
been attributed to seasonal shifts in faunal composition,
immigration, emigration and trophic interactions (Day
et al., 1989). Transient Gerreidae (Eucinostomus argen-
teus) and Lutjanidae (Lutjanus griseus) were associated
with lower salinities and young juveniles occurred in
upstream habitats in the rainy and north wind seasons
when oxygen levels also increased. Similarly Florid-
ichthys polyommus was twice more abundant in the rainy
season than in the dry one. November and January had
reduced salinities with increased oxygen levels as a result
of the north winds. These hydrological characteristics
promote the influx of diverse young stages (38 and 44
species, respectively), which is reflected in the low
numerical and biomass abundances. Salinity is often
considered a good criterion for defining species assemb-
lages, but this analysis has shown that, while salinity
variation constitutes an important parameter for sorting
fish populations in the lagoon, climatic period also
influences the distribution patterns.
Management of an estuarine system requires protect-
ing critical habitats of estuarine dependent species,
including those that lie outside its physical boundaries,
and controlling both quality and quantity of water
supplies on which its water balance and chemistry
depend. Identification of these habitats and processes
requires knowing the life histories of estuarine organ-
isms and the hydrological regime, including the estuary’s
water balance. Each species has characteristic ecological
requirements and one or more types of ‘‘critical habitat’’
during different stages of its life cycle. Understanding
the function of each habitat and the relation between
them in a heterogeneous environment, specially their
effects on abundance, movement and growth of the
associated fish fauna, is essential for management of
entire ecosystems (Laffaille et al., 2000). Coastal zones
are usually managed with two main objectives:
conservation of biodiversity and intrinsic ecosystem
services, and maintenance of sustainable fisheries. A
serious problem with marine habitats is that we do not
have historic or baseline data for comparison with
present conditions to evaluate massive alterations (Day-
ton et al., 2000). Management of protected areas must
take into account factors that threaten the biological
diversity and ecological health of the park, like degrada-
tion, human use and habitat destruction (Primack, 1998).
The information provided in this paper constitutes an
important contribution to the knowledge of tropical
biodiversity and to biological databases available for
management of the fish species in Rio Lagartos Bio-
sphere Reserve. This information will be of assistance for
future conflict resolution among fisherman, industry, and
ecotourism. It is important to realize that these human
activities may reduce productive habitat, estuarine water
quality, production of organic detritus, and feeding and
nursery habitats of fishery species.
Acknowledgements
The authors would like to thank the many persons
from CINVESTAV-IPN whose efforts in support of this
research were of great value, in particular to Gustavo de
la Cruz for his help in the first part of the work and to
Uriel Ordon
˜ez, Victor Castillo, Fanny Merino, and
Javier Hiroshe for their assistance in the field. We also
want to express our gratitude to Dr. Luis Capurro for
revision of the manuscript with his valuable suggestions
and the anonymous reviewers whose comments im-
proved and enriched this manuscript. Also thanks to
CONACYT-SISIERRA which provided the financial
support for the completion of the study and to the
Directorate of the Reserve for its help during the study.
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