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Estuarine, Coastal and Shelf Science 76 (2008) 418e430

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Water quality variability and eutrophic trends in karstic tropical

coastal lagoons of the Yucatán Peninsula
Fedro U. Tapia González, Jorge A. Herrera-Silveira*, Maria L. Aguirre-Macedo
Departamento de Recursos del Mar, CINVESTAV-IPN, Unidad Mérida, Carretera Antigua a Progreso km. 6,
Mérida, Yucatán C.P. 97310, Mexico
Received 27 April 2006; accepted 19 July 2007
Available online 15 August 2007

Abstract

Coastal lagoon ecosystems are particularly vulnerable to eutrophication due to often restricted water exchange with the adjacent ocean, lead-
ing to an accumulation of nutrients from the surrounding watershed. The coastal areas of the northern Yucatán (SE Mexico) show similar geo-
logical characteristics: carbonate soils, and strong groundwater discharges (SGD), which are a source of fresh water and dissolved inorganic
nutrients. However, due to differences in land use and human impact, these coastal lagoons have different water quality characteristics. To de-
termine the variables and processes that influence water quality and eutrophic status of these tropical coastal lagoons with different hydrological
regimes and human impacts, bimonthly samplings were carried for a year at 11 stations in Celestún and Chelem lagoons. The results indicate
that Celestún is influenced by bioturbation (resuspension and nutrients inputs from waterfowl) and SGD with high concentrations of nitrate and
silicate, leading to oligo-mesotrophic conditions. Chelem had high ammonium and phosphate concentrations, reflecting impacts by wastewaters
from the surrounding urban area, resulting in meso-eutrophic conditions. Forcing functions such as climatic patterns, water residence time and
local aquifer pollution are probably the main variables that explain the observed patterns.
Ó 2007 Elsevier Ltd. All rights reserved.

Keywords: water quality; eutrophication; tropical coastal lagoons; karst; submarine groundwater

1. Introduction and estuaries, submarine groundwater discharge (SGD)

Coastal ecosystems of karst regions are particularly vulner-
able to eutrophication because freshwater enters these areas
via groundwater which is highly susceptible to pollution
from urban and industrial wastewater, septic tanks, and open
sanitary landfills (Fetter, 1994). Eutrophication of coastal wa-
ters can have a number of adverse impacts on ecosystems, in-
cluding algal growth, hypoxia, and substantial loss of marine
life and habitat (De Jonge et al., 2002). Traditionally, studies
on coastal eutrophication have focused on point sources of nu-
trients, such as rivers and wastewater treatment plants (Ri-
chardson and Jorgensen, 1996). However, in coastal lagoons
* Corresponding author.
E-mail address: jherrera@mda.cinvestav.mx (J.A. Herrera-Silveira).
contaminated by urban or agricultural wastes are a source of
contaminants that can impact these ecosystems.
Nutrients entering via SGD have been shown to be a factor in
algal growth dynamics (Johannes, 1980; Sewell, 1982; Kinney
and Roman, 1998), harmful algal blooms (LaRoche et al., 1997;
Gobler and Sa~nudo-Wilhemy, 2001), and hydrological modifica-
tion of these ecosystems (Valiela et al., 1992; Short and Burdick,
1996; McClelland et al., 1997). Water filtration to the aquifer is
enhanced in karst coastal areas, as observed in the water quality
of coastal springs carrying nutrients from human activities. Nitro-
gen has been particularly important among these nutrients, be-
cause it is considered a limiting nutrient for primary production
in marine ecosystems (Nixon and Pilson, 1983; Borum, 1996).
However, in karst areas, phosphorus is generally the limiting
element due to its affinity to calcium carbonate and its rapid pre-
cipitation in the form of apatite (Fourqurean et al., 1993).

0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2007.07.025
 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430
Coastal development, including urbanization, intensive ag-
riculture, aquaculture, and coastal engineering such as artifi-
cial inlets, promotes some undesirable changes in lagoon
systems. These problems are increasing in developing coun-
tries that, lacking the appropriate technology for the imple-
mentation of wastewater treatment systems, promote an
increase in nutrients discharges to the coastal ecosystems, gen-
erating eutrophication conditions.
Given the explosive population growth in the Yucatán Pen-
insula (SE, Mexico), its karst soil, and the increment in urban
development and industrial and tourism activities, among
others, it is urgent to determine the water quality condition
and eutrophic status of the coastal ecosystems, since the lack
of wastewater treatment systems puts the ecological stability
and environmental services of these ecosystems at risk. The
aim of this study was to determine the water quality conditions
and eutrophic status of two coastal lagoons located in the same
region, with different hydrological regimes and human impact,
in order to advance in the understanding of the processes that
promote eutrophication in karstic tropical coastal lagoons.
2. Study area
The Celestún and Chelem coastal lagoons are located
northeast and north of Mérida, capital city of the state of
Yucatán (SE Mexico) (Fig. 1). Both have similar geological
characteristics in terms of morphology and depth of <1 m to
3 m. Celestún is located in a National Protected Area in the
northwest part of the Peninsula (20 450 and 20 580 ; 90 150
and 90 250 ). It has a total area of 28.1 km2 and is 22.5 km
U. S. A.
Gulf of Mexico
Caribbean
Fig. 1. Location of Celestún and Chelem lagoons, indicating sampling stations.
419
in length. Connection with the sea occurs via a 410 m wide in-
let at the southern end. It is surrounded by healthy mangrove
swamps. The hydrology is characterized by an estuarine salin-
ity gradient due to numerous springs located mainly in its in-
ner area (Herrera-Silveira, 1994). The main human activities
are fishing and tourism. Chelem lagoon is located in the north-
west zone of the Peninsula (21 150 and 21 170 ;89 390 and
89 480 ), covering a total area of 13.6 km2. It is connected to
the sea through an artificial inlet (100 m wide) in its central
portion. There is urban development and industrial facilities
for the region’s major fishing harbor (Yucalpeten) on its north-
ern border. Its southern border is a mangrove area impacted by
hydrological changes induced by the artificial inlet of the
Yucalpeten harbor (Herrera-Silveira et al., 2000).
There are three climate seasons: rainy, dry and ‘‘nortes’’.
The rainy season (July to October) has 400e700 mm of pre-
cipitation and high air temperatures (30e35  C). The ‘‘nortes’’
(November to February) is characterized by the influence of
cold fronts accompanied by strong winds (80 km h1), low
air temperatures (20e23  C) and scarce rainfall (<50 mm).
The dry season (March to June) is characterized by low rain-
fall (0e100 mm) and high air temperatures (36e40  C) pro-
moting high rates of evaporation (Herrera-Silveira, 1994).
Table 1 includes a description of the different land uses and
main hydrological characteristics of each lagoon.
3. Materials and methods
Eleven stations were sampled at each lagoon twice during
each season, between August 2001 and June 2002. In each
Gulf of Mexico
Chelem
Celestun Caribbean
Sea
Yucatan
Peninsula
420 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430

Table 1
Hydrobiological characteristics and land uses of the coastal lagoon Celestún and Chelem (SE, México). t, residence time of water. Range calculated according to
LOICZ model (Smith et al., 1999)
Lagoon Characteristic
Surface (km2) t (days) Salinity Population (inhabitants) Land uses Environmental impacts
Celestún 28 3e150 5e38 6065 Nature conservancy Stability of water flows and quality, sea and air
storm protection and improved biological productivity
(e.g. fisheries)
Integrated tourism Increasing evaluation of natural resources and territory
Food harvesting Weak habitat disturbance
Chelem 14 3e200 28e44 48798 Conventional road construction Loss of mangrove and sand dune habitats and water
flow disturbances
Industrial harbor Waste water and solid discharges and coastal transport
disturbances
Unregulated housing Beach erosion and loss sand dune habitat
Massive tourism Loss habitats, point source pollution, increased storm
hazards and water flow disturbances

station, in situ temperature ( C), salinity and dissolved oxygen
(mg L1) were measured with an YSI-85 multiprobe. Due
to the lack of water column stratification in both lagoons
(Herrera-Silveira et al., 1998), surface samples were collected
with a Dataflow IV system (Madden and Day, 1992). The sam-
pled water was stored and refrigerated at 4  C for later labora-
tory analysis. All samples were collected between 08:00 and
12:00 h, local time. Water quality analysis included ammo-
nium (NH4) using the phenol-hypochlorite method (Solórzano,
1972), nitrite (NO2) with the sulfanilamide method, and reduc-
tion of nitrate (NO3) to nitrite using a cadmiumecopper col-
umn. Phosphorus, as soluble reactive phosphorus (SRP), was
measured with the mixture of reagents technique (Solórzano
and Sharp, 1980), and soluble reactive silica (SRSi) was mea-
sured using the blue-molybdenum method (Strickland and
Parsons, 1972). Chlorophyll a (Chl-a) was determined by
filtering 250 ml of water through a Millipore membrane filter
(0.45 mm). Pigments were extracted with 90% acetone and
calculated using the equations of Jeffry and Humphrey (1975)
using a spectrophotometer wavelength scale.
3.1. Data analysis
With the objective of evaluating significant differences be-
tween the lagoons for all water quality variables, data were an-
alyzed using a one-way non-parametric ANOVA, with the
lagoons and seasons as main factors (Zar, 1997) (Table 2).
Several multivariate classification and ordination analytical
tools were used to extract, interpret or reveal structures that
otherwise would be overlooked or misinterpreted (Green and
Vascotto, 1978). A Principal Component Analysis was per-
formed to extract the main variables that explained the hydro-
logical behavior of each lagoon. This analysis was chosen
because it reduces the dimensions of the data matrix by pro-
ducing a small number of abstract variables, which are linear
combinations of the original variables. The results are dis-
played in a two-dimensional plot that uses the components
as axes (James and McCulloch, 1990).
As coastal lagoons often show environmental gradients,
a classification analysis was performed to distinguish areas
with similar water quality conditions, by placing the objects

Table 2
Average values of water quality variables calculated annual and seasonally in Celestún and Chelem lagoons. *Significant differences S.D. ( p < 0.05, one way
ANOVA). % Contribution: Contributions of each variable to the dissimilarity between lagoons. þMost important
Season Lagoon Temp.( C) Salinity D.O NO2 NO3 NH4 SRP SRSi Chl-a
(mg L1) (mM) (mM) (mM) (mM) (mM) (mg m3)
Annual Celestún 29.4 21.3 4.8 3.9 9.6 7.0 0.5 154.5 6.3
Chelem 29.8 33.9 3.9 2.4 9.5 13.5 0.7 41.5 4.1
S.D. O Lagoons * * * * * * *
Rainy Celestún 31.9 22.5 4.5 0.8 5.2 6.4 0.7 112.1 6.1
Chelem 30.9 33.2 3.2 1.5 7.6 10.6 0.6 47.5 2.8
S.D. O Lagoons * * * *
Nortes Celestún 25.6 17.0 6.3 5.8 15.3 2.5 0.4 236.4 7.4
Chelem 26.1 32.7 3.7 2.9 12.2 21.2 0.4 39.8 4.5
S.D. O Lagoons * * * * * * *
Dry Celestún 30.9 24.3 3.5 5.1 8.2 12.1 0.6 114.9 5.5
Chelem 32.5 35.8 4.8 2.9 8.7 8.7 1.1 37.2 5.0
S.D. O Lagoons * * * * * *
SIMPER % Contribution 9.53 14.81þ 10.48 8.72 10.03 9.84 11.62þ 13.31þ 11.62þ
 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430
(in this study, the sampling sites of each lagoon) in groups,
first by the similarity measure (Euclidian distance), and then
by the grouping algorithm (furthest neighbor) (Legendre and
Legendre, 1998).
To investigate if the lagoons were similar regarding their
water quality characteristics, a non-metric multidimensional
scaling (MDS) was carried out with standardized log-
transformed data to produce a two-dimensional ordination
plot of the similarities among the stations of each locality. Sig-
nificant differences between lagoons were determined using
a one-way analysis of similarities test (ANOSIM) (Clarke,
1993). This test assesses significant differences between
groups of replicates against a series of random simulations,
resulting in the calculation of a test statistic (R). The test sta-
tistic R will be close to 0 when no differences between data
sets are apparent, and will increase to a maximum of 1 as
data matrix of both lagoons become dissimilar. As a comple-
ment, in order to explore the variables that most contribute to
the observed differences between lagoons, the SIMPER
procedure was applied. This procedure analyzes similarity/
dissimilarity between pairs or groups of samples and calcu-
lates the contribution of each water quality variable to that
similarity/dissimilarity. This information indicates which
water characteristics are most important in terms of the ob-
served differences between samples or, in our case, between
lagoons. The MDS, ANOSIM and SIMPER analyses were
performed using the PRIMER software package developed
at the Plymouth Marine Laboratory (Clarke and Warwick,
1994).
3.2. Eutrophic status
The sampling sites of each lagoon are enriched with nutri-
ents from natural and anthropogenic sources; therefore, to
evaluate water quality in this context in both lagoons, it was
necessary to use an indicator, the Trophic Index (TI), for
each nutrient and Chl-a. This non-dimensional index was
designed to work in a specific manner for each nutrient,
with application for several types of waters; it is sensitive to
eutrophication stress and simple data is obtained from the cal-
culations (Karydis et al., 1983).
Trophic Index (TI) calculations were performed with data
grouped by zones according to the Classification Analysis
(Fig. 6).
C ally, seasonally and between lagoons (Table 2).
TI ¼ þ log A
C  logx
where C is the log of the total nutrient load, x is the nutrient
total concentration in a certain station, and A is the number
of stations. The TI generates a continuous evaluation of the
water quality and gives a value for the degree eutrophication.
The scale is: oligotrophic <3; oligo-mesotrophic >3 < 3.5;
mesotrophic >3.5 < 4.5; meso-eutrophic >4.5 < 5; and eutro-
phic >5. The variability and the differences between areas and
times were represented in box-and-whiskers diagrams of sev-
eral water quality variables. In these diagrams, the horizontal
421
line of each box corresponds to the median, and the mean is
symbolized by a cross. The upper and lower portions of
each box represent the 25th and 75th percentiles, while the
ends of the bars are the 5th and 95th percentiles. The lateral
notch in the boxes corresponds to 95% confidence interval
for the median, therefore, when the notches are overlapped,
it is assumed that the medians do not show significant differ-
ences among treatments (Zar, 1997).
4. Results
4.1. Spatial and temporal variation of water quality
conditions
The average values of water quality characteristics in both
lagoons are presented in Table 2. The variance analysis
showed significant differences ( p > 0.05) between the two la-
goons and among the different seasons.
Water temperature behavior was related to the seasonal pat-
tern. In Celestún, the highest mean temperature was 33.4  C
during the dry season (June, station 11), while the lowest
(24.6  C) was during the ‘‘nortes’’ period (December, station
1). In Chelem, the highest mean temperature occurred during
the dry season (36.1  C, April, station 6), and the lowest dur-
ing nortes (25.5  C, December, station 1) (Fig. 2a and b). The
ANOVA showed significant differences ( p < 0.05) between
nortes and dry seasons, and between lagoons (Table 2).
Salinity showed an estuarine gradient in Celestún (mean
salinity range was 13e27), while Chelem was marine (mean
salinity range was 31e36) (Fig. 2c). The highest mean value
in Celestún occurred during the dry season (27.2, June, station
11), and the lowest during the rainy season (13.6 October,
station 1). In Chelem, a similar pattern was observed of high av-
erage salinity during dry season (36.2, April, station 1), and low
values during rainy season (31.5, October, station 3) (Fig. 2d).
The ANOVA showed significant differences ( p < 0.05) annu-
ally, seasonally and between lagoons (Table 2).
Dissolved oxygen showed a slight state of hypoxia
(<2 mg L1) in station 1 of Chelem; however, the mean values
(Table 2) indicate general healthy conditions of the water col-
umn. Both lagoons showed similar season patterns with the
highest average during nortes season (>6.5 mg L1) while
the lowest was registered during dry season (<3 mg L1).
The ANOVA showed significant differences ( p < 0.05) annu-
Annual mean NO2 was greater in Celestún than in Chelem
(Table 1). In Celestún, the highest NO2 concentrations was
registered during the rainy season (9.9 mM, October, station 5),
and the lowest during the dry season (0.3 mM, June, station 11).
In Chelem, the highest mean value was registered during the
nortes period (4 mM, February, station 2), and the lowest during
the dry season (1 mM, June, station 10) (Fig. 3a and b). The
ANOVA showed no significant differences ( p < 0.05) during
the rainy season between lagoons.
The annual mean NO3 concentrations were similar in both
lagoons (Table 2), and showed the same temporal pattern with
422 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430

CE CH CE CH
(a) (b)
36
36
34

Temperature, ºC
Temperature, ºC
34
32 32

30 30

28 28

26 26

24 24
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

(c) CE CH (d) CE CH
40

40

30
Salinity

30

20 Salinity 20

10 10
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

CE CH CE CH
(e) 8 (f) 8

6 6
D.O, mg/l

D.O, mg/l

4 4

2 2

0 0
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

Fig. 2. Spatial and temporal variation of mean concentration of temperature (a,b), salinity (c,d) and dissolved oxygen (e,f), in Celestún (CE) and Chelem (CH)
lagoons.

high mean concentration during nortes (>12 mM, December),
and the lowest during the dry season (1.4 mM Celestún;
4.3 mM Chelem). The ANOVA showed no significant differ-
ences ( p < 0.05) (Fig. 3c and d), neither annually nor season-
ally, between lagoons (Table 2).
The annual mean NH4 concentration was different between
lagoons (Table 2). In Celestún, the highest average value oc-
curred during the nortes period (15.1 mM, February, stations
1 and 2), while the lowest occurred during the rainy season
(1 mM, October, station 11). In Chelem, the highest mean
value was observed during the rainy season (21.5 mM, Octo-
ber, station 1), while the lowest during the dry season
(4.5 mM, June, station 8) (Fig. 3e and f). The ANOVA showed
significant differences ( p < 0.05), annually, during the nortes
season and between lagoons.
Although mean annual SRP was similar between lagoons
(Table 2), the high values in Chelem during late nortes and
early dry season yielded significant differences between la-
goons ( p < 0.05). In Celestún, the highest mean annual SRP
occurred during the dry season (0.9 mM, June, station 8), while
the lowest was observed during the rainy season in both la-
goons (>0.4 mM, October). In Chelem, the highest average
concentration was observed during nortes (1.2 mM, February,
station 7) (Fig. 4a and b). The ANOVA showed annual signif-
icant differences ( p < 0.05).
The annual mean concentration of SRSi was different be-
tween lagoons (Table 2); however, there were similar seasonal
patterns of high values during rainy season (335.9 mM Celes-
tún; 58.8 mM Chelem) and lower in the dry season (69.8 mM
Celestún; 18.9 mM Chelem) (Fig. 4c and d). In both cases,
 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430 423

(a) CE CH (b) CE CH
12 12

10 10
Nitrites, µM

Nitrites, µM
8 8

6 6

4 4

2 2

0 0
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

(c) CE CH (d) CE CH
25 25

20 20
Nitrates, µM

Nitrates, µM
15 15

10 10

5 5

0 0
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

(e) 35 CE CH (f) CE CH
35

30 30
Ammonium, µM

Ammonium, µM

25 25

20 20

15 15

10 10

5 5

0 0
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

Fig. 3. Spatial and temporal variation of mean concentration of nitrites (a,b), nitrates (c,d) and ammonium (e,f), in Celestún and Chelem lagoons.

a decrease in SRSi concentrations was related to major marine
water influence during the dry period. The ANOVA showed
significant differences ( p < 0.05) both annually and season-
ally between lagoons (Table 2).
Chlorophyll a showed higher mean concentrations in Celes-
tún than in Chelem (Table 2). In both lagoons the highest
average were registered during nortes period (Celestún
9.1 mg m3, Chelem 7.4 mg m3), and the lowest during the
dry season (Celestún 6.5 mg m3, Chelem 2.8 mg m3).
(Fig. 4e and f). Significant differences were observed annually,
during rainy and nortes period. (Table 2).
4.2. Pattern analysis
An ordination analysis was performed with all water qual-
ity variables measured; due to the different nature of data,
these were log-transformed and standardized before the analy-
sis (Zar, 1997).
In Celestún, the first two components explained 62.3% of
the hydrological variability (Fig. 5a). Component I was associ-
ated with SRSi, temperature and salinity, suggesting a rela-
tionship with SGD from springs. Component II was associated
with Chl-a and dissolved oxygen, and may be related to produc-
tion-consumption processes.
In Chelem, the first two components explained 60.6% of
the hydrological variability (Fig. 5b). Component I was asso-
ciated with SRSi and inorganic nitrogen (NO3 and NH4), indi-
cating a relationship with polluted ground water discharges.
Component II was associated with dissolved oxygen and
Chl-a, and likely represent eutrophic symptoms.
Classification analysis shows that both lagoons are divided
into three zones (Fig. 6). In Celestún, the first zone includes
424 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430

CE CH CE CH
(a) 1.4 (b) 1.4

1.2 1.2

1.0 1.0
SRP, µM

SRP, µM
0.8 0.8

0.6 0.6

0.4 0.4

0.2 0.2
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

(c) 400 CE CH (d) CE CH

400

300 300
SRSi, µM

SRSi, µM
200 200

100 100

0 0
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

(e) CE CH (f) CE CH
12 12

10 10
Chl-a, mg/m3

Chl-a, mg/m3

8 8

6 6

4 4

2 2

0 0
1 2 3 4 5 6 7 8 9 10 11 A O D F A J
Station Month

Fig. 4. Spatial and temporal variation of mean concentration of soluble reactive phosphorus (SRP) (a,b), soluble reactive silica (SRSi) (c,d) and chlorophyll-a
(Chl-a) (e,f) in Celestún and Chelem lagoons.

stations 1, 2, 3 and 4, and is called the inner zone (IZ); the sec-
ond zone includes stations 5, 6, 7 and 8, called the mixing
zone (MZ); the third group included stations 9 and 10, corre-
sponding to the marine zone (SZ). Station 11 belongs to this
last group, although with low similarity, and could be a marine
reference station (Fig. 6a).
At Chelem, the inner zone (IZ) is formed by stations 1,
2, 3 and 4. This area has been modified as a canoeing trail
and show higher differences than the other zones. The mix-
ing zone (MZ) includes stations 5 and 6, while the area to-
ward the inlet, grouping stations 7, 8, 9 and 10, is the
harbor zone (HZ). As in Celestún, station 11 has high salin-
ity and as a consequence low similarity with other stations
and could be considered a marine reference location
(Fig. 6b).
The two-dimensional plot from the non-metric multidimen-
sional scaling (MDS) using the hydrological matrix of Celes-
tún and Chelem (Fig. 7), showed that the sampling stations of
each site are quite different. The ANOSIM test showed that
the water quality pattern of both areas differ significantly
(global R ¼ 0.577; p < 0.001). The exploratory analysis (SIM-
PER) indicated that salinity, SRSi, Chl-a and SRP were vari-
ables that contributed most to the differences between
lagoons (Table 2), suggesting that Chelem is impacted by cul-
tural eutrophication.
4.3. Eutrophic status
The trophic index (TI) regarding NO2 and NO3 showed dif-
ferent behavior in each lagoon. In Celestún, the MZ was
 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430 425

(a) 0.8
chemical characteristics, and perhaps physical processes
such as water residence time, are factors that play an impor-
0.6
NO2 tant role in promoting changes in the trophic status. Human
Component II (22%)

0.4 NH4
SRSi
SRP impacts and SGD have been recognized as sources of nutri-
0.2 Temp ents in shallow coastal ecosystems (Gobler and Boneillo,
0 2003), promoting space-time variations in water quality
-0.2 NO3 characteristics.
-0.4 D.O Sal In Celestún, SGD are important controllers of hydrological
Chl-a dynamics, inducing an estuarine salinity gradient. SGD is
-0.6
a source of silica and nitrate and thus plays an important
-0.8 role in the water quality of these lagoons (Herrera-Silveira,
-0.6 -0.4 -0.2 0 0.2 0.4 0.6
1994). Nitrate and silicate show peaks in Celestún in the inner
Component I (39%)
zone. In Chelem, the salt/fresh water balance promotes the la-
(b) 0.8 goon’s marine condition (Herrera-Silveira et al., 1998). How-
D.O ever, high ammonium, nitrate and SRP show that SGD is the
0.6 Chl-a
main source of nutrients to the system, suggesting that the
Component II (20%)

0.4 NO2 SRP

aquifer is polluted with municipal wastewaters because there
0.2 SRSi Sal
NO3
is no centralized wastewater treatment. Septic tanks provide
0 the only means of sewage treatment and these discharge di-
NH4 Temp rectly into the groundwater. A number of studies have shown
-0.2

-0.4
that septic tanks lead to pollution of groundwater and impair-
ment of water quality in coastal ecosystems (Persky, 1986; Gi-
-0.6
blin and Gaines, 1990; Valiela et al., 1992; LaRoche et al.,
-0.8
1997; Corbett et al., 2000).
-0.6 -0.4 -0.2 0 0.2 0.4 0.6
Celestún and Chelem have water quality variations on rel-
Component I (40%)
atively and spatial scales, and different behaviors in spite of
Fig. 5. Two-dimensional plot of water quality from the two Principal Compo- being in the same marine-coastal region, suggesting that local
nents of the PCA. (a) Celestún Lagoon; (b) Chelem Lagoon. forcing functions control this variability, and probably their
vulnerability to eutrophication.
mesotrophic while the IZ and the SZ were oligotrophic. In
Spatially, the gradients observed in each lagoon are related to
Chelem, a spatial gradient was observed from higher to lower
the balance of fresh/marine water inputs and the physical and
TI, from the IZ toward the HZ. Celestún was oligotrophic for
chemical characteristics of the groundwater. Biogeochemical
NO2 and oligo-mesotrophic for NO3, while Chelem lagoon
processes such as productivity, organic matter decomposition,
was mesotrophic for both nutrients (Fig. 8a and b).
and nitrification/denitrification in specific locations of each
In relation to NH4, the TI followed the same spatial pattern
system, which are related to water residence time, are also
in both lagoons, from higher to lower TI, going from the inner
important factors affecting water quality (Medina-Gómez and
area to the sea in each system (Fig. 8c). In Celestún, average
Herrera-Silveira, 2003).
TI was oligo-mesotrophic, while in Chelem it was mesotro-
The estuarine salinity gradient in Celestún results from
phic, with significant differences among areas.
freshwater springs in the inner area and strong mixing be-
For SRP, the TI in both lagoons was oligotrophic, without
tween middle and marine areas. Chelem is more marine, al-
significant differences among the areas of each lagoon. The
though the inner area (stations 1, 2, 3 and 4) receives SGD.
highest variability in Celestún occurred in the marine zone
However, high water residence time results in evaporation
(MZ), while in Chelem it was in the inner zone (IZ) (Fig. 8d).
and elevated salinity due to restricted water interchange
With respect to SRSi, the TI had similar spatial patterns in
with the middle zone (stations 5 and 6) due to the
both lagoons, higher in the inner areas and lower toward the
Mérida-Progreso highway (Valdés, 1999). Moreover, this
inlet of each lagoon. Variability among zones in each lagoon
condition can promote low dissolved oxygen concentrations
showed significant differences (Fig. 8e). TI average condition
in the inner zone, suggesting symptoms of eutrophication.
for this nutrient was mesotrophic in both lagoons.
Water circulation and residence times in coastal lagoons
Regarding Chl-a, Celestún was, on average, mesotrophic,
are dominated by tide cycles, morphology and fresh water
with significant differences between the SZ and the MZ. In Che-
inputs, and thus, structures that modify water flow, or those
lem, the TI average for Chl-a was oligo-mesotrophic and no sig-
affecting fresh/marine water balance, have been demon-
nificant differences were observed among areas (Fig. 8f).
strated to have effects on the hydrodynamics in these types
of ecosystems, impacting their water quality (Gomez et al.,
5. Discussion 1998; Arhonditsis et al., 2000). Furthermore, eutrophication
processes in these kinds of tropical karst systems are in-
The differences observed in water quality between Celes- duced through local forcing functions such as nutrient loads
tún and Chelem lagoons indicate that local SGD and from SGD and longer water residence times. Thus, the inner
426 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430

MZ
SZ

6 IZ
Disimilitud

0
1 2 3 4 5 6 7 8 9 10 11
Stations

IZ

HZ MZ 6
5
Disimilitud

4
3
2
1
0
1 2 3 4 5 6 7 8 9 10 11
Stations

Fig. 6. Zonation of (a) Celestún Lagoon and (b) Chelem Lagoon from Classification analysis (clusters) according to water quality variables.

zones of both lagoons and the harbor of Chelem show vul-
nerability to eutrophication.
Nutrient inputs from SGD with little surface drainage to the
costal ecosystems of the Yucatán Peninsula, could stimulate
aquatic production, heterotrophic activity and oxygen con-
sumption in the water column. These, in turn, can lead to un-
healthy ecosystem conditions as has been reported for other
coastal areas (Boynton et al., 1982; Malone et al., 1986; Ver-
ity, 1987; Kemp and Boynton, 1992; Malone, 1992; Patrıcio
et al., 2004; Xu et al., 2005).
Seasonally, the changes in water quality of each lagoon are
related to nutrient inputs that stimulate productivity, organic
decomposition, and sediment resuspension, resulting from
the mixed temperature conditions, rainfall, and winds that pre-
vail in each season. These forcing functions play an important
role in the residence time of water as demonstrated by
Herrera-Silveira et al. (1999) who used the LOICZ model
approach.
During dry seasons, high air and water temperatures, low
rainfall and reduced wind speed promote environmental stabil-
ity stimulating organic matter decomposition reflected in high
concentrations of SRP and NH4. During the rainy season, fresh
water inputs from the aquifer to coastal ecosystems increases,
resulting in reduced salinity and high concentrations of nutri-
ents, mainly NO3 and SRSi that stimulate phytoplankton bio-
mass. During the nortes season, there is continued aquifer
discharge, as reflected by the high nutrient concentrations.
Also, during this season, low air and water column tempera-
tures, and high wind speeds, promote sediment resuspension
and high water residence time (Herrera-Silveira and Comı́n,
1995). Similar spatial and seasonal patterns have been
observed in Dzilam lagoon, although this system is considered
to have relative pristine conditions (Medina-Gómez and Herrera-
Silveira, 2003).
In Celestún, high nitrite, nitrate and silicate concentrations
during the rainy season are related to SGD. While in Chelem,
 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430
2D Stress: 0.08
CH-I CH-I
CH-I
CE-I CE-I CH-M
CE-I CE-I
CE-M
CE-M CE-S
CH-M
CE-S
CE-M
CE-S CH-M
CH-H
CH-H
CE-S CH-H
CH-H
Fig. 7. MDS two-dimensional ordination plots. Celestún: inner zone (B CE-
I), mixing zone (: CE-M), sea zone (- CE-S). Chelem: inner zone (A CH-
I), mixing zone (, CH-M), sea harbor (* CH-H).
high nitrites, nitrates and ammonium, mainly in the inner area,
could be related to high water residence time and SGD pol-
luted with municipal wastewaters, as indicated by high fecal
coliformes (Tapia-González, 2003).
In both lagoons, the highest Chl-a concentrations occurred
during the nortes season, probably due to nutrient concentra-
tions and microphytobenthos resuspended by turbulence in
these shallow ecosystems. In coastal lagoons, the processes
of controlling phytoplankton abundance are very complex,
and are associated with nutrient inputs and turbulence induced
by winds and tides (Cloern, 1996).
Ordination multivariate analysis provided a better view of
the hydrological complexity and water quality of these la-
goons through the definition of key variables. These are di-
rectly related with SGD, although their relative contributions
are not the same.
In Celestún, the key variables indicate a strong saline gra-
dient and contributions of SRSi (Component I), as well as
a balance among the production, consumption and remineral-
ization processes reflected in dissolved oxygen and Chl-a (as
key variables in the Component II).
In Chelem, ammonium is a key variable (Component I),
and has been related to remineralization and wastewater dis-
charges (Liebeziet et al., 1980). The positive relationship be-
tween Chl-a, dissolved oxygen, and SRP with the second
component suggest SRP as a factor that stimulates phytoplank-
ton growth in this system, and also as a symptom of eutrophi-
cation (Cloern, 2001).
In spite of the spatial and temporal variability observed
in the water quality of both lagoons, it was possible to de-
termine similarities and differences in the water’s physical
and chemical characteristics among sampling stations that
made lagoon zoning possible. Both lagoons were divided
into three areas that included similar stations. The number
of stations in each area can vary seasonally as a result of
hydrological variability. This behavior of increasing and
decreasing the size of these areas is a basic characteristic
427
for estimating the conservation status of these types of eco-
systems, and could be useful as a vulnerability indicator,
CH-I
since the hypothesis has been that coastal ecosystems with
higher natural hydrological variability have higher resilience
capacity, at least to natural impacts such as hurricanes
(Herrera-Silveira, 1993; Comı́n et al., 2004). In this regard,
the distance matrix displayed as a two-dimensional multidi-
mensional scaling (MDS) ordination plot, showed clearly
that both lagoons are quite different reflecting the variability
of their hydrological matrix. The main variables, which
explain this dissimilarity, are related to specific characteris-
tics of SGD and pollution sources in each lagoon. However,
the distance among the sampling stations of each lagoon, in-
dicates that Celestún is more variable than Chelem, suggest-
ing that the latter is more vulnerable at least to natural
impacts.
The eutrophic status as a synthetic characteristic of these
coastal ecosystems (Karydis and Tsirtsis, 1996) indicates that
there are differences between the two lagoons that vary
spatially according to the zoning pattern. With respect to
dissolved inorganic nitrogen concentrations, Celestún showed
an oligo-mesotrophic behavior, while Chelem was meso-
eutrophic. The nutrient loadings from SGD and the higher
water residence time in Chelem promote these differences,
driving Chelem to short-term eutrophic conditions if no
actions are taken soon to reduce wastewaters discharge
from the urban area to the aquifer. Several symptoms of
eutrophic conditions in Chelem have already been observed,
including the loss of seagrass coverage and changes in the
phytoplankton community (Herrera-Silveira et al., 1999,
2000).
Regarding SRP, the status of both lagoons was oligotrophic,
being slightly higher in Chelem. The region’s karst soils pro-
mote low SRP inputs from SGD. This is due to SRP affinity
for calcium carbonate, which makes it less available in the wa-
ter column, turning it into a limiting element for phytoplank-
ton growth. Slight increases in SRP concentrations modify
significantly the N:P ratio in these ecosystems, and promote
significant changes in aquatic productivity and phytoplankton
community composition (Phlips et al., 2002; Skogen et al.,
2004; Vuorio et al., 2005).
The higher trophic status in Chelem with respect to Celes-
tún for nutrient concentrations is not reflected in the Chl-a tro-
phic index. However, the phytoplankton community structure
of both lagoons is different (Herrera-Silveira et al., 1999), sug-
gesting that, in these karst tropical ecosystems, phytoplankton
species composition could be in an early stage indicator of
eutrophication.
The methodological approach followed in this study to
understand the processes related to water quality and eutro-
phication trends in karst tropical coastal lagoons, through
the simultaneous analyses of two ecosystems differing in
water quality due to differences in intensity and type of hu-
man activities, represents a reference term for monitoring
programs, and should not substitute for long-term data anal-
ysis. We believe that with this paper, we are providing
a sound basis for developing an integrated approach for
428 F.U. Tapia González et al. / Estuarine, Coastal and Shelf Science 76 (2008) 418e430

(a) Nitrites (b) Nitrates

6 6
CE CH CE CH
5.5 E 5.5 E
5 5
Trophic Index

Trophic Index
4.5 4.5

4 M 4 M

3.5 3.5

3 3
2.5 O 2.5 O

2 2
IZ MZ SZ IZ MZ HZ IZ MZ SZ IZ MZ HZ
Zones Zones

(c) Ammonium (d) SRP

6 6
CE CH CE CH
5.5 E 5.5 E
5 5
Trophic Index

Trophic Index
4.5 4.5
4 M 4 M
3.5 3.5
3 3
2.5 O 2.5 O
2 2
IZ MZ SZ IZ MZ HZ IZ MZ SZ IZ MZ HZ
Zones Zones

(e) SRSi (f) Chl-a

6 6
CE CH CE CH
5.5 E 5.5 E
5 5
Trophic Index

Trophic Index

4.5 4.5
4 M 4 M

3.5 3.5
3 3
2.5 O 2.5 O

2 2
IZ MZ SZ IZ MZ HZ IZ MZ SZ IZ MZ HZ
Zones Zones

Fig. 8. Box-and-whisker diagrams of the Trophic Index calculated by zone of the lagoons: inner zone (IZ), mixing zone (MZ), marine zone (SZ), harbor zone (HZ).
The dashed lines indicate the trophic status: oligotrophic (O), mesotrophic (M) and eutrophic (E).

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Acknowledgments
This work is part of the MSc thesis of F.U.T.G. at CINVES-
TAV-IPN, University of Mérida. We acknowledge the help of
Javier Ramirez, Israel Medina, Jorge Trejo, Arturo Zaldivar,
Gregory Arjona, Jorge Guemez, and Victor Vidal for his
help in sample collection, analysis and experience in the study
area. We also thank CONACyT.
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