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Planktonic indicators of water quality
Water quality indicators in Lake Xochimilco, Mexico: zooplankton and Vibrio cholera
Sarma NANDINI,
*
Pedro RAMÍREZ GARCÍA, S.S.S. SARMA
Division of Research and Post-graduate Studies, National Autonomous University of Mexico
Campus-Iztacala, Av. De Los Barrios #1, Los Reyes Iztacala, Tlalnepantla, State of Mexico,
Mexico
*
Corresponding author; nandini@unam.mx
ABSTRACT
Lake Xochimilco is a eutrophic water body in Mexico City used by the local population
for aquaculture and agriculture. Water level is maintained with inputs of partially treated waste
water from the Cerro de la Estrella treatment plant. In this study we analysed the water quality at
two sites of Lake Xochimilco, Lake Xaltocan and the Santa Cruz Canal using various indicators
such as zooplankton diversity, saprobic indices, bacterial concentrations and physico-chemical
variables. Eighty litres of water was filtered from Lake Xochimilco from each site, once a month
from March to October of 2012, and the rotifers, cladocerans and copepods were enumerated and
identified. Physico-chemical parameters such as temperature, pH, Secchi depth, water depth,
nitrogen and phosphorus and chlorophyll a concentrations, and bacterial densities were measured.
During the study we recorded 33 species of rotifers, the most abundant being Brachionus
angularis, B. calyciflorus and B. havanaensis. Among the microcrustaceans the most abundant
were the cladoceran Moina micrura and the copepods Acanthocyclops americanus and
Arctodiaptomus dorsalis. The species diversity was around 2 bits/ind. and the saprobic index
between 1.5-2.0, indicating that both sites were β meso-saprobic. At both sites nitrogen was <1
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mg/L and phosphorus ranged between 2.5-7.8 mg/L. Chlorophyll a concentrations were between
66-136 µg/L. The toxigenic (Vibrio cholerae No-O1/No-O139) and the non-toxigenic (Vibrio
cholerae No-O135) strains of the bacterium were recorded, closely associated with littoral
rotifers and cladocerans particularly Brachionus quadridentatus and Alona sp. All variables
indicate that these sites in Lake Xochimilco are eutrophic and highly contaminated and that the
water quality needs to be improved.
Key words: Rotifers; microcrustaceans; saprobic index; Vibrio cholerae; water quality.
INTRODUCTION
Lake Xochimilco is a system of relict channels of large, shallow, ancient lakes, over
which the Aztecs built their city of Tenochtitlan and were transformed by the chinamperas
agricultural practices which includes building of floating islands for agriculture (UN-CSD-
WAND, 2006). This system is eutrophic and often polysaprobic and thus affecting sensitive
species and allowing only resistant taxa to persist. Its channels cover an area of 125 km
2
. One of
the major problems is the poor treatment of the water in the feeding channels and part of the
agricultural area. Most of it comes from the Cerro de la Estrella waste water treatment plant,
which for decades, has filled the lake area. This water body also contains several pathogens and
is often the focal point for several hydro-transmissible diseases, including cholera (Rodríguez-
Angeles, 2002). Unfortunately, the agricultural system on the lake, regardless of the poor water
quality, currently provides vegetables to Mexico City. Previous works showed the
epidemiological distribution of different serotypes and serogroups of pathogenic E. coli and V.
cholerae non- 01 (Solís, 2005).
Survival of pathogenic bacteria in aquatic environments is affected by biotic and abiotic
factors such as zooplankton bacterivory, oxygen concentrations, pH, temperature, conductivity
and availability of nutrients (Cortés-Muñoz et al., 2000; Joaquim-Justo et al., 2006). The
importance of zooplankton in the energy transfer to higher trophic levels has been well
documented (Nandini et al., 2004). Cladocerans, copepods and rotifers (40-500 µ) are important
generalist or specialist feeders, depending on the species (Gulati et al., 1990). Zooplankton are
important for the development and spread of V. cholerae (Huq et al., 1983). Microcrustaceans
such as cladocerans and copepods are particularly important since several studies show that V.
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cholerae (Huq et al., 1983; Huq and Colwell, 1996; Borroto, 1997) adheres to the animals using
the chitinous carapace as a source of nutrients to be degraded by chitinase (Lipp et al., 2002).
Lake Xochimilco has high densities of tilapias and carps, which makes the predation
pressure on microcrustaceans high; it is also populated by the endemic and endangered Axolotls
(Ambystoma mexicanum). The zooplankton is often dominated by rotifers, as in many tropical
water bodies, due to the high predation pressure on microcrustaceans by fish larvae. The lake also
has moderate densities and diversity of microcrustaceans (Nandini et al., 2005, 2007; Enriquez-
Garcia et al., 2009). Zooplankters are sensitive indicators of water quality and several indices
have been developed using them (Sládeček, 1983). A commonly used one is the saprobic index
which indicates the load of putrescible organic matter in surface waters and their decomposition.
Levels of decomposition are also reliably estimated by evaluating the BOD levels. Previous
studies in Xochimilco indicate that it has a high level of decomposition due to the BOD values
which were often above 10 and up to 80 mg L
-1
(Nandini et al., 2005). Rotifers, cladocerans and
copepods are often efficient bacterivores and are capable of lowering bacterial concentrations in
partially treated waste waters (Monakov, 2003; Nandini et al., 2005). Some taxa such as the
cladoceran Moina macrocopa and the rotifer Brachionus rubens, in fact have higher population
growth rates on partially treated waste water with high levels of decomposing organic wastes as
compared to defined cultured media with algal food (Nandini et al., 2004). Considered as
generalist, Moina species are unable to select specific food quality based on taste or nutritional
quality. Ramírez-García et al. (2012) report that rotifers do not feed on V. cholera as much as
cladocerans. The implication of this in relation to the zooplankton of Lake Xochimilco has rarely
been analysed, in spite of the importance of lowering densities of this pathogenic bacterium by all
possible means.
The increasing demand for freshwater for drinking water production and agriculture
emphazises the importance of research on water quality. From the clinical point of view, studies
on Vibrio cholerae in Lake Xochimilco are also very important because vegetables irrigated with
water from this lake are widely consumed in Mexico City. Therefore, the objectives of this study
were to analyse the zooplankton in relation of Vibrio cholerae and water quality variables in two
sites in Lake Xochimilco over a period of eight months.
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METHODS
Monthly samples were collected at two sites in Lake Xochimilco, the canal Santa Cruz
and the lake Xaltocan (Sites I and II, respectively) from March to October, 2012, a period that
includes the dry and the rainy season in Mexico City. We collected the zooplankton samples,
filtering 80 L of water through 63 µm plankton net (the effective pore size was much lower due
to the accumulation of seston from the lake on the mesh during the process of filtering) and
fixing the samples immediately in the field with 4% formalin. Moore swabs were set up at each
site in order to collect as many planktonic Vibrio as possible. After 24 h, these were removed and
transported to the laboratory in Amies medium and processed immediately to enumerate the
bacteria.
In the laboratory, rotifers were identified using Koste (1978) and quantified using a
Sedgewick Rafter counting chamber. We counted three aliquots of one millilitre from each
sample, and the average of the three counts were used for further analyses. During this study all
the rotifer, cladoceran and copepod species were quantified and in this process higher than 1000
individuals of the dominant taxa were enumerated. We selected rotifers which reached densities
more than 300 ind L
-1
at either study site during any month of the year as a dominant species and
followed changes in its population density over the study period. In the case of micro-
crustaceans, species present for most of the sampling period were selected for further analyses.
Physical and chemical variables such as temperature, pH, dissolved oxygen and
conductivity were measured in the field using Hanna probes and transparency was also measured
using a Secchi disk. Dissolved nitrates and phosphates were measured using a YSI 9100 multi-
parameter test kit and the BOD
5
following Clesceri et al. (1998). Chlorophyll a was extracted
using acetone and measured using a Fluorometer (Aquafluor, Turner Equipments). Bacteria were
enumerated by growing 10 mL aliquots of the sample on alkaline peptone broth, incubated at
37ºC for 18 h, and then the biofilm was plated on TCBS agar plates for enumerating typical
colonies of Vibrio cholerae (Colwell et al., 1980).
Zooplankton diversity was calculated using the Shannon-Wiener formula (Krebs, 1993):
H´= -∑ p
i
log
2
p
i,
where H´ is the index of species diversity, and p is the proportion of individuals of the ith species.
Species diversity was calculated using the program DIVERS as in Krebs (1993). Data
were tested for statistically significant differences using t-tests (Sigma Plot 12 -
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http://www.sigmaplot.com). In order to test for relations between the physicochemical variables
and Vibrio cholerae with zooplankton we conducted a multifactorial analysis using CANOCO for
Windows 4.5.
Saprobic indices (S) were calculated using the formula proposed by Pantle and Buck
(1955):
S = Ʃ (s.h) / Ʃh
where
S is the Pantle and Buck (1955) saprobic index;
s is the valence of each rotifer (Sládeček, 1983);
h is the relative frequency (1, uncommon; 3, common; 5, abundant);
The saprobic index S is based on the following ranking scale: 1.0-1.5, oligosaprobic; 1.6-2.5, β-
mesosaprobic; 2.6-3.5, α-mesosaprobic; 3.6≥4.4, polysaprobic.
The trophic state of the reservoir was calculated using ratios based on the number of
Brachionus to Trichocerca species (B/T ratios; Sládeček, 1983).
RESULTS
The physicochemical variables observed at both study sites during this period are shown in
Tab. 1. The temperature ranged between 19.5-22°C with no significant differences between sites.
Both sites are part of a shallow water body where the maximum depth did not surpass 1.5 m; the
Secchi transparency was also low ranging between 0.18-0.4 m. The conductivity was low as can
be expected in a freshwater body; the pH ranged between 6.9-9.5 and was almost always alkaline
at both sites. The COD ranged between 80-135 mg/L and was often lower in the lake as
compared to the canal. The dissolved oxygen was higher (>10 mg/L) during spring and autumn
as compared to the summer months at both sites. In general, the oxygen levels were lower (<4
mg/L) in the Canal as compared to the lake (Fig. 1). Both sites were severely nitrogen (<1 mg/L)
limited as compared to phosphorus (2.5-7.8 mg/L) (Fig. 1) Chlorophyll a (66-136 µg/L), coliform
bacteria and Vibrio sp. concentrations were higher in the canal as compared to the lakes (Fig. 1);
overall these levels along with those of the nutrients clearly indicate that this is a highly
eutrophic water body.
During this study we observed 33 species of Monogonont rotifers; bdelloids were observed
but not identified and therefore not enumerated (Tab. 1). The most species rich family was
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Brachionidae. The rest of the families were represented by just a few species. Amongst predatory
rotifers we only observed Asplanchna brightwellii and Dicranophorus caudatus, of which the
former was more abundant with densities frequently above 50 ind/L B. calyciflorus, B. angularis
and B. havanaensis were present most of the study period at densities above 1000 ind/L, even
more than the evasive Polyarthra vulgaris (Fig. 2). At both study sites, during the study we
observed four species of cladocerans and two species of copepods, Arctodiaptomus dorsalis and
Acanthocyclops americanus (Tab. 2). The most abundant cladoceran was Moina micrura
although its density was very low compared to those of rotifers, rarely increasing beyond 10
ind/L. Among the copepods, naupliar and copepodite stages of both species were more abundant
as compared to the adult stages. However, the densities of cyclopoids were more than twice as
high as that of the calanoid (Fig. 3). Females of both taxa were more abundant than the males.
While rotifers were generally more abundant at site I, the micro-crustaceans were more abundant
at Site II. The species diversity was above 2 bits/ind. during most of the study period, at both
sites; in general it was significantly higher (P<0.01; t-test) at Site II as compared to Site I (Fig. 4).
The evenness ranged between 0.4-0.65, during most of the study period with no significant
differences amongst the study sites (P>0.05; t-test). As expected, the Pantle and Buck saprobic
index was above 1.5 but below 2.0 for most of the study period at both sites but it was
significantly lower (P<0.01; t-test) at Site II as compared to Site 1.
In this study, both the toxigenic (Vibrio cholerae No-O1/No-O139) and the non-toxigenic
(Vibrio cholerae No-O135) strains of the bacterium were recorded. The multifactorial analyses
indicate that more taxa of zooplankton are associated with low levels of contamination as
compared to high degrees of the same (Fig. 5). Shallow waters also promote greater species
richness as do high pH and higher concentrations of oxygen. Vibrio cholerae was closely
associated with littoral rotifers and cladocerans particularly Brachionus quadridentatus and
Alona sp. Most species were positively associated with high Secchi depth (less phytoplankton)
and high oxygen availability or conditions of less decomposition.
DISCUSSION
Lake Xochimilco is part of the ancient lake basin that once covered the Valley of Mexico
but is now restricted to small pockets in the north and south of Mexico City. This study was
carried out in the southern zone of the city which has a high density of human population, thus
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the pressure on the water body is high. Our study clearly indicates that both the Santa Cruz canal
and Lake Xaltocan are highly eutrophic and contaminated with bacteria. The coliform bacteria
concentrations observed in this work were higher than the permissible limits of 400 MPN/100
(Clesceri et al., 1998).
Rotifers are common inhabitants of freshwater bodies and along with cladocerans and
copepods form the dominant biomass of planktonic communities (Walz, 1993). Two of the
factors that control the proportion of zooplankton in aquatic systems are competition and
predation. Rotifers suffer from exploitative and interference competition from cladocerans which
results in an inverse relationship between their densities and that of microcrustaceans (Gilbert,
1988). However, as compared to competition, predation is a stronger structuring force. The high
predation pressure in Lake Xochimilco from larval tilapia and carps is well documented
(Zambrano et al., 2010); these taxa reach high densities and since they reproduce all year around,
they consume high numbers of cladocerans and copepods especially since the prey are more
visible to these visual predators. This often results in higher densities of rotifers as compared to
microcrustaceans, as observed in our study. The densities of rotifers were more than a 1000 fold
as compared to the micro-crustaceans in both the Santa Cruz canal and the Lake Xaltocan;
previous studies also report similar findings (Nandini et al., 2005). Among cladocerans, the only
species that could be recorded on a regular basis was Moina micrura, probably because of its
high reproductive rate and the copepods (Acanthocyclops americanus and Arctodiaptomus
dorsalis). Copepods frequently escape predators as a result of their rapid (80 mm/s) and evasive
movements (Bradley et al., 2012).
Zooplankton species have been used as indicators of water quality in several studies in
lakes and rivers (Wallace et al., 1996). Rotifers are one of the sensitive indicators but pose
difficulties in acquiring adequate taxonomic skills to identify them. Nevertheless, it has been well
documented that brachionids are indicators of eutrophic waters while trichocercids of oligo-
mesotrophic water (Sládeček, 1983). The extremely high densities of the rotifers, often above
3000 ind/L is also probably due to the high availability of bacteria on which most rotifers feed
(Monakov, 2003). The physico-chemical variables of a low N:P ratio and high concentration of
Chlorophyll a (66-136 µg/L) are indicative of a eutrophic system (Gulati et al., 1990). Our study
clearly shows that the study sites in Lake Xochimilco are eutrophic since it has a B/T ratio of 10,
in spite of the fairly high species diversity also reported in other studies from this water body
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(Nandini et al., 2005; Enriquez-García et al., 2009). The saprobic index also ranged from 1.5-2.0,
that is β-mesosaprobic, which shows high levels of decomposition in this aquatic system, also
corroborated by the high COD. High levels of bacteria, in general and coliform bacteria in
particular are also indicative of poor water quality; in Lake Xochimilco these levels are more than
the maximum permissible limit since the water used to maintain the water level comes from a
water treatment plant which often does not treat water to adequate levels.
The male-female ratio in copepods is often biased towards females which is important
since it results in higher population growth rates. We also found that the densities of females
were higher than that of males in both Acanthocyclops robustus as well as Arctodiaptomus
dorsalis. It has been suggested that this skewed sex ratio, common in both field and experimental
situations, is also a result of sex change and forming intersexes that copepods are capable of
(Gusmão and McKinnon, 2009).
Vibrio cholerae is frequently found in Lake Xochimilco, mostly associated with cyclopoid
copepods (64.8%), copepod nauplii (28.9%), cladocerans (6.3%) and the rest with rotifers.
Several studies have shown that Vibrio cholerae is associated with rotifers, cladocerans and
copepods in fresh and brackish waters (de Magny et al., 2011). Rawlings et al. (2007) have
shown that Vibrio has a propensity to be epizoic on micro-crustaceans and this helps them to
cross various barriers in lakes such as the thermocline and pycnocline (Grossart et al., 2010).
With total rotifer or crustaceans vs Vibrio density we found no significant correlations; however
we found that Vibrio was most strongly associated with zooplankton, especially the rotifers
Brachionus plicatilis, B. leydigi, B. quadridentatus and the cladoceran Alona. Brachionus
plicatilis is frequently associated with several species of Vibrio and a new species, Vibrio
rotiferianus was also reported on this rotifer taxa (Gomez-Gil et al., 2003). There was however
no association of Brachionus angularis and B. havanaensis in the multivariate analyses with
Vibrio although the density of these rotifers was highest during the period in which that of the
bacteria was also high (Figs. 1 and 2).
Lake Xochimilco is a UNESCO Cultural Heritage Site and urgent measures are necessary
to improve the water quality, especially since it is also the type locality of the endangered axolotl
Ambystoma mexicanum (Zambrano et al., 2010). Our study clearly shows that both study sites are
eutrophic and moderately to highly contaminated as measured by all indicators used, rotifers in
the saprobic index, bacterial densities, nitrogen and phosphorus concentrations or the COD
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concentrations. The lake is also shallow (<1.5 m) and thus with a greater propensity to harbour
high densities of Vibrio cholerae as shown in an extensive study by Huq et al. (2005). It is
obvious that there is a health risk for the people who live in the region and use this water to fish
or for agriculture. The most recommended means to improve the water quality is to improve the
functioning of the water treatment plant which provides water to the lake.
CONCLUSIONS
Our study showed that in spite of the high levels of contamination by organic matter in
the eutrophic Lake Xochimilco, as seen in the β-mesosaprobic state of the lake, the species
diversity is mostly above 2. We found both the toxigenic and the non-toxigenic strain of Vibrio
cholerae (Vibrio cholerae No-O1/No-O139 and No-O135, respectively) of the bacterium in the
lake. The species richness was significantly higher in the shallow part of the lake. Vibrio sp. is
closely associated with littoral rotifers and cladocerans particularly Brachionus plicatilis, B.
leydigi, B. quadridentatus and the cladoceran Alona sp. This indicates a health risk for the people
who live in the region and use this water for fishing or agriculture. Water quality can be
improved if the functioning of the water treatment plant, which provides water to the lake, is
ensured.
ACKNOWLEDGMENTS
We thank PAPCA 16 (Programa de Apoyo para Profesores de Carrera para Promover Grupos de
Investigaciòn) for financial support and Martha Gaytan for technical assistance. We also thank
PAPIIT (Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica) IN213413
for additional support.
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Zambrano L, Valiente E, Vander Zanden MJ, 2010. Food web overlap among native axolotl
(Ambystoma mexicanum) and two exotic fishes: carp (Cyprinus carpio) and tilapia
(Oreochromis niloticus) in Xochimilco, Mexico City. Biol. Invasions 12:3061-3069.
Accepted Article
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Tab. 1. Physicochemical variables at the study sites in Lake Xochimilco.
Site
Mar
April
May
June
July
Aug.
Sep.
Oct.
Depth (m)
Canal Santa Cruz
1.00
1.08
1.31
1.23
1.24
1.45
1.26
1.12
Laguna Xaltocan
1.21
1.32
1.32
1.26
1.35
1.28
1.38
1.27
Secchi depth (m)
Canal Santa Cruz
0.2
0.34
0.30
0.25
0.38
0.38
0.34
0.25
Laguna Xaltocan
0.4
0.30
0.27
0.18
0.43
0.35
0.43
0.37
Temperature (°C)
Canal Santa Cruz
19.7
19.4
22.3
20.7
21.5
20.9
19.5
20.0
Laguna Xaltocan
21.4
19.4
22.0
21.0
21.0
20.7
19.9
19.9
Conductivity (µS/cm)
Canal Santa Cruz
812
738
691
671
1124
997
901
813
Laguna Xaltocan
780
747
750
750
954
974
994
838
pH
Canal Santa Cruz
7.88
8.41
8.25
7.64
7.56
7.38
6.92
7.45
Laguna Xaltocan
8.60
9.53
9.35
9.23
7.71
7.44
7.20
8.36
Chemical oxygen demand (mg/L)
Canal Santa Cruz
134.1
104.8
109.1
105.6
133
80.20
94.47
94.47
Laguna Xaltocan
80.51
65.22
113.0
105.31
71.64
95.75
81.48
92.47
Dissolved oxygen (mg/L)
Canal Santa Cruz
3.65
11.2
12.4
4.05
2.19
2.45
0.45
3.15
Laguna Xaltocan
19.33
17.55
18.38
12.50
4.75
4.41
8.30
9.61
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Tab. 2. List of species found in the sites of Lake Xochimilco.
Taxonomic group Species
Rotifera
Epiphanidae
Epiphanes macrourus (Barrois & Daday. 1894)
Brachionidae
Anuraeopsis fissa (Gosse, 1851)
Brachionus angularis (Gosse, 1851)
B. bidentatus Anderson, 1889
B. budapestinensis (Daday, 1885)
B. calyciflorus Pallas, 1766
B. caudatus Barrois & Daday, 1894
B. durage Dhanapati, 1978
B. havanaensis Rousselet, 1911
B. leydigi Cohn, 1862
B. quadridentatus (Hermann, 1783)
B. plicatilis (O.F. Müller, 1786)
Plationus patulus (O.F. Müller, 1786)
Platyias quadricornis (Ehrenberg, 1832)
Keratella americana Carlin, 1943
K. cochlearis (Gosse, 1851)
K. tropica (Apstein, 1907)
Mytilinidae
Mytilina ventralis (Ehrenberg, 1832)
Lindidae
Lindia torulosa Dujardin, 1841
Colurellidae
Lepadella rhomboides (Gosse, 1886)
L. patella (O.F. Müller, 1786)
Lecanidae
Lecane curvicornis (Murray, 1913)
L. hamata (Stokes, 1896)
Notommatidae
Cephalodella gibba (Ehrenberg, 1838)
Trichocercidae
T. similis (Wierzejski, 1893)
Gastropodidae
Ascomorpha ovalis (Bergendal, 1892)
Synchaetidae
Polyarthra vulgaris Carlin, 1943
Synchaeta pectinata Ehrenberg, 1832
Asplanchnidae
Asplanchna brightwellii (Gosse, 1850)
Dicranophoridae
Dicranophorus caudatus (Ehrenberg, 1834)
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Taxonomic group Species
Flosculariidae
Sinantherina sp.
Filiniidae
Filinia longiseta (Ehrenberg, 1834)
Microcrustaceans
Cyclopoid copepod
Acanthocyclops americanus (Marsh, 1893)
Calanoid copepod
Arctodiaptomus dorsalis (Marsh, 1907)
Cladocera
Moina micrura Kurz, 1874
Alona sp.
Chydorus sphaericus (O. F. Müller, 1776)
Diaphanosoma birgei Korinek, 1981
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Fig. 1. Seasonal variations in the concentration of phosphate phosphorus, nitrate nitrogen,
chlorophyll a, coliform bacteria and Vibrio at the two study sites in Lake Xochimilco!
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Fig. 2. Seasonal variations in the abundance of selected rotifer species from Lake Xochimilco.
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Fig. 3. Seasonal variations in the abundance of selected crustacean species from Lake
Xochimilco.
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Fig. 4. Changes in the value species diversity index from the lake Xochimilco.
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Fig. 5. Results of multifactorial analysis using CANOCO. 1. Asplanchna 2. B. durgae 3.
Synchaeta 4. B. quadridentatus 5. Filinia 6. Sinantherina 7. B calyciflorus 8. B. angularis 9.
Polyarthra vulgaris 10. K. tropica 11. B. caudatus 12. B. havanaensis 13. D. caudatus 14. T.
similis 15. B. plicatilis 16. B. leydigi 17. K. cochlearis 18. B. bidentatus 19. B. budapestinensis
20. F. opoliensis 21. Epiphanes macrourus 22. Lindia torulosa 23. L. patella 24. M. ventralis
25. K. americana 26. A. ovalis 27. Anuraeopsis fissa 28. L. curvicornis 29. L. rhomboides 30.
L. hamata 31. C. gibba 32. Platyias quadricornis 33. Plationus patulus 35. Nauplii 36.
Cyclopoid copepodite 37. Cyclopoid female 38. Cyclopoid male 39. Calanoid copepodite 40.
Calanoid female 41. Calanoid male 42. Moina micrura 43. Alona 44. Pleuoroxus 45
Chydorus.!
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