Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)

Abstract

Karstic water bodies represent the most relevant limnologic feature of the Yucatan Peninsula, Mexico. These systems harbor endemic species and are the main regional epigean source of freshwater. In this work, the morphometry, basic limnological features, and the zooplankton and fish fauna of five aquatic karstic systems from the central zone of Quintana Roo State, Mexico (in the heart of the Zona Maya) were surveyed. The possible relation between species richness and morphometric features was tried to be established. Overall, 79 taxa were found, 64 belong to zooplankton, and 15 to nekton. All studied systems were oligotrophic, with high transparency, and low nutrients and chlorophyll a concentration, thus differing from other water bodies in central Mexico. The two different types of karstic systems studied were the typical "cenote", and the "aguada". Both showed differences in biological, physical, and chemical variables. A one-way ANOVA test demonstrated significative differences in nutrients (nitrates, F = 61.52, p<0.001; nitrites, F=7.361, p<0.001) and conductivity (F = 497.491, p<0.001) among systems. A simple concordance cluster analysis showed that species richness and community composition were also different between these two types of aquatic systems. In contrast to previous results found in central and southeastern Mexico, no correlation between species richness and morphometric parameters (area and shoreline development) were found. In the south-central region of the Yucatan Peninsula, the aquatic karstic systems are poorly known (physically, chemically and biologically). In fact, this is the first approach to understand the limnology and the relation between species richness and morphometric variables of the sinkholes from the region.

Full text

49
Teoría y Praxis · ISSN 1870 1582 · núm. 25 · may-august 2018 · pp. 49-68
*E-mail:
adcervantes@uqroo.edu.mx
Aquatic biodiversity in cenotes from the Yucatan
Peninsula (Quintana Roo, Mexico)
Adrián Cervantes-Martínez*
Martha A. Gutiérrez-Aguirre
Universidad de Quintana Roo
Manuel Elías-Gutiérrez
Ana Minerva Arce-Ibarra
Alma García-Morales
El Colegio de la Frontera Sur
Recieved: 05/10/17 · Accepted: 28/10/17
Abstract
Karstic water bodies represent the most relevant limnologic feature of the Yucatan
Peninsula, Mexico. These systems harbor endemic species and are the main regional
epigean source of freshwater. In this work, the morphometry, basic limnological features,
and the zooplankton and fish fauna of five aquatic karstic systems from the central zone
of Quintana Roo State, Mexico (in the heart of the Zona Maya) were surveyed. The
possible relation between species richness and morphometric features was tried to be
established. Overall, 79 taxa were found, 64 belong to zooplankton, and 15 to nekton.
All studied systems were oligotrophic, with high transparency, and low nutrients and
chlorophyll a concentration, thus differing from other water bodies in central Mexico.
The two different types of karstic systems studied were the typical “cenote”, and the
“aguada”. Both showed differences in biological, physical, and chemical variables. A
one-way ANOVA test demonstrated significative differences in nutrients (nitrates, F =
61.52, p<0.001; nitrites, F=7.361, p<0.001) and conductivity (F = 497.491, p<0.001)
among systems. A simple concordance cluster analysis showed that species richness
and community composition were also different between these two types of aquatic
systems. In contrast to previous results found in central and southeastern Mexico, no
correlation between species richness and morphometric parameters (area and shoreline
development) were found. In the south-central region of the Yucatan Peninsula, the
aquatic karstic systems are poorly known (physically, chemically and biologically). In
fact, this is the first approach to understand the limnology and the relation between
species richness and morphometric variables of the sinkholes from the region.
Key words: cenotes, freshwater, karst, aquatic biodiversity, limnology.

50
Biodiversidad acuática en cenotes de la Península
de Yucatán (Quintana Roo, México)
Adrián Cervantes-Martínez*
Martha A. Gutiérrez-Aguirre
Universidad de Quintana Roo
Manuel Elías-Gutiérrez
Ana Minerva Arce-Ibarra
Alma García-Morales
El Colegio de la Frontera Sur
Recibido: 05/10/17 · Aceptado: 28/10/17
Resumen
Los cuerpos de agua kársticos representan la característica limnológica más relevante
en la península de Yucatán, México. Estos sistemas albergan especies endémicas y
son la principal fuente regional epigea de agua dulce. En este trabajo se estudian
la morfometría, las propiedades limnológicas básicas, así como el zooplancton y la
fauna de peces en cinco sistemas acuáticos kársticos de la zona centro del estado
de Quintana Roo, México (en el corazón de la zona maya). Se trató de establecer la
relación entre la riqueza de especies y las propiedades morfométricas. En general se
encontraron 79 especies, 64 corresponden a zooplancton y 15 a necton. Todos los
sistemas estudiados son oligotróficos de alta transparencia con bajas concentraciones
de nutrientes y clorofila a diferenciándose así de otros cuerpos de agua en el centro
de México. Los dos sistemas kársticos estudiados fueron los cenotes y las aguadas.
Ambos mostraron diferencias en las variables biológicas, físicas y químicas. Una prueba
ANOVA unidireccional demostró diferencias significativas en nutrientes (nitratos, F =
61.52, p<0.001; nitritos, F=7.361, p<0.001) y conductividad (F = 497.491, p<0.001)
entre los sistemas. Un análisis simple de concordancia de grupos mostró diferencias en
riqueza de especies y composición de la comunidad entre los dos sistemas acuáticos.
En contraste con resultados previos encontrados en el centro y sureste de México, no se
encontró correlación entre riqueza de especies y parámetros morfométricos (desarrollo
del área y litoral). Se conoce poco de los sistemas acuáticos kársticos de la región sur-
centro de la Península de Yucatán (física, química y biológicamente). De hecho, este es
el primer intento por estudiar la limnología y la relación riqueza de especies y variables
morfométricas de los cenotes de la región.
Palabras clave: cenotes, agua dulce, karst, biodiversidad acuática, luminología
Teoría y Praxis · ISSN 1870 1582 · núm. 25 · mayo-agosto 2018 · pp. 49-68
*Correo electrónico:
adcervantes@uqroo.edu.mx

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Teoría y Praxis núm. 25
Introduction
Karstic surfaces occupy 10% of the world land mass and contain up to 25%
of the freshwater available for human use (White et al., 1995: 451; González &
Hernández 1998: 57-58). Part of this amount is found in karstic aquatic sys-
tems known in the Yucatan Peninsula as “cenotes” and “aguadas”, both
formed by dissolution of Eocene limestone rocks (Hall 1936: 5; Gaona-Vizcaino
et al.,1980: 32). This kind of systems harbour endemic taxa of fish and inverte-
brates (Suárez-Morales & Rivera-Arriaga 2000: 152).
The Mayan zone is located in the center region of the state of Quintana
Roo, Mexico, it has a large number of aquatic karstic systems, many of them
unknown and without any studies (Cervantes-Martínez, et al., 2002: 170). This
zone is composed by the municipalities of Felipe Carrillo Puerto (including part
of the Sian Ka’ an, Biosphere Reserve) and the town of José María Morelos.
Most of the recent publications on Mexican karstic systems deal with tax-
onomy (Suárez-Morales et al., 1996: 296; Schmitter-Soto 1998: 238; Suárez-
Morales & Rivera-Arriaga 2000: 151; Sarma & Elías-Gutiérrez 1999: 187; Elías-
Gutiérrez & Suárez-Morales 2000: 64). Conversely, non-taxonomical aspects are
scarce (Chumba-Segura & Medina-González 2000: 9). It is clear that any kind
of integrative approach will allow general comparisons at the biological, and
ecological levels of the karst hydrology in the region and it will generate limno-
logical knowledge, which is still scarce in tropical latitudes.
So, the proposal of this work was to analyze the species richness of zoo-
plankton and fishes from five cenotes located in the central zone of Quintana
Roo, Mexico (Figure 1), to determine their possible relation to limnological and
morphometric characteristics.
Methods
Five karstic systems (named Esperanza, Galeana, Donato, km 157 and Mini-
cenote) were selected and sampled biweekly from February to May 2001 (dry
season). The study area is located between 19° 28’-19° 45’ N and 87° 53’-87°
59’ W in the state of Quintana Roo, Mexico. According to Hall (1936: 5) Galeana
(1), Esperanza (2), Km 157 (3), and Donato (4) are classified as type “aguada”
and minicenote (5) as vase-shaped sinkhole.

Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)
52


Yucatan
Peninsula
Caribbean
Sea
Figure 1. Location of the aquatic systems: 1) Galeana, 2) Esperanza,
3) km 157, 4) Donato and 5) Minicenote

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Zooplankton samples were collected from both the limnetic and the littoral
zones, with a filtering mesh of 50 µm. Samples were preserved in 4% sucred
formalin, followed by species level identification at the laboratory. Hook-and-
line gear, hand net, throw net, and visual records were used to collect and deter-
mine the fish fauna. A simple concordance cluster analysis was used to estimate
the similitude in species richness and composition among systems (Legendre &
Legendre, 1998: 853). The analysis was performed with the Statistical Package
MVSP 3.21.
Physical and chemical parameters such as temperature (°C), conductivity
(mS cm-1), pH, and dissolved oxygen, (mg l-1) were measured in situ at three
layers (surface, middle, and bottom) along the water column using an Hydro
lab Sonde Recorder™. Transparency was measured with a Secchi disk (Lind
1985: 199).
Chlorophyll a and nutrients (NO3, NO2 and PO4
3-) were determined by spectro-
photometry (A.P.H.A. 1990: 1193). Water samples were also taken at three layers
(superficially, middle and bottom) at the deepest point of the water column; us-
ing a 2 l Van Dorn sampler. All (biological, physical, and chemical) samples were
taken by triplicate. A single average value of physical and chemical variables was
obtained for each system (Armengol & Miracle 1999: 2245).
Morphometric data of the water bodies such as depth (m), area (m2), and
shoreline development (DL) were measured in situ and/or estimated using
standard methods (Lind 1985: 199). Differences in nutrients concentration (ni-
trates, nitrites, phosphates), chlorophyll a concentration, and water conductiv-
ity among systems were tested through a one-way ANOVA analysis. Relations
between species richness (a diversity) vs. system area, and vs. shoreline devel-
opment (DL) (all data was transformed to log) were estimated using Spearman
rank correlations (rs) (Legendre & Legendre, op. cit). All statistical analyses
were performed with the Statistical Package MVSP 3.21.
Results
Seventy-nine taxa were recorded, 43 species were rotifers, 18 cladocerans,
2 copepods 1 ostracod, and 15 fish (Table 1). They belong to 11 orders, 28
families, and 45 genera. The number of species was different in each system:

Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)
54
49 in Galeana, followed by Minicenote (36), Donato (25), km 157 (15), and
Esperanza (12). The general distribution of the species recorded here is as fol-
lows: most species recorded have cosmopolitan distribution (mainly rotifers),
followed by circumtropical (cladocerans), neotropical (fish), and one endemic
species (cladoceran) (see Table 1).
Table 1. Species registered in the cenotes of Quintana Roo. Dist=
Distribution; St= Subtropical; C= Cosmopolitan; Tn= Tropicopolitan; T=Tropical; An=
Antarctic; Ne-P= Nearctic-Palearctic region; N= North America; Ne-Tn= Nearctic-
tropicopolitan; N-He= North-hemisphere; A-A= America-Africa; Ct= Circumtropical;
Tr-C= Tropical-Caribbean; A= America; Ne= Neotropical; E= Endemic;
ND= Not determined
Taxon Dist
12345
Phylum: Rotifera
Clase: Monogononta
Orden: Ploimida
Familia: Brachionidae Harring, 1913
Anuraeopsis fissa (Gosse, 1851) St
+
Brachionus falcatus Zacharias, 1898 C
+ +
B. havanaensis Rousselet, 1991 St
+ +
Keratella americana Carlin, 1943 C
++++
K. lenzi (Hauer, 1953) St
+
Familia: Euchlanidae Ehrenberg, 1832
Dipleuchlanis propatula (Gosse, 1886) C
+
Euclanis incisa Carlin, 1939 C
+
Tripleuchlanis plicata (Levander, 1894) C
+
Familia: Mytilinidae Bory de St. Vincent, 1826
Mytilina ventralis (Ehrenberg, 1838) C
+
Familia: Colurellidae Bory de St. Vincent, 1824
Lepadella heterostyla Murray, 1913 ND
+
L. quadricarinata (Stenroos, 1898) ND
+
L. latusinus (Hilgendorf, 1899) ND
+
L. patella (O. F. Muller, 1786) C
+
L. triptera (Ehrenberg, 1830) C
+
Familia: Lecanidae Nizsch, 1827
Lecane aculeata (Jakubski, 1912) C
+
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Taxon Dist
12345
L. arcula Harring, 1914 C
+ + +
L. bulla (Gosse, 1851) C
+++++
L. closterocerca (Schmarda, 1859) C
+ +
L. cornuta (O. F. Muller, 1786) C
+ + + +
L. crepida Harring, 1914 Tn
+ + +
L. furcata (Murray, 1913) C
+ + +
L. hamata (Stokes, 1896) C
+++
L. hornemanni (Ehrenberg, 1834) C
+++++
L. leontina (Turner, 1892) T
+ + +
L. luna (O. F. Muller, 1776) C
+
L. lunaris (Ehrenberg, 1836) C
+ +
L. monostyla (Daday, 1897) St
+
L. obtusa (Murray, 1913) C
+ + +
L. pyriformis (Daday, 1905) C
+
Familia: Proalidae Harring & Myers, 1924
Prolaes dicipiens (Ehrenberg, 1831) C
+
Familia: Notommatidae Remane, 1933
Eothinia carogaensis Myers, 1937 ND
+
Notomata pachyura (Gosse, 1886) C
+ +
Familia: Scaridiidae
Scaridium botsjani Dames & Dumont, 1974 A
+
Familia Trichocercidae Lamarck, 1801
Trichocerca capucina (Wierzejski, & Zacharias, 1853) C
+
T. iernis (Gosse, 1887) C
+
T. weberi (Jennings, 1903) C
+
Familia: Synchaetidae Ehrenberg, 1832
Polyarthra cf. dolichoptera Idelson, 1925 C
+
Familia: Dicranophoridae Nitzsch, 1827
Dicranophorus prionacis Harring & Myers, 1928 Ne-P
+
Orden: Flosculariaceae
Table 1. Species registered in the cenotes of Quintana Roo. Dist= Distribution; St= Subtropical; C=
Cosmopolitan; Tn= Tropicopolit an; T=Tropical; An= Antarctic; Ne-P= Nearctic-Palearctic region; N=
North America; Ne-Tn= Nearctic-tropicopolitan; N-He= North-hemisphere; A-A= America-Africa;
Ct= Circumtropical; Tr-C= Tropical-Caribbean; A= America; Ne= Neotropical; E= Endemic;
ND= Not determined
(Continue)
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Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)
56
Taxon Dist
12345
Familia: Testudinellidae Bory de St. Vincent,
1826
Testudinella patina (Hermann, 1783) C
+ +
Familia: Flosculariidae
Ptygura furcillata (Kellicott, 1889) N
+ +
P. libera (Myers, 1934) Ne-Tn
+ +
Familia Hexarthridae Schmarda, 1854
Hexarhtra intermedia Wiszniewski, 1929 St
+
Subclase: Bdelloidea
Familia: Philodinidae Ehrenberg, 1830
Dissotrocha aculeata (Ehrenberg, 1832) ND
+ + + +
Superclase: Crustacea
Clase: Branchiopoda
Superorden: Cladocera
Orden: Anomopda
Familia: Daphnidade
Ceriodaphnia dubia Richard, 1894 C
+
Simocephalus mixtus Sars, 1903 N-He
+
S. serrulatus (Koch, 1841) C
+
Familia: Bosminidae Sars, 1865
Eubosmia (Neobosmina) tubicen Brehm 1953 A-A
+ + + +
Familia: Ilyocryptidae Smirnov, 1992
Ilyocryptus spinifer Herrik, 1882 C
+ + +
Familia: Macrothricidae Norman & Brady, 1867
Macrothrix cf. flabelligera Sminorv, 1992 Ct
+ + + +
Familia: Chydoridae Stebbing, 1902
Alonella cf. excisa Fischer 1854 ND
+
Chydorus sp. ND
+++
Ch. cf. kallipigos Brehm 1934 ND
+
Ch. eurynotus Sars, 1901 Ct
+
Ephemerophorus hybridus Daday, 1905 A
+
Dunhevedia odontoplax (Sars, 1901) Ne
+
Table 1. Species registered in the cenotes of Quintana Roo. Dist= Distribution; St= Subtropical; C=
Cosmopolitan; Tn= Tropicopolit an; T=Tropical; An= Antarctic; Ne-P= Nearctic-Palearctic region; N=
North America; Ne-Tn= Nearctic-tropicopolitan; N-He= North-hemisphere; A-A= America-Africa;
Ct= Circumtropical; Tr-C= Tropical-Caribbean; A= America; Ne= Neotropical; E= Endemic;
ND= Not determined
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Taxon Dist
12345
Alona cf. ossiani Sinnev, 1998 ND
+++
A. cf. verrucosa Sars, 1901 ND
+ + +
A. pectinata Elías-Gutiérrez & Suárez-Morales, 1999 E
+ +
A. cf. karua (King, 1853) ND
+
Camptocercus cf. dadayi (Stingelin, 1913) Ne
+
Graptoleberis occidentalis Sars, 1901 Ne
+
Ostracoda
Cypridopsis sp. C
+ +
Subclase: Copepoda
Infraclase: Neocopepoda
Superorden: Gymnoplea
Orden: Calanoida*
Familia: Diaptomidae G. O. Sars, 1903
Subfamilia: Diaptominae Kiefer, 1932
Mastigodiaptomus nesus Bowman, 1986 Ne
+++++
Superorden: Podoplea
Orden: Cyclopoida
Familia: Cyclopidae G. O. Sars, 1913
Subfamilia: Eucyclopinae Kiefer, 1927
Thermocyclops inversus Kiefer, 1936 Tr-C
+++++
Chordata
Astyanax aeneus (Günther, 1860) Ne
+ + +
Rhamdia guatemalensis (Günther, 1864) Ne
+ +
Belonesox belizanus Kner, 1860 Ne
+
Gambusia sexradiata Hubbs, 1936 Ne
++++
G. yucatana Regan 1914 Ne
+ +
Poecilia mexicana Steindachner, 1863 Ne
+ + + +
P. orri Fowler, 1943 Ne
+
“Cichlasoma” friedrichsthali (Heckel, 1840) Ne
+ +
“C.” salvini (Günther, 1862) Ne
+ +
“C.” synspilum (Hubss, 1935) Ne
+ + +
Table 1. Species registered in the cenotes of Quintana Roo. Dist= Distribution; St= Subtropical; C=
Cosmopolitan; Tn= Tropicopolit an; T=Tropical; An= Antarctic; Ne-P= Nearctic-Palearctic region; N=
North America; Ne-Tn= Nearctic-tropicopolitan; N-He= North-hemisphere; A-A= America-Africa;
Ct= Circumtropical; Tr-C= Tropical-Caribbean; A= America; Ne= Neotropical; E= Endemic;
ND= Not determined
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Taxon Dist
12345
“C.” urophthalmus (Günther, 1862) Ne
+++
Petenia splendida Günther, 1862 Ne
+ + + +
Thorichthys affinis (Günther, 1862) Ne
+
T. meeki (Brind, 1918) Ne
+ + +
Gobiomorus dormitor (Lacepéde, 1800) Ne
+
Table 1. Species registered in the cenotes of Quintana Roo. Dist= Distribution; St= Subtropical; C=
Cosmopolitan; Tn= Tropicopolit an; T=Tropical; An= Antarctic; Ne-P= Nearctic-Palearctic region; N=
North America; Ne-Tn= Nearctic-tropicopolitan; N-He= North-hemisphere; A-A= America-Africa;
Ct= Circumtropical; Tr-C= Tropical-Caribbean; A= America; Ne= Neotropical; E= Endemic;
ND= Not determined
Esperanza, Donato, and km 157 are the most similar systems in terms of
species richness/systems; Minicenote is separated from this first cluster (vase-
shaped), as well as Galeana an “aguada” type with the higher species richness
(Figure 2).

Figure 2. Simple concordance analysis (medium linkage clustering).
1) Galeana, 2) Esperanza, 3) km 157, 4) Donato, and 5) Minicenote.

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Teoría y Praxis núm. 25
We found no statistical correlation between species richness and system
area (rs = -0.07, p>0.05, n= 5), or with shoreline development (rs = 0.2143,
p0.05, n= 5).
Minicenote was the deepest system and Galeana the shallowest. The major
area and shoreline development was observed in Donato, and the lowest was
found in Minicenote (see Table 2). Shoreline values show that all surveyed sys-
tems are almost circular (Table 2).
Table 2. Morphometric and geographic data of cenotes
Site Depth
(m)
Area
(m2)
Shoreline
development
(DL)
Latitude N Longitude W
1. Galeana 9.5 5375 1.04 19° 28´ 07´´ 87° 01´ 46´´
2. Esperanza 14 12450 0.99 19° 29´ 09´´ 87° 59´ 19´´
3. Km 157 16 10925 1.01 19° 45´ 38´´ 87° 54´ 15´´
4. Donato 17 28895 1.28 19° 46´ 36´´ 87° 53´ 55´´
5. Minicenote 40 264 0.98 19° 36´ 23´´ 87° 59´ 18´´
Secchi transparency fluctuated between 1.7 m (Galeana) and 7.5 m (Esper-
anza) (Table 3). Mean water temperature was 27° C (Table 3) with a maximum
of 32.8°C (Galeana) and a minimum of 23.4°C (km 157).
Conductivity varied between 0.8 and 2.0 mS cm-1. In average, Minicenote
displayed the highest values of conductivity; the lowest occurred in Galeana,
Donato, and km 157. The pH values ranged between 6.4 and 13.0, all systems
were considered alkaline type (Table 3). The maximum value of dissolved oxy-
gen was found in Minicenote (15.3 mg l-1), and the minimum in km 157 at the
bottom (1.3 mg l-1). In average, Esperanza showed the highest values (Table 3).
In general, nitrate, nitrite, and orthophosphate measurements were low, ex-
cept the nitrate in Minicenote (Table. 3). A one-way ANOVA test showed signifi-
cative differences in nitrates (F = 61.52, p<0.001), and nitrites concentration
(F= 7.361, p<0.001) among systems. A Tukey test allowed to confirm that Mini-
cenote (the vase-shaped system) had the highest nitrates and nitrites values.

Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)
60
Orthophosphates concentrations had similar values to all the systems
(F=1.64, p> 0.05), and relative low when compared to the other nutrients val-
ues. The major value of chlorophyll a was recorded in Minicenote (maximum
value = 0.43 mg m-3), and the minimum in Donato (0.01 mg m-3). In average,
Minicenote presented the highest values, followed by Galeana, km 157, Esper-
anza, and Donato (Table 3).
Table 3. Values of environmental parameters of ve systems. 1= Galeana, 2=
Esperanza, 3= km 157, 4= Donato, and 5= Minicenote
Transparency
(m)
Water
temperature
(°C)
Dissolved
Oxygen
(mg l-1)
pH Conductivity
(mS cm-1)
N03
-
(mM)
NO2
-
(mM)
PO4
3-
(mM)
Chl-a
(mg m-3)
1 2.2 ±
0.3
27.3 ±
2.7
7.3 ±
2.7
9.0 ±
1.0
0.8 ±
0.0
4.3 ±
4.2
0.12 ±
0.05
0.007 ±
0.006
0.31 ±
0.12
2 6.5 ±
0.8
27.6 ±
1.3
9.7 ±
1.4
8.9 ±
0.6
1.5 ±
0.1
6.5 ±
4.4
0.12 ±
0.05
0.008 ±
0.017
0.04 ±
0.02
3 2.7 ±
0.5
25.9 ±
2.5
5.5 ±
2.8
9.6 ±
1.2
0.9 ±
0.0
3.7 ±
3.5
0.11 ±
0.06
0.006 ±
0.007
0.16 ±
0.07
4 5.4 ±
0.7
27.5 ±
2.0
7.4 ±
2.4
9.3 ±
0.7
0.8 ±
0.0
3.8 ±
2.8
0.08 ±
0.05
0.008 ±
0.019
0.03 ±
0.03
5 6.4 ±
1.5
25.5 ±
2.5
6.2 ±
2.7
8.4 ±
1.1
1.7 ±
0.4
27 ±
13
0.15
± 0.11
0.005 ±
0.006
0.32 ±
0.10
Water temperature was homogeneous along the water column of Esper-
anza and Minicenote (Figure 3), whereas stratification occurred in Galeana,
km 157, and Donato.

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Sampling campaings
32
30
28
26
24
22 1 2 3 4 5 6 7 8
Water temperature ºC
AB
CD
E
surf midd bott
32
30
28
26
24
22
32
30
28
26
24
22
surf midd bott
1 2 3 4 5 6 7 8
1 2 3 4 5 6 7 8
surf midd bott surf midd bott
32
30
28
26
24
22
1 2 3 4 5 6 7 8
1 2 3 4 5 6 7 8
32
30
28
26
24
22
surf midd bott
Figure 3. Vertical prole of temperature (surf=surface, midd=middle, and
bott=bottom): A) Esperanza, B) Minicenote, C) Galeana, D) Donato,
E) km 157. The number represents the sampling campaings

Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)
62
Discussion
Three aguada-type systems (Esperanza, Donato, and km 157) had similar spe-
cies richness. The fourth (Galeana) was the richest system and Minicenote was
different from the rest. The number of zooplankton species found in this study
(17-38 species) is similar to that recorded in dams and lagoons from the central
part of Mexico (Elías-Gutiérrez et al., 1997: 68) even though it is a much smaller
lake compared to the aquatic systems from the center of the country (e.g. Díaz-
Pardo et al. 1991: 70; Flores-Tena & Silva-Briano, 1995: 238; Dodson & Silva-Bri-
ano 1996: 168). A direct correlation between zooplankton species richness and
system area or littoral development, has been reported in lakes and ponds from
central and southeastern Mexico (Dodson & Silva-Briano 1996: 170; Gutiérrez-
Aguirre & Suárez-Morales 2001: 662). This correlation was not observed in the
karstic systems surveyed here. Conversely, the smaller systems had more spe-
cies. Probably, other factors such as the maturity and eutrophy level of the sys-
tems (Contreras-Espinosa et al., 1994: 62), the effect of predation (Mazumder
& Havens 1998: 1658) or refuge availability in submersed vegetation are more
important to determine the species richness in these water bodies.
On the other hand, these isolated systems can become highly diversified
with some possible endemic species (Fiers et al., 1996: 72; Elías-Gutiérrez &
Suárez-Morales 1999: 109). The high species richness in zooplankton and fish
in Galeana, in comparison with the other systems evaluated here is interesting
and shows the great biodiversity that these systems contain. The composition
and distribution of the different aquatic taxa surveyed here can be the result
of dispersion processes related to the peninsular geological history (Suárez-
Morales, 2003).
Most rotifer species found here are considered as cosmopolitan (see Table
1). In cladocerans, an important number of the total are restricted to the tropics
(39%); only two species are confirmed as cosmopolitans, and a third one is an
endemism (Elías-Gutiérrez & Suárez-Morales 1999: 107). Finally, fish species
recorded in these systems are considered as neotropical, with previous records
in the Mexican Southeast, Guatemala, Belize, and Costa Rica (Schmitter-Soto
1998: 296) (see Table 1). These results confirm the rich fauna dwelling in the
surveyed cenotes, and the need to conduct more faunistic studies.

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Temperatures recorded here are typical of tropical systems; however, a slight
thermic stratification was found in three of them (Galeana, Donato, and km
157). In Esperanza and Minicenote no thermal differences were found among
layers; both were the systems with higher Secchi values. Apparently, transpar-
ency plays an important role in determining the thermic nature of the water col-
umn: in karst systems suspended matter prevents free light penetration to the
bottom, thus favoring the formation of water strata (Navarro-Mendoza 1987:
167; Mazumder & Havens 1998: 1558, Lampert & Sommer, 2007: 223). On the
other hand, Esperanza has scarce peripheral vegetation; this condition allows a
greater water-air exchange, allowing a permanent water mixing (Torres-Orozco
& García-Calderón 1995: 130; Díaz-Arce et al., 2000: 2).
According to the area values, all studied systems can be considered as small
(less than one km2). DL values suggest a regular shoreline, typical in volca-
nic and dissolution lakes (Arredondo et al., 1983: 42; Torres-Orozco & Gar-
cia-Calderón 1995: 66). The depth of the systems surveyed is similar to other
Mexican volcanic lakes (Arredondo et al., 1983: 42), and other dissolution lakes
(Armengol & Miracle 1999: 2253).
In addition to physical differences (in the area, DL, and depth), it was pos-
sible to observe differences in conductivity and nutrients between the vase-
shape and aguada-shape. Vase-shape cenote is smaller in area, irregular, deep,
and with major conductivity and nutrients than the “aguada” type.
The higher conductivity value found in Minicenote (see Table 3), in com-
parison with the rest of the systems (F= 497.49, p< 0.001) is probably related to
a greater dissolution of rock, since this cenote is vase-shaped, and pores or frac-
ture in the walls are not sealed, allowing a major dissolution of the calcareous
wall. This would also favor also a greater input of ground water and minerals
into the system (Flores-Nava et al. 1989: 227; Díaz-Arce et al. 2000: 3). In addi-
tion, Navarro-Mendoza (1987: 161) suggested that depth can be another factor
related to high conductivity in karst systems, because the ground water currents
in contact with them allows the input of ions already dissolved.
Conductivity values (from 0.8 to 1.7 mS cm-1) suggest the presence of dis-
solved carbon dioxide (CO2) and bicarbonates (HCO3+) into the water (Lampert
& Sommer, 2007: 34), which is characteristic of the freshwater systems from
Yucatan Peninsula (Alcocer & Escobar 1996: 62). The basic pH values were

Aquatic biodiversity in cenotes from the Yucatan Peninsula (Quintana Roo, Mexico)
64
present in all systems, which is expected, according to the karstic nature of the
systems studied (Alcocer & Escobar 1996: 65).
Except for Minicenote, all the systems showed the same range of nutrient
concentrations. Values found there was lower than in lagoons or dams from in
the central region of Mexico (Tavera & Castillo 2000: 107), but similar to that
found in other karstic systems from the Yucatan Peninsula (Herrera-Silveira et
al., 1998: 1349). The higher nitrates and nitrites concentrations in Minicenote
could be related to its vase-shaped and small area, with a smaller trophogenic
zone, compared to the volume of the system, so the intake of nutrients by phy-
toplankton could be limited. According to Contreras et al. (1994: 61) all values
of chlorophyll obtained in these cenotes are characteristic of oligotrophic sys-
tems. Therefore, the relative low Secchi transparency (mainly in Galeana) was
not related to chlorophyll a, but to other organic and inorganic suspended ma-
terials such as solids or even mineral precipitation that could reduce its values
(Armengol & Miracle 1999: 2257).
Contrary to other published works, this result suggests that each of these
systems is unique with their characteristics, even when they are close to each
other. A general approach on their species richness and limnology should take
into this account this wide range of variability.
Acknowledgements
We thank G. de J. Pérez-Cal, A. Maya, R. Calderón, C. Quintal-Lizama, I. Castellanos-
Osorio, A. Kotov from ECOSUR-Chetumal, for assisting in the collection of samples at
cenotes in Quintana Roo. Some water samples were analyzed by A. Zavala ECOSUR-
Chetumal. A. Kotov, and Silvia Aviles kindly helped in the identification of zooplankton
and necton species. X. Armengol (U. de Valencia) and E. Suárez-Morales (ECOSUR)
provided all the facilities to visit and to analyze data in the University of Valencia,
Spain. We are grateful to E. Suárez-Morales, R. Velázquez Tagle and two anonymous
reviewers for their helpful comments on the original manuscript. This work is part of
the graduate project by A. Cervantes to study the cenotes in Quintana Roo, and forms
part of a CONACYT and SISIERRA grant (No. 20000635).

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