Contemporary Engineering Sciences, Vol. 11, 2018, no. 59, 2931 - 2948
HIKARI Ltd, www.m-hikari.com
https://doi.org/10.12988/ces.2018.86300
Structure of the Zooplanktonic Community in
a Tropical Dam (Betania, Colombia) with High
Environmental Tension
Paula Martínez-Silva1, Jorge Leonardo Muñoz-Yustres2
and Natalia Rodríguez Charry3
1 Universitary Coorporation of Huila
Environmental Engineering Program, Colombia
2 Universitary Coorporation of Huila
Environmental Engineering Program, Colombia
3 Universitary Coorporation of Huila
Environmental Engineering Program, Colombia
Copyright © 2018 Paula Martínez-Silva et al. This article is distributed under the Creative
Commons Attribution License, which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Abstract
The Betania Dam is a strategic ecosystem of the department of Huila in Colombia,
whose goods and services include the generation of hydroelectric energy and the
production of red tilapia (Oreochromis mossambicus) and silver tilapia
(Oreochromis niloticus) in intensive systems. These activities generate conditions
in the flow of matter and energy through the introduction of nutrients and foreign
species that cause responses in the hydrobiological communities. In this research,
zooplankton samples collected every two months for eighteen months were
analyzed qualitatively and quantitatively at three sampling stations of the reservoir
corresponding to three hydro morphological zones to determine the species
present in the reservoir and the relative abundance of each one in this period.
Biological diversity indexes, Kruskal Wallis tests were applied and oxygen and
pH profiles were obtained throughout the day. Seven new zooplankton records
were found for the reservoir. In addition, temporal variations were observed in the
abundance of the species and some relationships between nutrient abundance and
climatic conditions were discussed with the diversity and abundance patterns of
2932 Paula Martínez-Silva et al.
zooplankton where some of them reflect the typical behavior of a eutrophic
system.
Keywords: Lentic ecosystems, Eutrophication, Diversity, Fish farming, biological
components of water
Introduction Studies on the use of water are indispensable in any place of the world, especially
in water bodies that are part of strategic ecosystems which productivity and
stability may be affected by human activities and climatic phenomenon (Aguirre
et al., 2008;) [1].
The dam of Betania, is one of the strategic ecosystems in the Department of Huila
- Colombia for the goods and services it offers such as fish production and electric
power, artisanal fishing, water sports and tourism. Its filling began in 1986 and is
formed by the Magdalena and Yaguara Rivers, with an initial depth of 91 meters
and an area of approximately 7,400 hectares (Betania, 2002) [8].
The reservoir is divided into three longitudinal zoning: the riverine area,
characterized by its elongated shape and high capacity for transporting materials;
the transition zone, and the lacustrine area characterized by sedimentation and
high penetration of light (Thornton, 1981) [53]. In addition, it presents vertical
zoning with chemical and thermal stratification; a superficial area (Epilimnion)
with high values of productivity during daylight hours and a deep-water area
(hypolimnion) that can fluctuate between hypoxic and anoxic conditions (Beisner,
2001 [6]; Betania, 2002) [8].
For some years, the dam has been in an eutrophication process, caused by the
contribution of nutrients from different sources, such as fertilizers and pesticides
used in surrounding agriculture and the fishing activity (Martínez, 2015) [34]. On
the other hand, the dynamic of the reservoir as well as its dendritic shape and a
fifty-day hydraulic retention time provides water blockage, allowing the
succession of hydrobiological communities and the generation of anoxic
conditions in the bottom layers affecting the dam biota and the water quality
(Roldán, 1992 [46]; Betania, 2002 [8]; Beisner, 2001 [6] and Sommer, 1999) [17].
Studies of biological communities and physico-chemical characteristics of water
allow us to understand the water quality. The zooplankton, as well as all other
components, has an important role in the interaction of the ecosystem as a link in
the food chain and as active participant in the transfer of energy and the nutrients
cycle (Conde et al, 2004 [9]; Gallo et al, 2009) [20]. In addition, it can be used as
an indicator of the water quality since the richness and abundance of some species
reflect responses from this community to variations in nutrient concentrations,
alkalinity, temperature, and others (García, 2001 [21]; Ruokolainen et al, 2009
[48]; Paturej et al, 2016 [37]; García-Chicote et al, 2017) [22].
There are three studies about the composition of the community of zooplankton in
the dam of Betania: a scientific article published by Herrera and Guillot in 1999
[28] and two theses published by Vélez in 1989 [55] and Largo in 2007 [30]. This
research allows to update knowledge about the composition of the community of
Structure of the zooplanktonic community … 2933
zooplankton in this dam and to propose explanations of the richness and
abundance of these organisms due to activities developed in the dam as well as the
climatic phenomena of La Niña and the El Niño.
Methodology
This research is qualitative and quantitative, non-experimental type of inductive
method. The study area corresponds to three stations in Betania Dam (Figure 1)
located in the Riverine area (Station 1), the transition zone (Station 2) and the
lacustrine area (Station 3), as shown in Figure 1. At each station 9 samplings were
done every two months for eighteen months.
Figure 1. Map of the study area and sampling points
For the physic-chemical parameters, the electric conductivity was measured at
each station in a superficial manner through YSI 30 digitial conductimeter, the
2934 Paula Martínez-Silva et al.
total hardness through the range of colors as well as disk transparency through
Secchi disk, according to Ruiz (2002) [47]. Laboratory analysis were made for
Total suspended solids, alkalinity and ammonium in a certified laboratory
according to the Standard methods (APHA-AWWA-WEF, 1999) [2].
Furthermore, each sampling station has a multiparametric buoy which emits data
in real time of dissolved oxygen, pH and water temperature every 15 minutes
through a GPRS system.
Zooplankton samples were analyzed qualitatively using an optical microscope
(Olympus CX31) with Magurran’s (2004) [32] technique of species curve and
Infante’s (1980) [29], Pennak’s (1989) [39], Flössner’s (2000) [18], Turner’s
(1990) [54] and Gaviria and Aranguren’s (2007) [23] taxonomic keys. For
quantification, Sedgwick-Rafter-type cameras were used implementing random
subsamples to get a number close to 100 individuals of the most abundant species
according (Wetzel and Likens, 1991 [58]; Paggi and Paggi, 1995) [10].
For data analysis, Simpson’s dominance, Margalef’s Diversity, Shannon-Wiener’s
heterogeneity (H') and J evenness rates were estimated (Washington, 1984 [57];
Magurran, 2004 [32]; Gotellli and Colwell, 2001) [25]. Kruskal Wallis’s analysis
for k means was applied to verify whether there is statistical variability between
the abundances of species amongst months and amongst stations (Gomez-
Marquez et al., 2013 [24]; Aranguren and Monroy, 2014 [3]; Badii et al., 2014)
[5]. Physic-chemical variables were interpreted by using descriptive statistics:
average and degree of dispersion (standard deviation and coefficient of variation)
for each variable (Guisande et al. 2006 [27]; Aranguren and Monroy, 2014) [3].
Oxygen and pH profiles were built in the three stations throughout the day using
multiparametric buoys data to observe the behavior of the O2-CO2 system in the
dam (Roldán, 1992 [46]; Herrera and Guillot, 1999 [28]; Paturej, et al; 2016) [37].
Results
Table 1. Species of Zooplankton reported for Betania Dam in different research
projects PHYLLUM SPECIES 1999 2007 2017
ROTÍFEROS
Conochilus dossuarius X X
Conochilus sp. X X
Lacinularia sp. X X
Epiphanes sp. X X
Filinia pejleri
X
Filinia termalis X X
Hexarthra sp. X X X
Testudinella patina X X
Asplanchna sp.
X X
Structure of the zooplanktonic community … 2935
Table 1. (Continued): Species of Zooplankton reported for Betania Dam in
different research projects
Anuraeopsis fissa X X
Anuraeopsis navicula X X
Brachionus ampiceros X X
Brachionus angularis X X
Brachionus
calyciflorus
X X X
Brachionus falcatus X X X
Brachionus
havanaensis
X X X
Brachionus
quadridentatus
X X
Brachionus sp. X X X
Brachionus urceolaris X X
Brachionus caudatus
X X
Brachionus patulus
X X
Keratella americana X X X
Keratella tropica X X X
Platyias quadricornis X X
Epiphanes sp. X X
Lepadella sp. X X
Polyarthra vulgaris X X X
Trichocera pusilla X X
Trichocera similis X X X
Trichocera sp.
X X
Lecane quadridentata
X
Lecane bulla X X
Lecane levistyla X X
Lecane sp. X X
2936 Paula Martínez-Silva et al.
Table 1. (Continued): Species of Zooplankton reported for Betania Dam in
different research projects
CLADOCEROS
Bosmina longirostris
X X
Alona sp. X
Ceriodaphnia cornuta X X
Ceriodaphnia silvestrii
X X
Daphnia sp.
X
Moina sp. X
X
X
Moina minuta X X
Diaphanosoma birgei
X
Diaphanosoma
brachyurum X X
COPÉPODOS
Artodiaptomus
dorsalis X X
Nauplio Calanoide
X X
Nauplio Cyclopoidae
X
Mesocyclops sp.
X
Termocyclops
decipiens X X X
OSTRÁCODOS Strandesia sp.
X
48 species of zooplankton were found, corresponding to the Rotifer class (34
pecies), Cladocera (8 species), Copepods (5 species) and Ostracods (1 species). Of
the registered species, 7 had not been reported in the three previous studies (See
Table 1).
Structure of the zooplanktonic community … 2937
Figure 2. Abundance of zooplankton groups in the sampling months
As it can be seen in Figure 2, during the first seven samplings, the most abundant
group were the copepods, followed by the rotifers. For October and December
2016, the rotifers were more abundant than the copepods. In all the quantitative
analyzes, the most abundant species were Keratella americana, Brachionus
falcatus and Polyarthra sp. (Rotifers), Bosmina longirostris (Cladocerans) and
Mesocyclops sp. (Copepods).
The Kruskal Wallis analysis for stations yielded a p-value of 0.005 indicating that
there are differences between the sampling months at a significance level of 0,01
and a p-value of 0.03 significant at 0,05 level, showing statistically significant
differences between the variances of the stations. The sampling station with the
greatest abundance for the four groups is the transition zone and the station with
the lowest numbers of abundance is the lacustrine zone.
Table 2. Physicochemical data of Betania Dam during the nine sampling months
Sampling
Date
STATIO
N
DISSOLVED
OXYGEN
pH
SUPERFICI
AL WATER
WATE
R T°
AMONI
UM
ALCALINI
TY
HARDN
ESS
TRANSPARE
NCY
DEPT
H
MARCH
2015
1 5,49 7,75 27 0,01 50 65 60 6
2 3,94 7,77 27,2 0,04 30 45 100 41
3 3,98 8,21 26,2 0,02 30 55 110 39
MAY
2015
1 5,27 8,29 22,37 0,16 140 130 20 8
2 4,65 9,3 25,58 0,01 40 55 110 29
3 6,08 8,97 26,44 0,01 40 40 100 39
AUGUST
2015
1 8,45 7,9 20,65 0,05 90 60 20 2,3
2 6,86 7,21 23,86 0,01 30 50 120 39
2938 Paula Martínez-Silva et al.
Table 2. (Continued): Physicochemical data of Betania Dam during the nine
sampling months
3 6,91 7,59 24,36 0,01 35 55 120 40
NOVEMBER 2015
1 6,3 8,42 26,51 0,02 45 55 70 5
2 3,75 7,58 27,85 0,01 35 40 120 33
3 7,16 7,67 28,97 0,01 35 50 110 41
MARCH 2016
1 3,43 7,18 23,09 0,21 140 40 20 1,5
2 3,11 7,9 27,91 0,16 45 33 100 26
3 3,23 7,98 30 0,01 40 45 100 32
APRIL 2016
1 5,1 7,86 27,08 0,06 100 50 50 4
2 3,35 7,22 27,5 0,18 40 55 120 40
3 1,73 6,94 26,44 0,01 45 55 130 37
JUNE 2016
1 5,03 6,78 21,67 0,14 110 150 10 1,3
2 5,42 7,93 25,02 0,21 60 40 120 28
3 4,1 7,6 27,81 0,11 55 60 130 37
OCTOBER 2016
1 7,27 7,31 22,5 0,12 175 150 15 12
2 6,65 7,63 27,8 0,01 40 45 120 43
3 7,15 6,7 27,9 0.01 45 45 120 45
DECEMBER 2016
1 7,23 7,43 22,65 0,01 80 70 30 4
2 9,61 8,37 30,78 0,01 65 80 110 42
3 5,19 7,15 26,48 0,01 55 75 80 46
In Betania dam, transparency, alkalinity and hardness showed the highest
temporal variability during the study with variation coefficients (VC) of 41.3%,
38.2% and 30.9% respectively (Table 2). The change in these variables is related
to the variations in depth and climatic conditions generated by the meteorological
phenomena of El Niño and La Niña, and the organic waste from the Quimbo dam
which was built twelve kilometers upstream of Betania dam.
Structure of the zooplanktonic community … 2939
Figure 3. Results of ecological indexes of richness, equitativity, dominance and
diversity
Figure 3 synthesizes the results obtained by applying the ecological indices,
showing very low diversity (Margalef and Shannon) and the presence of dominant
species in all the samplings. Spearman's correlation analysis yielded values that
are not statistically significant.
Figure 4. Behavior of pH and Dissolved Oxygen during the day
Figure 4 shows the behavior of D.O and pH reflect conditions of a eutrophic
system, reaching the highest concentrations of D.O at noon as well as a highest
pH, changing completely at night.
Discussion
In this study, a total of 48 species of zooplankton are recorded. Of the 23 species
2940 Paula Martínez-Silva et al.
registered by Herrera and Guillot in 1999 [28], Alona sp. is not found in 2007 or
in this study. Most of the species recorded in this study correspond to the group of
rotifers, and within this group, the most abundant genera were Brachionus,
Keratella and Polyarthra. There is no pattern regarding the tolerance of these
genera to environmental conditions since they can bear both oligotrophic to
eutrophic environments and when filtered they adapt themselves to any condition
as long as there is organic matter to filter (Roldan, 1992 [46]; Kirk, 2000) [35].
According to Pennak (1989) [39] and Ramírez (1987) [41], the genus Brachionus
has been reported as an indicator of eutrophic conditions due to its resistance to
high pH and high concentrations of carbonates, sulfates, chlorides, and calcium.
Similarly, Keratella species have rapid rates of growth and manage to colonize
different habitats since they are opportunistic organisms that adjust to fluctuations
and environmental changes (Rodríguez and Matsumura, 2000 [44]; Esparcia et al.,
2001 [13]); other species of rotifers can be found in any environment independent
of the trophic level (Esteves, 1988) [14]. The species Bosmina longirostris
(Cladocerans) and Mesocyclops sp. (Copepods) were also abundant species in this
research and have been reported by other authors as species that tolerate eutrophic
conditions (Nogueira et al., 2008) [36].
The registration of new species (Table 1) can be the consecuence of lack of
sampling efforts and also fish farming activities in which the fingerlings are
transported from other regions of the country in water tanks bringing
microorganisms not found previously in the dam. Once these new species get to
Betania, they find ideal conditions for their development and establishment
(Merriman and Kirk, 2000) [35]. Some of these species had not been registered in
Betania before, although they have been registered in other regions of Colombia,
such as Lecane, Filinia, Diaphanosoma, Mesocyclops and Strandesia (Guevera et
al., 2009 [26]; Villabona-González et al, 2015) [56].
The genus Mesocyclops thrives well in tropical waters and is known for its
function as a biocontroller of transmitting agents for dengue (Aedes aegypti) and
malaria (Anopheles sp.) (Ferrari and Bradley, 1994) [16]. It can be adapted to
anoxia conditions and feeds on larvae of mosquitoes being available throughout
the year in Betania; since 1984 there are reports of Mesocyclops in Colombia
according to Gaviria and Aranguren (2007) [23] when it was found for the first
time in artificial containers in Anapoina. Since then it has been established that it
is a fugitive species that has achieved a wide geographic distribution in the
Neotropic (Reid and Saunders, 1986) [42]. It is important to note that this is the
first record in the department of Huila, where it has probably found ideal
conditions for its existence as well as a good amount of food. During the research,
the Cladoceran Alona sp. reported by Herrera and Guillot in 1999 [28] was not
evidenced. This may be happening due to competition with the species Bosmina
longirostris, one of the most abundant in this research. Some studies have
previously suggested that the existence of competition between these two species
can reach the point that either one of them can temporarily exclude the other
(Dumont et al., 1994 [11]; Nogueira et al., 2008) [36].
Structure of the zooplanktonic community … 2941
The Strandesia genus, on the other hand, is a genus of ostracods reported in
several places in Colombia, including the Magdalena River basin and some areas
of the Eastern Mountain Range (Roessler, 1988 [45]). However, it had not been
registered in Betania in previous studies. Strandesia has the capacity to lay
drought-resistant eggs, so this dam, with problems of eutrophication and periods
of high environmental stress such as the El Niño phenomenon does not represent
any problem for colonization and the establishment of this Ostracode (Fernando,
1984 [15]).
The copepods were the most abundant group in the first seven samplings, and the
rotifers in the last two (Figure 2). This change is mainly due to the fact that the
first seven samplings coincided with El Niño phenomenon characterized by high
temperatures in the air, complete cessation of rainfall, decrease in water depth,
increase of suspended solids and decrease in dissolved oxygen levels, conditions
for which copepods are more resistant (Pennak, 1989 [39]; Galassi et al., 2009)
[19]. On the other hand, the months of October and December 2016 coincided
with the end of this phenomenon and the beginning of La Niña phenomenon,
accompanied by rains, and increase in the flow allowing the reestablishment of
the dam level, the decrease in solids dissolved, the increase of dissolved oxygen
and depth. According to Roldan (1992) [46] and Nogueira et al. (2008) [36], these
are optimal conditions for the proliferation of rotifers.
Kruskal Wallis statistical analysis shows statiscal evidence about the spatial and
temporal variation of zooplanktonic abundance of species, which may be
influenced not only by the characteristics of each hydromorphological zone of the
dam but also by the climatological phenomenon of El Niño and La Niña.
Diversity indexes show us that the stations with the greatest diversity are the
transition and lacustrine ones, partly because they have stable physical and
chemical conditions and slow currents. This allows the plankton communities to
establish themselves for a longer period and present patterns of ecological
succession giving way to the increase in diversity (Villabona-González et al.,
2015) [56]. On the other hand, the riverine station has the lowest abundance and
diversity of zooplankton because it has fast currents, a constant water exchange
and a lower depth, which prevents the establishment of plankton communities for
long periods of time (Aranguren-Riaño et al., 2011) [4]. For the months of March
and April 2016, the company operating the reservoir closed the floodgates
reducing the flow and preventing the replacement of water, which, added to the
high temperatures produced by the El Niño phenomenon, generated a decrease in
the depth of the reservoir, a high accumulation of dissolved solids and a flowering
phenomenon of microalgae such as Microcystis and Ceratium, according to
Martínez et al. (2016) [33]. This caused a high mortality of fish and a variation in
the zooplankton communities due to competition in the food since, when fish
died, the predators of copepods and cladocerans of larger size decreased (Roldan,
1992 [46]; Ruokolainen et al., 2009) [48].
It is interesting to note how changes in the physicochemical, morphometric and
hydrological conditions of the stations generate important variations in the zoo-
2942 Paula Martínez-Silva et al.
plankton community highlighting that the alkalinity data agree with those of a
system with high productivity. This coincides with high abundances of groups of
phytoplankton that, as previously mentioned, present flowering episodes during
the periods of greatest drought in the reservoir (Aranguren and Monroy, 2014 [3]).
This also agrees with the behavior of oxygen and pH throughout the day, where it
is seen that oxygen increases in sunlight hours as a result of photosynthetic
activity and decreases at night due to an increase in the release of oxygen. CO2
(see figure 4). This reflects the typical condition of a eutrophic reservoir, with
positive peaks of oxygen and pH during the day because of photosynthesis and an
opposite situation during the night as a result of algae cellular respiration,
according to Roldan (1992) [46] and Esteves (1988) [14]. This can be clearly
evidenced in the months of lower rainfall and closure of the reservoir floodgates,
between March and April 2016, according to EMGESA (2016) [12]. Likewise, in
these months the lowest levels of dissolved oxygen and the highest levels of
ammonium are present, especially in the river and transition stations. In all the
months and seasons the hardness data correspond to productive waters (Roldan,
1992) [46]. However, much remains to be understood and it is essential to
continue conducting research to understand the structure of these communities in
the upper basin of the Magdalena River and to deepen the consequences that these
activities have on these ecosystems, such as agriculture, fish farming and the
construction of hydroelectric plants, among others (Villabona-González et al.,
2015) [56].
Conclusions
The most abundant species of zooplankton recorded during the study allow to
conclude, as in other studies, that the reservoir is in a eutrophic state, caused
mainly by the nutrient inputs of the surrounding crops and the fish farming
activities that take place in the interior of the reservoir.
The transport of fingerlings from other regions of the country to the Betania
Reservoir is probably the main reason new species are registered in the reservoir,
which can cause an imbalance in the zooplanktonic community due to the
invasion of non-native species. It is necessary to continue with studies on the
Betania plankton to chronologically track the evolution of this body of water to
provide the necessary information to begin to find solutions to the problems that
occur as a consequence of the eutrophication process.
The zooplankton community is more diverse than the communities of other
tropical reservoirs with high environmental stress, although the most abundant
species coincide with species resistant to eutrophic conditions. As for the three
seasons, the highest diversity and abundance are recorded in the transition station
corresponding to the transition station; the lowest diversity and abundance
corresponds to the riverine area.
Acknowledgements. The authors want to express our sincere gratitude to the
Limnology Laboratory of the Corporación Universitaria del Huila - CORHUILA,
Structure of the zooplanktonic community … 2943
for laboratory facilities and supplies throughout the research and to the ACUAPEZCDT for the sampling and contribution of cartography. Additionally,
our gratitude for each of the researchers and technicians who made this research
possible.
Conflict of Interests: The authors declare that there is no conflict of interests
regarding the publication of this paper.
References
[1] D. J. Aguirre Sanchez, N. R. Aguirre, O. C. Quintero, Evaluación de la
calidad del agua a través de los protistas en la quebrada La Ayurá en
Envigado (Antioquia), Producción mas Limpia, 3 (2008), no 1.
[2] Apha-Awwa-Wef, Standard Methods for the Examination of Water and
Wastewater, 20th. Washington D.C. American Public Health Association,
1999.
[3] N. J. Aranguren, J. D. Moroy-Gonzales, Respuestas del zooplancton en un
sistema tropical (embalse la chapa, Colombia) con alta tensión
ambiental, Acta Biológica Colombiana, 19 (2014), no. 2, 281-290.
https://doi.org/10.15446/abc.v19n2.38095
[4] N. Aranguren-Riaño, C. Guisande, R. Ospina, Factors Controlling
Crustacean Zooplankton Species Richness in Neotropical Lakes, J. Plankton
research, 33 (2011), no. 8, 1295-1303.
https://doi.org/10.1093/plankt/fbr028
[5] M. H. Badii, A. Guillen, O. P. Serrato, J. J. Garnica, Correlación No
Paramétrica y su Aplicación en la Investigaciones Científica, Revista Daena
(International Journal of Good Conscience), 9 (2014), no. 2.
[6] B. Beisner, Plankton Community Structure in Fluctuating Environments and
the Role of Productivity, Oikos, 95 (2001), no. 3, 496-510.
https://doi.org/10.1034/j.1600-0706.2001.950315.x
[7] L. C. L. Benavides, L. A. C. Pinilla, R. R. Serrezuela, W. F. R. Serrezuela,
Extraction in Laboratory of Heavy Metals Through Rhizofiltration using the
Plant Zea Mays (maize), International Journal of Applied Environmental
Sciences, 13 (2018), no. 1, 9-26.
[8] S.A. Betania, Plan de Manejo Ambiental de Betania en Operación, Informe
final 76, 2002.
2944 Paula Martínez-Silva et al.
[9] J. M. Conde, E. Ramos, R. Morales, El zooplancton como integrante de la
estructura trófica de los ecosistemas lénticos, Ecosistemas, 13 (2004), no. 2,
23-29.
[10] S.J. De Paggi, J.C. Paggi, Determinación de la Abundancia y Biomasa
Zooplanctónica. En: Lopreto E, Tell G, editors. Ecosistemas de Aguas
Continentales, Metodologías para su Estudio, Vol. 1, Universidad Nacional
de Salta, Argentina: Ediciones Sur., 315-324, 1995.
[11] H. J Dumont, J. Green, H. Masundire, Studies on the Ecology of Tropical
Zooplankton, Reprinted by Hydrobiología, 1994.
[12] EMGESA. 2016. Reporte de información hidrológica y de operación del
Embalse Betania.
[13] A. Esparcia, X. Armengol, M. R. Miracle, Relación de la distribución de los
rotíferos con la de los principales factores físicos y químicos en la laguna de
La Cruz, Limneica, 20 (2001), no. 2, 305-320.
[14] F A. Esteves, Considerações sobre a aplicação da tipologia de lagos
temperados a lagos tropicais, Acta Limnol. Bras., 2 (1988), 3-28.
[15] C.H. Fernando, Ecology and Biogeography in Sri Lanka. Dr W. Junk
Publishers. Boston, Lancaster, 1984.
[16] F. Ferrari, B. Bradley, Ecology and Morphology of Copepods, Proceedings
of the 5th International Conference in Copepoda, Baltimore USA, Reprinted
from Hydrobiologia, (1993), 292-293.
[17] S. Flöder U. Sommer Diversity in Planktonic Communities: An
Experimental Test of the Intermediate Disturbance Hypothesis, Limnology
and Oceanography, 44 (1999), no. 4, 1114-1119.
https://doi.org/10.4319/lo.1999.44.4.1114
[18] D. Flössner, Die Haplopoda und Cladocera (Ohne Bosminidae)
Mitteleuropas, Netherlands: Backhuys Publishers, 2000.
[19] M. D. Galassi, H. R. Rony, J. Reid, Diversity, ecology and evolution of
groundwater copepods, Freshwater Biology, 54 (2009), 691-708.
https://doi.org/10.1111/j.1365-2427.2009.02185.x
[20] L. Gallo, N. Aguirre, J. Palacio, J. Ramírez, Zooplancton (rotífera y
microcrustacea) y su relación con los cambios del nivel del agua en la
Ciénaga de Ayapel. Córdoba, Colombia, Caldasia, 31 (2009), no. 2, 339-
353.
Structure of the zooplanktonic community … 2945
[21] M. García, Las Comunidades De Zooplancton De Los Embalses Españoles,
Ecosistemas. Año X, 2001.
[22] J. García-Chicote, J. Armengol, C. Rojo, Zooplankton abundance: A
neglected key element in the evaluation of reservoir water quality,
Limnologica, 69 (2017), 46-54. https://doi.org/10.1016/j.limno.2017.11.004
[23] S. Gaviria, N. Aranguren, Especies de vida libre de la subclase Copepoda
(Arthropoda, Crustacea) en aguas continentales de Colombia, Biota
Colombiana, 8 (2007), no. 1, 53-6.
[24] J. L. Gómez, B. Peña, J. L. Guzmán, V. Gallardo, Composición, abundancia
del zooplancton y calidad de agua en un microreservorio en el estado de
Morelos, Hidrobiológica, 23 (2013), no. 2, 227-240.
[25] N. J. Gotellli, R. K. Colwell, Quantifying biodiversity: procedures and
pitfalls in measurement and comparison of species richness, Ecol. Lett., 4
(2001), 379-391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
[26] G. Guevara, P. Lozano, G. Reinoso, F. Villa, Horizontal and seasonal
patterns of tropical zooplankton from the eutrophic Prado reservoir in
Colombia, Limnología- Ecology and Management of Inland Waters, 39
(2009), 128-139. https://doi.org/10.1016/j.limno.2008.03.001
[27] C. A. Guisande, A. Barreiro, I. Maneiro, I. Riveiro, A. Vergara, A.
Vaamonde, Tratamiento De Datos. España: Editorial Díaz de Santos, 2006.
[28] Y. Herrera, G. Guillot, Composición taxonómica del zooplancton del
embalse de Betania, departamento del Huila, Colombia, Acta Biológica
Colombia, 4 (1991), no. 1.
[29] A. Infante, Los rotíferos del lago de Valencia, Acta Cient. Venezola, 3
(1980), 30-47.
[30] C.R. Largo Urrea, Estudio Del Zooplancton En Zonas De Producción
Piscícola En El Embalse De Betania (Huila - Colombia), PhD Tesis,
Universidad Jorge Tadeo Lozano. Bogotá D.C, Colombia, 2007.
[31] V. A. R. Losada, E. P. Bonilla, L. A. C. Pinilla, R. R. Serrezuela, Removal
of Chromium in Wastewater from Tanneries Applying Bioremediation with
Algae, Orange Peels and Citrus Pectin, Contemporary Engineering
Sciences, 11 (2018), no. 9, 433 – 449.
https://doi.org/10.12988/ces.2018.8235
2946 Paula Martínez-Silva et al.
[32] A. E. Magurran, Measuring Biological Diversity, Blackwell Publishing,
2004.
[33] P. Martínez, J. F. Delgado, J. L. Muñoz, Diversidad de Géneros del
Fitoplancton del embalse de Betania–Huila y su importancia como
bioindicadores- Diversity of Phytoplankton genera of the Betania-Huila
reservoir and its importance as bioindicators, Revista Científica, 2 (2016),
no, 25, 241-251. https://doi.org/10.14483//udistrital.jour.rc.2016.25.a8
[34] P. Martínez, Variación espacio temporal de microalgas acuáticas del
embalse de Betania - Huila y su relación con la calidad del agua,
Intropica: Revista del Instituto de Investigaciones Tropicales, 10 (2015),
no. 1, 11-19. https://doi.org/10.21676/23897864.1642
[35] J. Merriman, J. Kirk, Temporal patterns of resource limitation in natural
populations of rotifers, Ecology, 81 (2000), no. 1, 141-149.
https://doi.org/10.2307/177140
[36] M. G. Nogueira, C. P. Y. De Reis, T. Y. Britto, Zooplankton assemblages
(Copepoda and Cladocera) in a cascade of reservoirs of a large tropical
river, Limnetica, 27 (2008), no. 1, 151-170.
[37] E. Paturej, A. Gutkowska, J. Koszałka, M. Bowszys, Effect of
physicochemical parameters on zooplankton in the brackish, coastal Vistula
Lagoon, Oceanologia, 59 (2017), no. 1, 49-56.
https://doi.org/10.1016/j.oceano.2016.08.001
[38] N. A. P. Pedraza, J. I. P. Montealegre, R. R. Serrezuela, Feasibility Analysis
for Creating a Metrology Laboratory Serving the Agribusiness and
Hydrocarbons in the Department of Huila, Colombia, International Journal
of Applied Engineering Research, 13 (2018), no. 6, 3373-3378.
[39] R.W. Pennak, Fresh-Water Invertebrates of the United States: Protozoa to
Mollusca, Wiley-Interscience, New York, 1989.
[40] L. A. C. Pinilla, R. R. Serrezuela, J. David, S. Díaz, M. F. Martínez, L. C. L.
Benavides, Natural Reserves of Civil Society as Strategic Ecosystems: Case
Study Meremberg, International Journal of Applied Environmental
Sciences, 12 (2017), no. 6, 1203-1213.
[41] J. J. Ramírez, Contribución al conocimiento de las condiciones limnologícas
de la laguna del Parque Norte, Medellín, Actual. Biol., 16 (1987), no. 59,
12-30.
Structure of the zooplanktonic community … 2947
[42] W. J. Reid, J. F. Saunders, The Distribution of Mesocyclops Aspericornis
(Von Daday) in South America, Journal of Crustacean Biology, 6 (1986),
no. 4, 820-824. https://doi.org/10.1163/193724086x00604
[43] R. Rodríguez Serrezuela, L. A. Carvajal Pinilla, Ecological determinants of
forest to the abundance of Lutzomyia longiflocosa in Tello, Colombia,
International Journal of Ecology, 2015 (2015), 1-7.
https://doi.org/10.1155/2015/580718
[44] M. P. Rodríguez, T. Matsumura, Variation of density, species composition
and dominance of rotifers at a shallow tropical reservoir (Broa Reservoir,
SP, Brazil) in a short scale time, Revista Brasileira de Biología, 60 (2000),
no. 1, 1-9. https://doi.org/10.1590/s0034-71082000000100002
[45] E. W. Roessler, Estudios taxonómicos, ontogenéticos, ecológicos y
etológicos sobre los Ostracodos de agua dulce en Colombia, VI. Estudio
Taxonómico del género Strandesia STUHLMANN 1888, (OSTRACODA,
PODOCOPIDA, CYPRIDIDAE) parte I. Aspectos morfológicos de una
nueva especie del género Strandesia, Caldasia, 15 (1988), 71-75.
[46] G. Roldán, Fundamentos De Limnología Neotropical, Medellín (Colombia),
Editorial Universidad de Antioquia 1, 1992.
[47] E. Ruíz, Métodos para el Estudio de las Características FísicoQuímicas del
Agua, En: Rueda G, editor, Manual de Métodos en Limnología. Bogotá:
ACL- Limnos, 2002.
[48] L. Ruokolainen, E. Ranta, V. Kaitala, M.Fowler, Community Stability
Under Different Correlation Structures of Species Environmental
Responses, J. Theor. Biol., 261 (2009), no. 3, 379-387.
https://doi.org/10.1016/j.jtbi.2009.08.010
[49] N. C. Sánchez, R. R. Serrezuela, A. M. N. Ramos, J. L. A. Trujillo, Real
Process Characteristic Capacity Weight in the Product 500 Grams in a Rice
Mill, International Journal of Applied Engineering Research, 12 (2017), no.
21, 11588-11597.
[50] N. C. Sánchez, A. L. P. Salazar, A. M. N. Ramos, Y. M. Calderón, R. R.
Serrezuela, Optimization of the Paddy Rice Husking Process, Increasing the
useful Life of the Rollers in Florhuila Plant Campoalegre Mills,
International Journal of Applied Engineering Research, 13 (2018), no. 6,
3343-3349.
[51] R. R. Serrezuela, N. C. Sánchez, J. B. R. Zarta, D. L. Ardila, A. L. P.
Salazar, Case Study of Energy Management Model in the Threshing System
2948 Paula Martínez-Silva et al.
for the Production of White Rice, International Journal of Applied
Engineering Research, 12 (2017), no. 19, 8245-8251.
[52] P. M. Silva, J. L. M. Yustres, L. C. L. Benavides, R. R. Serrezuela,
Composition of the Phytoplankton Community in the First Stages of the
Quimbo Dam Life Cycle in Huila–Colombia, Contemporary Engineering
Sciences, 11 (2018), no. 19, 907-924.
https://doi.org/10.12988/ces.2018.8265
[53] J.M. Thornton, Disulphide bridges in globular proteins, Journal of
Molecular Biology, 151 (1981), no. 2, 261-287.
https://doi.org/10.1016/0022-2836(81)90515-5
[54] P.N. Turner, The rotifer genus Platyias Arring In the Neotropics, Acta
Limnol. Brasil., 3 (1990), 741-756.
[55] N. Vélez, Análisis Regional, Hidrodinámico Y Limnológico Del Embalse De
Betania, Huila-Colombia, Trabajo de grado Departamento Biología,
Universidad Nacional de Colombia, 1989.
[56] S. Villabona-González, J. Ramírez-Restrepo, J. Palacio-Baena, B. C. Costa,
Respuesta de la biomasa zooplanctónica a los gradientes de estado trófico y
precipitación de un embalse tropical, Rev, Acad. Colomb. Cienc, Ex. Fis.
Nat., 39 (2015), no. 152, 374-388. https://doi.org/10.18257/raccefyn.203
[57] H. Washington, Diversity, Biotic and Similarity Indices - a Review with
Special Relevance to Aquatic Ecosystems, Water Res., 18 (1984), no. 6,
653-694.
[58] R. Wetzel, G. Likens, Limnological Analyses, 2 Ed., USA: Springer Verlag,
1991. https://doi.org/10.1007/978-1-4757-4098-1
Received: July 15, 2018; Published: August 6, 2018
