© The Authors, 2021, Published by the Universidad del Zulia*Corresponding author: ymendezm@uteq.edu.ec
Yuniel Méndez-Martínez1*
Mariuxi F. Cevallos-Chevez
1
Yenny G. Torres-Navarrete
1
Edilmar Cortés-Jacinto
2
Jorge L. Ramírez-de la Ribera
3
Rev. Fac. Agron. (LUZ). 2022, 39(1): e223910
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v39.n1.10
Animal Production
Associate editor: Dr. Rosa Razz
Keywords:
Cholesterol
Condition factor
Freshwater sh
Gonadosomatic index
Glucose
Effect of habitat and sex on biological indicators and blood biochemistry of Andinoacara
rivulatus in the province Los Ríos - Ecuador
Efecto del hábitat y el sexo sobre indicadores biológicos y la bioquímica sanguínea de Andinoacara
rivulatus en la provincia Los Ríos - Ecuador
Efeito do habitat e do sexo nos indicadores biológicos e na bioquímica do sangue na Andinoacara
rivulatus provincia Los Ríos - Equador.
Abstract
The effect of the habitat and sex on biological indicators and
blood biochemistry of Andinoacara rivulatus in the province of Los
Ríos - Ecuador was evaluated. Were captured 60 specimens for each
zone (180 total), the eight of the animals, length, thickness of the
head, tail and the factor were evaluated. Blood glucose, cholesterol
and triglyceride indicators were determined. A completely
randomized design was used with factorial arrangement (three x
two), three habitats and two sexes. A double classication analysis
of variance was applied considering the habitat and sex as sources
of variation. The results showed the highest morphometric values
for males and varied with the habitat, except in the body indices,
what were the females. The functional relationship between length
and weight was established using quadratic regression equations,
with greater signicance for males with r
2
greater than 0.70.
No interaction between zones and sex was shown for the blood
indicators studied. The results showed interaction between the
habitat locations and sex for the different morphometric indicators
evaluated. The biochemical indicators of the blood were conditioned
by the habitat.
1
Facultad
de
Ciencias Agropecuarias,
Universidad
Técnica
Estatal de Quevedo (UTEQ), Quevedo, Los Ríos, Ecuador.
2
Programa
de
Acuicultura,
Centro
de
Investigaciones
Biológicas del Noroeste (CIBNOR), La Paz, BCS, México.
3
Centro
de
Estudio
de
Producción Animal,
Universidad
de
Granma (UDG), Bayamo, Granma, Cuba.
Received: 07-09-2021
Accepted: 19-10-2021
Published: 03-01-2022
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2022, 39(1): e223910. January - March. ISSN 2477-9407.2-6 |
Resumen
Se evaluó el efecto del habitat y el sexo sobre indicadores
biológicos y bioquímica sanguínea de Andinoacara rivulatus en la
provincia de Los Ríos, Ecuador. Se capturaron 60 ejemplares por cada
zona (180 total). Se evaluaron los indicadores peso de los animales,
longitud, grosor de la cabeza, cuerpo, la cola y factor de condición.
Se determinaron los indicadores sanguíneos glucosa, colesterol y
triglicéridos. Se empleó un diseño completamente aleatorizado con
arreglo factorial tres x dos, tres habitat y dos sexos. Se le aplicó
un análisis de varianza de clasicación doble considerando la zona
de habitad y el sexo como fuentes de variación. Los resultados
mostraron los mayores valores morfométricos para los machos y
variaron con la localidad, excepto para los índices corporales, que
fueron en las hembras. Se estableció la relación funcional entre el
peso y la longitud mediante ecuaciones de regresión cuadráticas,
con mayor signicación para los machos con r
2
superiores a 0.70. No
se mostró interacción entre las zonas y el sexo para los indicadores
de la sangre estudiados. Los resultados mostraron interacción entre
las localidades de hábitat y el sexo para los diferentes indicadores
morfométricos evaluados. Los indicadores bioquímicos de la sangre
estuvieron condicionados por la localidad.
Palabras clave: colesterol, factor de condición, glucosa, índice
gonadosomático, peces de agua dulce.
Resumo
Foi avaliado o efeito do habitad e do sexo nos indicadores
biológicos e na bioquímica do sangue de Andinoacara rivulatus na
província de Los Ríos, Equador. 60 espécimes foram capturados
para cada zona (180 total). Foram avaliados o peso dos animais,
comprimento, espessura da cabeça, corpo, cauda e fator de condição.
Foram determinados os indicadores sanguíneos de glicose, colesterol
e triglicerídeos. O delineamento experimental foi inteiramente
casualizado, com arranjo fatorial três x dois, três localidades e dois
sexos. Uma dupla classicação de análise de variância foi aplicada
considerando a área de habitat e sexo como fontes de variação. Os
resultados mostraram os maiores valores morfométricos para os
machos e variaram com a localidade, excetp nos indices corporais,
quais eram as fêmeas. A relação funcional entre peso e comprimento
foi estabelecida por meio de equações de regressão quadrática,
com maior signicância para o sexo masculino com r2 maior que
0.70. Nenhuma interação entre zonas e sexo foi mostrada para os
indicadores sanguíneos estudados. Os resultados mostraram interação
entre a localização do habitat e o sexo para os diferentes indicadores
morfométricos avaliados. Os indicadores bioquímicos do sangue
foram condicionados pela localidade.
Palavras-chave: colesterol, fator de condição, peixes de água doce,
índice gonadossomático, glicose.
Introduction
Ecuador is considered an important reserve of native freshwater
sh in the southeastern tropical Pacic, where 951 native species
are recognized (Barriga, 2012; FAO, 2019). On the other hand, most
Neotropical cichlids occupy habitats within slow-owing lakes, rivers,
and streams. The Andinoacara rivulatus (Cichlidae: Andinoacara)
is a native sh of the Pacic basin, covering its distribution from
Panama to Peru, in addition to being of great ornamental importance,
it is also a source of food and work for the populations that have these
economic resources (Revelo and Laaz, 2012; Jiménez Prado et al.,
2015).
The A. rivulatus is a species that lives in slow, shallow waters
that are close to the shores, they feed near the rocks with vegetation,
it also lives in the lower course of the rivers, with soft waters (turbid)
or clear with a muddy background. Jiménez Prado et al. (2015), state
that the height of the body is 2.6 cm of the total length, the length
of the head is 2.8 cm of the total length. It has a tall body, laterally
compressed and has four to ve spots. Both males have a hump, and
females have electric blue lines in the chin area and a black spot on
the body (Jiménez Prado et al., 2015).
The phenotypic plasticity of sh, evaluated by morphological
measurements, is higher than in the rest of vertebrates and this
variation can be attributed in part to the inuence of environmental
parameters (González et al., 2016; Ahmadniaye Motlagh et al., 2020).
Physiological differences between gender are related to primary
and secondary sexual characteristics and their adaptations, result
of different strategies used for reproductive success, with marked
differences in blood parameters between females and males due
to a high metabolism in males. Although according to the report
by Bastardo et al. (2004) that females have higher values in blood
parameters. The variation of the results may be due to the different
conditions in which the organisms were maintained in each study
(Enayat Gholampour et al., 2020). The study of blood chemistry and
morphometry are currently of great interest in determining the health
status and metabolic balance in wild sh, since several intrinsic and
extrinsic factors can inuence blood parameters and morphometry in
sh.
The determination of the morphometric values and the blood
chemistry of the A. rivulatus in the province of these rivers will help
to generate strategies for the conservation of the species and the
lotic environments of the region. Due to the above, the objective of
this work was to evaluate the effect of habitat and sex on biological
indicators and blood biochemistry of A. rivulatus in the province Los
Ríos, Ecuador.
Materials and methods
Location
This investigation was carried out in three areas of the Los Ríos
province, Fumisa, Camarones area, geographically at coordinates
0º 43’ 16’S and 79º 27’ W; Pajarito precinct belonging to Mocache
canton 1º 8’ 03.92’’ S, 79º 29’ 07.8’’ W and Quevedo, the route of the
River 1º 2’ 30’ S and 79º 28’ 30’ W (gure 1). The climatic conditions
are shown in table 1.
Ethics statement
The study was performed in strict accordance with the Standard
Operation Procedures (SOPs) for Use of Experimental Animals of
UTEQ (Quevedo, Los Ríos, Ecuador). The experimental protocol and
procedures are approved by the Institutional Animal Care and Use
Committee of UTEQ.
Procedure
This research was developed during the month of December-2019;
One of the native freshwater species that are most commercialized in
the cantons of Quevedo, Mocache and Fumisa of the Rivers Province,
A. rivulatus was identied; Through artisanal shing, 60 specimens
were captured for each area (180 total), once captured, sexing was
carried out taking into account the morphological characteristics
(Nugra et al., 2018; Rodríguez Pulido et al., 2018). Males represented
47.78 percent of the total and 52.22 %.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Méndez-Martínez et al. Rev. Fac. Agron. (LUZ). 2022, 39(1): e2239103-6 |
Figure 1. Map of sampling areas
Table 1. Annual climatic characteristics of three areas of province
Los Ríos - Ecuador.
Zone Temperature
°C
Precipitation
mm
Weather
Fumisa
21 - 31 2000 - 3500 Tropical
Mocache
20 - 30 1626 - 3500 Tropical semi-humid
Quevedo
23 - 31 1750 - 2500 Tropical humid
Biology indicators
The sh were weighed individually on a digital scale ± 0.01 g
(PE 3600 Mettler-Toledo, Columbus, Ohio, USA), the length was
determined with the help of a tape measure (Truper, 3m-Fh, Distrito
Federal, MX) measuring from the tip of the mouth to the n of the
tail. To measure the thickness of the head, body and tail, a digital
vernier caliper (GT-MA15 Gester, ± 0.001 mm, Xiamen, CN) was
used.
The Condition Factor was determined according to the following
formula (Moreno et al., 2019):
-Condition Factor = (live weight / total length
3
) x 100
The animals were dissected, which allowed the macroscopic
classication of the gonad according to Holden and Raitt (1975). The
following indices were subsequently calculated:
-Gonadosomatic index = (gonad weight / body weight) x100
-Hepatosomatic index = (liver weight / body weight) x 100
Biochemistry in blood plasma
1 mL of blood was extracted from the hemal arch by puncturing
the caudal artery, for which three mL syringes were used (Bio-In,
Guayaquil, EC); which were placed in capillary tubes (Isolab,
Laborgeräte GmbH, Eschau, DE) with heparinized inner surfaces,
then the samples were centrifuged (Gemmy, PLC-05, Taipei, TW) at
1200 rpm for 10 min to obtain serum plasma and later determine the
levels of glucose, cholesterol and triglycerides (Méndez Martínez et
al., 2021). For which kit reagents were applied (Human liquicolor,
Wiesbaden, DE); and they were incubated for 25 min at 37 oC
(Trinder, 1965). Readings were performed on a spectrophotometer
(SunostIk, SBA-733 Plus, Kunshan Road, CN) at ABS: 510 nm for
glucose, 500 nm for cholesterol and triglycerides. The analyzes were
carried out in triplicate.
Experimental design and statistical analysis
A completely randomized design was used with a three x two
factorial arrangement, three localities Mocache (one), Fumisa (two)
and Quevedo (three) and sexes females (one) and male (two).
An analysis of variance (p≤0.05) of classication double was
applied considering the area of habitat and sex as sources of variation.
The Kolmogorov–Smirnov (p≤0.05) and Bartlett (p≤0.05) tests were
applied prior to the analysis of variance (ANOVA). The difference
between the means was quantied using the Tukey (p≤0.05).
Regression equations were established to establish the functional
relationship between length and weight. To select the expressions of
best t, the following elements were considered: high coefcient of
determination (r
2
), high signicance, signicant contribution of the
terms and low coefcients of indeterminacy (1- r
2
), standard errors of
the terms, standard errors of estimation and mean square of the error.
For data analysis, SPSS® 21.0 software (Inc., Chicago, IL USA) was
used.
Results and discussion
The results reected that the interaction of the locality and sex
showed the highest weight values of the animals for treatment four
290.93 ± 28.3 g, Fumisa locality x males, (p<0.05), with differences
compared to the rest. Emphasizing that no differences were shown
between treatments one, three and ve (table 2).
Table 2. Biological indicators of the Andinoacara rivulatus according to habitat and sex interaction
Interaction of
habitat and sex
1
Biological indicators
Weight,
g
Length,
cm
Head thickness,
cm
Body thickness,
cm
Tail thickness,
cm
Condition fac-
tor
Hepatoso-matic
index
Gonado-somatic
index
1 168.19
d
21.25
e
5.60
d
9.26
f
6.26
d
1.88
a
1.40
c
14.51
b
2 266.29
b
26.90
b
7.25
a
12.34
b
8.53
a
1.37
b
0.91
f
8.52
e
3 179.88
d
24.15
c
6.51
b
11.14
d
6.50
c
1.30
c
1.67
a
13.9
c
4 290.93
a
28.11
a
7.35
a
13.24
a
7.51
b
1.39
b
1.38
d
8.49
e
5 169.20
d
23.14
d
6.18
c
10.23
e
6.73
c
1.38
b
1.24
e
15.54
a
6 225.40
c
26.24
b
6.94
b
11.96
c
7.33
b
1.24
c
1.59
b
10.86
d
SE
2
± 7.51 0.39 0.09 0.21 0.13 0.05 0.05 0.62
P
0.001 0.01 0.001 0.002 0.002 0.001 0.001 0.003
1
Habitat x Sex interaction (1: Mocache x females, 2: Mochache x males, 3: Fumisa x females, 4: Fumisa x males, 5: Quevedo x females, and 6: Quevedo x males). 2 SE ±,
standard error of the Habitat x Sex interaction.
abcde
Values with unusual letters differ at p<0.05, Tukey.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2022, 39(1): e223910. January - March. ISSN 2477-9407.4-6 |
Regarding length, something similar occurred and treatment four
reected the highest length, with differences (p<0.05) compared to
the rest. Treatments two and six did not reect a difference between
them, and without with the rest. Body thickness showed the highest
value for the fourth interaction, which differs from the rest, the
lowest value was reected in the rst treatment (table 2). In the case
of the thickness of the tail, interaction two presented the highest
value and differed from the rest. Interactions four and six, as well
as three and ve did not show differences between them, and the
lowest of the values was reected for number one.
The condition factor showed the highest value for the rst
interaction, which differed from the rest. The number two, four and
ve did not present differences between them, something similar
happened for three and six, which were in turn the lowest values.
The results reported according to the effect of the locality-
sex interaction (table 2), results that are corroborated by what
was proposed by Turán et al. (2006), where he afrms that the
introduction of a species of sh leads to a high adaptation to
different geographies, which leads to phenotypic variations
with respect to those that gave rise to it (Fagbuaro et al., 2015;
Solomon et al., 2015). The previously explained is conrmed when
evaluating the remaining indicators. For the thickness of the head,
the highest values were reected in treatments two and four with
differences (p<0.05) compared to the rest. The lower thickness of
the head was shown for the rst interaction and differences between
three and six were not reected. In all these cases the highest
values correspond to males and differences are established between
localities. Studies carried out in Ecuador showed results similar
to those of this research, in terms of morphometric characteristics
such as: thickness of the head, body, tail and the condition factor
(González, 2017). This is because the different parts of the body
vary depending on environmental conditions and gender. Different
authors highlight the variation of the morphometric characteristics
of this species depending on the locality and sex (Solomon et al.,
2015; González et al., 2016).
Hepatosomatic index (table 3) showed the highest value for
treatment three (Fumisa x females), with differences (p<0.05) with
respect to the rest, and the lowest value was reected by treatment
two. For the gonadosomatic index the highest content was shown
by treatment ve, reecting differences (p<0.05) with respect to
the rest. The lowest appeared for treatment two, which reects
less precipitation than treatment three. In this sense, Kerguelen
and Atencio (2015), reported that, in tropical aquatic systems,
the hydrological patterns and the transport of nutrients generated
by the rainy season are denitive for the selection of the optimal
reproduction time.
This is related to the amount of rainfall depending on the
location. Andrade and Braga (2005) afrm that the intensity of
the rain is the most important factor in the synchronization of the
reproduction of tropical sh, therefore coinciding the reproductive
period with the rainy season may be an evolutionary strategy. The
sh only have to nd favorable habitat conditions for spawning and
recruitment (Jiménez et al., 2016).
On the other hand, a study carried out in Ecuador in Eremophilus
mutisii reected that females presented higher hepatosomatic
and gonadosomatic indices (Moreno et al. 2019). Similar to what
happened in this work. This nding agrees with the records of
Landines et al. (2017). In this way, it is to be assumed that after
starting the gonadal maturation processes, the female must allocate a
greater proportion of energy and nutrients towards the reproductive
function to support a greater growth of the gonad (ovary) than the
male.
The relationship between weight and length in the Mocache
locality (gure 2a), reected a coefcient above 0.70, with high
signicance of the terms of the equation for the case of males.
However, for females, although there are differences in the model,
the coefcient of determination is not high (0.48).
For the habitat of Fumisa and Quevedo (gure 2b and 2c) the
functional relationship between length and weight was shown
by a quadratic regression equation with a high coefcient and
signicance of the terms of the equation. This did not happen for
the females in Fumisa, where the terms of the equation did not show
signicance, and the coefcient of determination was low.
In the town of Quevedo, the relationship between length and
weight was adjusted to a quadratic regression equation for both
males and females, with high coefcients of determination in both
cases (gure 2), and high signicance of the terms of the equation.
Moreno et al. (2019), reported results that differ from those of
this research, when evaluating the total length-weight relationship
of Eremophilus mutisii in growing females and males, where
it showed potential equations with r
2
greater than 0.88. These
authors reported that the allometric coefcient of the length-weight
relationship was numerically higher for maturing females than for
males. The allometric coefcient was signicant for both maturing
females and males (p<0.05). This is due to the fact that the increase
in weight as a function of size is more accentuated in females than
in males, especially during gonadal maturation. This difference can
be explained to a large extent by the differences that exist in the
weight of the gonads, where the gonadosomatic index was higher
for maturing females when compared to that of males, an issue that
did not occur in this experiment.
y = -0.0003x
2
+ 0.1708x + 2.1588
R² = 0.4781
y = -6E-05x
2
+ 0.07x + 12.421
R² = 0.7346
0
5
10
15
20
25
30
35
40
0 50 100 150 200 250 300 350 400 450
A
y = -0.0001x
2
+ 0.0716x + 16.26
R² = 0.1194
y = -0.0002x
2
+ 0.2148x - 12.7
R² = 0.8511
0
5
10
15
20
25
30
35
40
0 50 100 150 200 250 300 350 400 450
Length (cm)
B
y = -0.0003x
2
+ 0.1857x + 1.9253
R² = 0.9154
y = -0.0001x
2
+ 0.1134x + 8.4753
R² = 0.8182
0
5
10
15
20
25
30
35
40
0 50 100 150 200 250 300 350 400 450
Females Males
Weight (g)
C
Figure 2. Length and weight relationship in males and females
of Andinoacara rivulatus from three habitats a)
Mocache, b) Fumisa and c) Quevedo.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Méndez-Martínez et al. Rev. Fac. Agron. (LUZ). 2022, 39(1): e2239105-6 |
A study in Ecuador when evaluating the length-weight
relationship of the main sh species (Andinoacara rivulatus,
Hoplias microlepis, Rhamdia cinerascens, Brycon sp, Leporinus
ecuadoriensis, Pseudocurimata sp) of commercial interest in
the Abras of Mantequilla wetland, Ecuador (Ochoa et al., 2016);
reported potential equations for all species, but Ichthyoelephas
humeralis, A. rivulatus and Pseudocurimata sp. with negative
allometric growth, while Hoplias microlepis, Brycon sp. and
Leporinus ecuadoriensis. Differences between growth types can
be related to many factors, such as differences in sample sizes,
specimen size ranges, genetic differences between groups of species,
and local environmental conditions. Furthermore, parameters of the
length-weight relationship may differ not only between species
but also between populations of the same species, considering
that the growth coefcient depends on genetic, nutritional and
environmental differences.
Other studies report similar results, and report that different
factors may inuence this behavior, such as: sample range,
seasonality, habitat, gonad maturity, stomach fullness, and
development phase, among others (Sharma et al., 2015).
The biochemical indicators of the blood did not show differences
when interacting the locality with sex, for which the values of the
effect of the localities and the effect of sex were shown. For glucose
the highest value was reected by Fumisa, followed by Mocache.
The lowest was shown by Quevedo, and differences appear between
the three locations. When evaluating the sexes, the males showed
the highest amount of glucose (table 3).
Table 3. Indicators of the blood biochemistry in males and females of Andinoacara rivulatus from three habitats.
Indicators,
mg.dL
-1
Habitat Sex
Mocache Fumisa Quevedo SE
1
± P Females Males SE
1
± P
Glucose 231.33
b
311.00
a
79.00
c
5.26 0.001 222.22
a
185.33
b
6.9 0.002
Cholesterol 169.17
b
128.67
c
241.33
a
3.77 0.002 164.89 161.56 19.92 0.23
Triglycerides 75.00
a
66.00
b
77.00
a
0.94 0.01 77.22
a
68.11
b
0.52 0.05
1
SE ±, standard error of the Sex x Habitat interaction. abcdeValues with unusual letters differ at p<0.05, Tukey.
For cholesterol, the highest value was reected in the town of
Quevedo and the lowest was Fumisa, with signicant differences
between them. The sexes did not show differences when analyzing
this compound. For the triglycerides Mocache and Quevedo they do
not differ from each other, and the lowest value appears in Fumisa.
When analyzing the sexes, females present a higher amount of
triglycerides than males (table 3).
This was veried with the different behaviors depending on
the localities. Castellanos et al. (2003), reported values lower than
those of this investigation for the localities of Mocache and Fumisa
in terms of glucose. These authors evaluated the yamú species, the
values showed a range between 131.1 and 147.6 mg.dL
-1
. In the
case of cholesterol, the results were higher, the values were between
299.5 and 365.9 mg.dL
-1
.
The study of these parameters in native sh is scarce, so it is
important to analyze these hematological components such as red
blood cells, leukocytes and platelets, as well as biochemical such
as proteins, triglycerides, minerals, enzymes. Serum biochemistry
in sh can estimate the animal’s response to different factors such
as: stress, diseases, nutritional imbalances. The disorders that can
occur from these factors depend on the species, age, physiological
phase, the concentration of cortisol, glucose and cholesterol, and
can be affected by hypoxic stress, this is altered by animal density,
therefore, These parameters are fundamental to know the state of
the animal, to recognize the failures that appear in the system due to
internal elements such as water quality, and external elements such
as management (Vargas, 2019).
Other studies on hematological parameters of Brycon
amazonicus (Bryconidae) and Astronotus ocellatus breeders found
glucose and cholesterol levels of 60.2-64.39 mg.dL.
1
and 253.4
mg.dL
-1
concentrations considered normal in the range of 14.7-
155.3 mg.dL
-1
and 78 at 397 mg.dL
-1
according to the literature.
Results lower than those reported in this investigation (311 mg.dL
-1
for glucose) and higher than 241 mg.dL
-1
for cholesterol. Such
variations of these hematological parameters can be attributed to
intra- and interspecic factors such as sex, age, gonadal maturation,
genetic variation, habitat, eating habit, climate, and stress caused
during handling (Ahmadniaye Motlagh et al., 2020).
Conclusions
There is interaction between habitat locations and sex for
different morphometric indicators evaluated. The males presented
greater size, weight and thickness in the studied measurements of
the body, but the females presented the highest corporal indices.
The biochemical indicators were conditioned by the habitat and
without interaction.
Acknowledgment
Our thanks to Don Quirola, president of the Bella Vista artisanal
shing association for his support in catching the organisms.
We thank Wendy Hidalgo for technical support in processing
the samples. The research was supported by the Universidad
Técnica Estatal de Quevedo (UTEQ). Support project for the call
FOCYCYT-7th, project PFOC7-48-2020.
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