Yuniel Méndez-Martínez1*

Mariuxi F. Cevallos-Chevez

Yenny G. Torres-Navarrete

Edilmar Cortés-Jacinto

Jorge L. Ramírez-de la Ribera

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

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.

Facultad

Ciencias Agropecuarias,

Universidad

Técnica

Estatal de Quevedo (UTEQ), Quevedo, Los Ríos, Ecuador.

Programa

Acuicultura,

Centro

Investigaciones

Biológicas del Noroeste (CIBNOR), La Paz, BCS, México.

Centro

Estudio

Producción Animal,

Universidad

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

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

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

) 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

), high signicance, signicant contribution of the

terms and low coefcients of indeterminacy (1- r

), 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

Biological indicators

Weight,

Length,

Head thickness,

Body thickness,

Tail thickness,

Condition fac-

tor

Hepatoso-matic

index

Gonado-somatic

index

1 168.19

21.25

5.60

9.26

6.26

1.88

1.40

14.51

2 266.29

26.90

7.25

12.34

8.53

1.37

0.91

8.52

3 179.88

24.15

6.51

11.14

6.50

1.30

1.67

13.9

4 290.93

28.11

7.35

13.24

7.51

1.39

1.38

8.49

5 169.20

23.14

6.18

10.23

6.73

1.38

1.24

15.54

6 225.40

26.24

6.94

11.96

7.33

1.24

1.59

10.86

± 7.51 0.39 0.09 0.21 0.13 0.05 0.05 0.62

0.001 0.01 0.001 0.002 0.002 0.001 0.001 0.003

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

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

+ 0.1708x + 2.1588

R² = 0.4781

y = -6E-05x

+ 0.07x + 12.421

R² = 0.7346

0 50 100 150 200 250 300 350 400 450

y = -0.0001x

+ 0.0716x + 16.26

R² = 0.1194

y = -0.0002x

+ 0.2148x - 12.7

R² = 0.8511

0 50 100 150 200 250 300 350 400 450

Length (cm)

y = -0.0003x

+ 0.1857x + 1.9253

R² = 0.9154

y = -0.0001x

+ 0.1134x + 8.4753

R² = 0.8182

0 50 100 150 200 250 300 350 400 450

Females Males

Weight (g)

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

± P Females Males SE

± P

Glucose 231.33

311.00

79.00

5.26 0.001 222.22

185.33

6.9 0.002

Cholesterol 169.17

128.67

241.33

3.77 0.002 164.89 161.56 19.92 0.23

Triglycerides 75.00

66.00

77.00

0.94 0.01 77.22

68.11

0.52 0.05

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.

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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