Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49

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Comparative Biochemistry and Physiology, Part C

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Interference of heavy metals present in the water of the Lagoa Tramandaí/ T

RS on the carbohydrate metabolism of the GURI Sea Catfish (G. genidens)
and Bay whiff (C. spilopterus)
⁎
Brunna Castilhos Petersena, , Tássia Huff Tietböhlb, Alessandra Marquezea
a
Unilasalle-Universidade Lassalle, Mestrado de Avaliação em Impactos Ambientais, Av. Victor Barreto, 2288, CEP 92010-000 Canoas, RS, Brazil
b
Unilasalle-Universidade Lassalle, Bolsista Laboratório de Fisiologia Comparada, Av. Victor Barreto, 2288, CEP 92010-000 Canoas, RS, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: This study aims to evaluate the contamination of the water of Lagoa Tramandaí on Genidens genidens and
Lagoa Tramandaí Citharichthys spilopterus residents of Lagoa Tramandaí, a region susceptible to environmental damage due to the
Guri Sea Catfish release of domestic sewage from the municipalities bathed by the lagoon. Thereby, the biota suffers the inter-
Bay whiff ference of heavy metals, affecting their behavior and the metabolism of these individuals. The hepatic and
Carbohydrate metabolism
muscular glycogen, glucose and plasma lactate of these species were analyzed, as well as the presence of heavy
Metals
metals in lagoon water. When the species were analyzed separately with their controls, both mobilized more
glycogen than the control and presented increased glucose and lactate, which is characteristic of animals con-
taminated by heavy metals. When compared with each other, they showed differences regarding carbohydrate
metabolism. It was observed that the Guri Sea Catfish suffers more influence of heavy metals than the Bay whiff.
Thus, we can conclude that the water contaminated with heavy metals of this lagoon interferes in the carbo-
hydrate metabolism of both species of fish.

1. Introduction range dissipation means. On the ground, however, such compounds,

The state of Rio Grande do Sul has 3 hydrographic regions: coastal,
Uruguay and Guaíba (SEMA, 2016). In the coastal region, Lagoa Tra-
mandaí stands out as it bathes the municipalities of Imbé, Osório and
Tramandaí; the lagoon has a connection with the sea through Barra de
Tramandaí with a channel that is 1.5 m long and 100 m wide
(Tramandaí, 2016). It receives water and fine sediments such as clay
and silt from rivers and lagoons located to the north, through the Rio
Tramandaí.
The Bacia do Rio Tramandaí water quality, analyzed by
Taramandahy Project (Castro and Rocha, 2016), qualified it as class 1
for brackish water and according to Anama (2015) the basin has large
concentrations of metals in the water, sediment and fishes.
According to Lissner and Gruber (2009), the north coastal waters,
especially Lagoa Tramandaí, have been, in the most part, contaminated
by household wastewater, agrochemicals and pesticides from local
agriculture. The basin water contaminants are several, among which
are worth mentioning metals and agrochemicals applied to the soil,
which are leached to the surface and groundwater. Expected levels of
contaminants in the water are a few portions, because water is a long-
especially heavy metals, tend to settle and remain longer, acting as a
storage where metals accumulate, and may return to the water column
at any moment. (Castro and Mello, 2013). The Lagoa Tramandaí has
heavy metals accumulated on the sediments, of which mercury was the
only one that presented values above the reference limit required by
CONAMA 420/09 (Castro and Mello, 2013). Heavy metals can be in-
serted into natural environments (running water) through the discharge
of domestic and industrial wastewater. Such elements, when dumped in
the environment do not decompose nor become less toxic; instead, they
become even more toxic than their initial form once they are converted
by natural processes (Sisinno and Oliveira-Filho, 2013).
In recent years the world population has seen an increase in en-
vironmental pollution and thus, in investments to try to reverse the
situation. Several environments are contaminated with heavy metals
and these enter the fish food chain ending up in human consumption.
Thus, the quality and safety of fish for human consumption has become
increasingly important since metals are related to the development of
certain types of cancer (Li et al., 2017b).
Li et al. (2017a) have reported in their paper that due to the large
amounts of heavy metals used in recent years, it has become impossible

⁎
Corresponding author.
E-mail address: brunnapetersen@gmail.com (B.C. Petersen).

https://doi.org/10.1016/j.cbpc.2019.01.007
Received 29 November 2018; Received in revised form 27 January 2019; Accepted 30 January 2019
Available online 10 February 2019
1532-0456/ © 2019 Elsevier Inc. All rights reserved.
B.C. Petersen, et al.
to reduce/eliminate them from the environment. In addition, high le-
vels of metals in the body can cause “metabolic, biochemical, and
physiological changes and inhibit the synthesis of proteins and nucleic
acids” (Li et al., 2017a). Fish tissues produce an antioxidant defense
system which protects animals from oxidative stress caused by metals;
however, it does not eliminate the presence of this contaminant from
the tissues of individuals (Li et al., 2017a).
According to Silveira (2013) the species of fishes of Lagoa Tra-
mandaí like Guri Sea Catfish (Genidens genidens) and Bay whiff (Ci-
tharichthys spilopterus) are resident estuarine (RE), that is, they are
species that live in the estuary. The Guri Sea Catfish spends all stages of
its life in this environment, has the habit of living at the bottom of the
estuary, where there is sand and mud (Fischer et al., 2011) and has
carnivorous habits (Deus et al., 2009). The Bay whiff has a benthic
habit (Fischer et al., 2011), has a carnivorous feeding behaviour and
ends up ingesting portions of sediment with the food.
The organic matter consumed by animals is composed of proteins,
lipids and carbohydrates, all of which are large molecules that the body
cannot absorb. They need to be digested to monosaccharides to be
absorbed by the blood (Smith et al., 2007). The amount of food that
exceeds consumption will be stored as fat, glycogen and protein in
different tissues. Hepatic glycogen is responsible for maintaining gly-
cemia while the muscle serves as storage of glucose for muscle cells and
is released at times of intense muscle activity (Silveira et al., 2009).
According to the study by Petersen and Damin (2016) of fish from
Lagoa Tramandaí, the presence of heavy metals such as arsenic was
found to be higher than allowed in some species of fish. In addition to
the arsenic analysis, metals cadmium (Cd), lead (Pb) and mercury (Hg)
were also analyzed. In all the analyses, we had the presence of heavy
metals, however in lower concentrations. In this paper, the average
concentrations of arsenic in the tissues of the Guri Sea Catfish was
2.032 μg kg−1, and the maximum residue concentration allowed by the
Ministry of Agriculture, Livestock and Supply (MAPA) was
1.000 μg kg−1 (Brasil, 2012). For the other metals the values obtained
were below this maximum residue limit.
Therefore, the purpose of this study is to analyze the metabolic
profile of carbohydrates of the different species of fish, Guri Sea Catfish
(Genidens genidens) and Bay whiff (Citharichthys spilopterus), living in
Lagoa Tramandaí.
2. Materials and methods
The water samples and the specimens studied come from Lagoa
Tramandaí on the north coast of Rio Grande do Sul (Fig. 1). These
species were chosen because they are residents of Lagoa Tramandaí,
that is, they spend all their life stages in this ecosystem, and therefore
they are exposed to all the contaminants and stressors present in the
environment.
For the study, 3 samplings were performed, 1 per month. In each
collection there were 5 samples of adult fish of each species. The col-
lections were carried out from January to March 2016, seeking a period
with constant temperatures without large oscillations in order to avoid
interfering in the metabolism of the individuals.
At the moment of fish catching, the water temperature was mea-
sured using a mercury thermometer, the pH with the Kasvi portable pH
meter and also the dissolved oxygen (DO) with the portable oxygen
meter Kaito Electronics Inc.
2.1. Fish capture and sampling
The fishes (n = 15) were caught through artisanal fishing, being
caught with a cast net and driven slowly. The fish were anaesthetized
with MS222 (300 mg/L, Argent Redmond, WA, USA). Blood samples
were then collected from the caudal vessels using heparinized syringes.
Following this, the fish were killed by means of spinal section, and liver
and muscle tissue was removed, weighed, placed on ice, frozen in liquid
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Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49
nitrogen and stored at −20 °C for later analysis. The blood samples
mentioned above were then centrifuged (3000 ×g, 10 min), and the
plasma was stored at −25 °C for later analysis.
2.2. Blood and tissue analyses
2.2.1. Glucose measurement
Plasma glucose was analyzed by a colorimetric test (Kit Vis Labtest,
MG, Brazil).
2.2.2. Lactate measurement
Plasma lactate was analyzed by a colorimetric test (Kit Vis
Interteck/Katal— SP, Brazil).
2.2.3. Glycogen measurement
Liver and muscle tissues were homogenized, and the glycogen
concentration was determined according to Van Handel (1965).
All the procedures involving animals were conducted in compliance
with the guidelines approved by the Committee on Research Ethics and
Animal Welfare of the Universidade de Passo Fundo (CEUA-UPF,
number 035/2016), and authorized from the Ministry of the
Environment (MMA) through the Sistema de Autorização e Informação
da Biodiversidade (SISBIO) for scientific activities (number 52354-2).
2.3. Water analyses
One liter of water was collected at the place where fishing was being
carried out at Lagoa Tramandaí, at approximately 15 cm deep. The
water was stored in plastic bottles acidified with nitric acid (HNO3),
identified and maintained on ice to retain their properties until the
analyses were carried out by the Eurofins/ALAC laboratory. The ana-
lysis methods of metals arsenic, cadmium, lead and chromium in the
water were Standard Methods 22nd - Method 3120 B [PNT003-AB] and
for Mercury Standard Methods 22 nd - Method 3112 B [PNT002-AB].
Limits of detection (LD) and limits of quantification (LQ) of the method
are in Table 1.
These screenings were carried out to obtain an overview of the
metal content (As, Cd, Cr, Pb and Hg) present in the study environment.
2.4. Statistics
The mean ± S.E.M. of each group was calculated and analyzed
using the Graph Pad InStat 3.00 statistical package (GraphPadSoftware,
San Diego, California, USA). The glucose, lactate and glycogen values of
all groups in all sampling moments were compared by two-way ana-
lyses of variance (ANOVA), followed by Tukey's test. Statistical sig-
nificance was accepted at p < 0.05. A Hartley test was carried out to
verify the homogeneity of variance, and normality was tested using the
Kolmogorov–Smirnov test. Log-transformation was performed when
necessary, while non-transformed data are shown in the figures.
3. Results
3.1. Water analyses
Data from the physio-chemical analyses showed that there were no
large variations among the parameters analyzed in the collection per-
iods. The pH average was 7.54, the dissolved oxygen was 3.46 mg/L
and the water temperature was 25.6 °C. The analyses of heavy metals in
the water of Lagoa Tramandaí were carried out in March 2016, with
values of 0.4 μg/L of arsenic (As), < 0.1 μg/L of cadmium (Cd), 0.6 μg/
L lead (Pb), 2 μg/L chromium (Cr) and no value for mercury (Hg).
3.2. Fish carbohydrate metabolism analyses
As there were no studies in the literature related to carbohydrate
B.C. Petersen, et al. Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49

Fig. 1. Highlight for the Lagoa Tramandaí.

(Source: Based on Machado et al. (2015).)

Table 1 These species were chosen because they had some characteristics in
Limits of detection (LD) and Limits of quantification (LQ) of metals analyzed in common with the species collected in this study. G. genidens and
the water. Rhamdia quelen have similar characteristics, such as inhabiting the
Ar Cd Pb Cr Mg bottom, belonging to the same class (Siluriformes), diets composed
mainly of smaller fish and crustaceans, besides being considered second
LD 0.00005 0.00005 0.00015 0.0005 0.00005 or third order consumers in their food chains. C. spilopterus and Sparus
LQ 0.0001 0.0001 0.0003 0.001 0.0001
aurata are also similar in some respects, such as: the belong to the same
class (Actinopterygii), inhabit the bottom, consume fish and crusta-
ceans and are also considered to be consumers of second or third order
metabolism in the studied species, and also due to the difficulty in
in their food chains.
obtaining a control group (CTR) since the samples were carried out in
the field, control values of similar taxonomic species were used in order
to obtain a parameter of comparison and, with that, to be able to 3.2.1. Guri Sea Catfish (G. genidens)
evaluate the alteration or not of these data within the environment in The figure (Fig. 2) shows the comparison of values obtained for G.
which they were. The values used as reference for comparison with the genidens with values of the reference species (Rhamdia quelen)
specimens of this study were obtained through an average between (Barcellos et al., 2010; Zeppenfeld et al., 2013, Miron et al., 2008;
some results referring to the species Rhamdia quelen and Sparus aurata. Lermen et al., 2004), for both hepatic and muscular glycogen.

44
B.C. Petersen, et al. Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49

Fig. 2. Hepatic glycogen, muscle glycogen, glucose and lactate values - G. genidens.

The data found for G. genidens were lower (p < 0.05) than the re-
ference group, presenting a reduction of ± 62% for glycogen in liver
tissue and ± 66% in muscle.
The figure (Fig. 2) shows that the Guri Sea Catfish presented a high
concentration of plasma glucose, which is a significantly high con-
centration, with an increase of ± 100% in relation to the reference
group (Barcellos et al., 2010; Lermen et al., 2004; Rempel, 2014; Souza
et al., 2015).
3.2.2. Bay whiff (C. spilopterus)
The hepatic glycogen concentration in the Bay whiff (Fig. 3) showed
a significant increase of ± 77% in relation to the reference group
(Sparus aurata) (Carrión et al., 2005; Peres et al., 1999 and Montserrat
et al., 2007). For the muscle glycogen (Fig. 3) the values of the Bay
whiff were much higher (p < 0.05) than those of the reference group
(Peres et al., 1999 and Montserrat et al., 2007).
As observed in the Guri Sea Catfish, the Bay whiff presented a sig-
nificant increase in plasma glucose levels (Fig. 3), with an increase
of ± 69% in relation to the reference group (Carrión et al., 2005;
Arends et al., 1999; Rollant et al., 2001; Teles et al., 2004; Peres et al.,
1999; Montserrat et al., 2007).
The lactate concentration (Fig. 3) also showed higher values
(p < 0.05) at 100% in relation to the reference group (Carrión et al.,
2005; Arends et al., 1999; Teles et al., 2004).
3.2.3. Guri Sea Catfish (G. genidens) × Bay whiff (C. spilopterus)
The figures (Fig. 4) show the comparison of the two species sampled
in this study, analyzing if there are differences, significant or not, be-
tween the parameters analyzed.
The hepatic glycogen (Fig. 4) of the Bay whiff showed a significant

Fig. 3. Hepatic glycogen, muscle glycogen, glucose and lactate values - C. spilopterus.

45
B.C. Petersen, et al.
Fig. 4. Hepatic glycogen, muscle glycogen, glucose and lactate values - G. genidens × C. spilopterus.
increase of ± 67% in relation to the Guri Sea Catfish and, for muscle
glycogen, (Fig. 4), this rise was ± 16%.
As shown in Fig. 4, the glucose and lactate values between the
species did not present significant differences.
4. Discussion
4.1. Water analyses
The values found for pH and water temperature are in agreement
with the values found in the literature by Castro and Rocha (2016). On
the other hand, DO values were divergent, with the study average being
3.46 mg/L, while Castro and Rocha (2016) found values between 6.1
and 10.3 mg/L. This variation may be influenced by the periods of the
analyses, which were different, by the sampling point and the depth.
The DO conditions found in this study are not favorable for the survival
of aquatic organisms, as the minimum value stipulated by CONAMA
357/2005 is 5.0 mg/L. However, there are tolerance variations de-
pending on the species of fish, which may be more resistant and able to
live in environments with DO content lower than 5.0 mg/L while others
may require higher values, such as 8 mg/L, for example, as the case of
trout (Salmo trutta fario) (CETESB, 2016).
The values obtained by Castro and Rocha (2016) in the waters of
Lagoa Tramandaí were analyzed during the irrigation period of the rice
crop, which shows that the crop has some relation with the presence of
heavy metals in the lagoon. The data found by these authors may have
numbers above those obtained in that study due to the collection
period; in addition, the variation in metals in the water varies greatly,
even throughout the same day, and this may be one of the reasons the
concentration is higher, Fig. 5. Another factor that may have con-
tributed to the difference in the results were the months of collection, as
the analysis of this study was outside the period of irrigation of the rice
crop, which may be indicative of the lower value found.
In addition, the month of March presented the highest rainfall index
during the analysis period (Fig. 6), with a value of 317.7 mm. Castro
and Rocha (2016) had pluviometric indexes around 120 mm in all
months of collections, so this index was approximately 60% lower than
that found in March 2016. This factor contributes to the difference in
the drop of the values obtained due to the dilution of the metals in the
water during the rainy season.
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Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49
4.2. Analysis of carbohydrate metabolism in fish
4.2.1. Guri Sea Catfish (G. genidens)
The decrease in glycogen levels in the hepatic and muscular tissues
in relation to the reference group may be related to the presence of
heavy metals, since metal values were found in Lagoa Tramandaí by
Castro and Mello (2013) and by Petersen and Damin (2016) and also as
verified in the study by Cicik and Engin (2005) for Cyprinus corpio ex-
posed to cadmium. The authors revealed that heavy metals can cause
stress in fish and may lead to decreased glycogen, as metals affect the
activities of enzymes that work on carbohydrate metabolism. Oruç and
Üner (1999) found an increase in muscular glycogen consumption in
relation to the reference suggesting an energetic alternative to com-
pensate for stress and to maintain accumulated storages in the liver, in
cases of persistent contamination.
The increase in plasma glucose probably occurred because the or-
ganism was mobilizing more glycogen reserves, since there was a re-
duction of glycogen in both tissues. The increase in glucose may also be
related to stress situations, for example, the time of flight in the capture,
boats traffic and the very contamination of the environment in which
they are. Some studies indicate that glycogen depletion in the liver and
muscle are closely related to increased plasma glucose as a common
response to fish exposure to heavy metals (Cicik and Engin, 2005;
Pretto et al., 2013). Guri Sea Catfish, as already reported in the Petersen
and Damin (2016) study, presented levels of metals in their tissues, and
arsenic was above the maximum residue limit adopted by the Ministry
of Agriculture, Livestock and Supply (MAPA). These metals con-
centrations in the organism, and also the amount present in the water of
the Lagoa Tramandaí can interfere in the carbohydrate metabolism
altering its functions.
In Fig. 2 the increased lactate indicates that the anaerobic glycolytic
pathway is active, in other words, that the glucose is being degraded
with reduction of the oxygen levels for its use. The increase (p < 0.05)
of ± 200% of lactate relative to the reference group (Rempel, 2014 and
Souza et al., 2015) may be related to the ability of agrochemicals to
induce a low concentration of oxygen available to fish, thus favoring
anaerobic metabolism and thereby increasing lactate levels.
The high presence of lactate may be related to the presence of
agrochemicals in lagoon water. Taking into account the studies of
Castro and Mello (2013), which analyzed the presence of agrochemicals
and heavy metals in Lagoa Tramandaí and reported that, although the
B.C. Petersen, et al.
Fig. 5. Comparison between the results of heavy metals in water found in this study with results from the literature.
levels of agrochemicals were not detected owing to biotransformations
they suffer when entering the environment, they are present and ex-
ercising their functions. Thus, the presence of these compounds de-
creases the concentration of oxygen available in the environment and
forces the use of anaerobic metabolism, thereby increasing blood lac-
tate levels. On the other hand, according to Rempel (2014), the increase
in plasma lactate may not just mean the increase of its production, but
may simply be a delay in its use by the tissues, its high rate in blood.
4.2.2. Bay whiff (C. spilopterus)
The increase of hepatic glycogen in Bay whiff was also observed by
Pretto et al. (2013) with Rhamdia quelen exposed to cadmium, who
reported that increased glycogen is a common response to heavy metal
exposure. These authors also describe that fish can adapt to environ-
ments containing cadmium in order to maintain tissue and blood glu-
cose. The high value of muscle glycogen may be related to previous
consumption of hepatic glycogen by the body. In this case, in which
Fig. 6. Pluviometric indices of the Lagoa Tramandaí region during the study period.
(Source: Adapted from IRGA (2016).)
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Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49
there is a high blood glucose level, there was little or no consumption of
muscle glycogen, so the blood glucose content and the degradation of
hepatic glycogen were sufficient to guarantee the energetic supply of
the individual (Cyrino and Zucas, 1999). Other factors that may have
contributed to this wide difference in glycogen values are the differ-
ences in the species, the environment they were in, and also the in-
terferences they were suffering from the environment.
This large variation of both muscular and hepatic glycogen may be
related to the environment in which these organisms lived: in this study
they were captured in their natural environment and those of the re-
ference group were kept in the laboratory. In addition to being different
species, they may present diversity in metabolic functioning. The con-
centration of contaminants may also have influenced such variation:
while the study samples were exposed to all types of contaminants and
interferences present in Lagoa Tramandaí, those of the reference group
were kept in laboratories in waters with no anomalous substance con-
tent.
B.C. Petersen, et al.
It is also worth mentioning that Bay whiff, as well as Guri Sea
Catfish, are predominantly bottom animals and live in sandy or muddy
sediment environments and, by feeding close to the bottom, end up
ingesting sediment particles that, as found by Castro and Mello (2013),
have deposited heavy metals that enter their food chains and may in-
terfere with their carbohydrate metabolism.
The increase in glucose observed in the Bay whiff shows that these
animals were mobilizing glycogen reserves by maintaining glycemia in
order to balance their metabolic needs. The high value found for lactate
shows and proves the degradation of glucose for use by the body, thus
maintaining available energy to meet energy demand.
The increased lactation in this study was also reported by Rempel
(2014), who found high values for lactate compared to their control. In
this work the interference of agrochemicals in carbohydrate metabo-
lism of Rhamdia quelen was analyzed. This author suggests that the
search for homeostasis led the body to use an alternative route due to
the drop in dissolved oxygen levels caused by the presence of agro-
chemicals in the water, which explains the lactate increase. The lactate
increase observed in this study may also be related to the low levels of
dissolved oxygen that were found in Lagoa Tramandaí. The research
presents an average DO of 3.46 mg/L while CONAMA 357/2005 (Brasil,
2005) stipulates the minimum value of 5 mg/L as favorable to fish
survival, thus providing anaerobic route and organic compost increase.
4.2.3. Guri Sea Catfish (G. genidens) × Bay whiff (C. spilopterus)
The hepatic and muscle glycogen reserves were higher in the Bay
whiff, that is, it used fewer energy reserves than the Guri Sea Catfish.
According to a study by Petersen and Damin (2016), which founded
metals concentration in the muscle of the Guri Sea Catfish, it can be
inferred that this species is influenced by the presence of metals, even in
low concentrations. This is due to glycogen degradation and increased
plasma glucose, which is typical behavior of organisms in the presence
of heavy metals (Cicik and Engin, 2005).
According to the study by Moreira (2015), which analyzed the
presence of heavy metals (As, Cd, Cu and Pb) in the muscle of some
species of fish most consumed by humans in Baía de Sepetiba in Rio de
Janeiro, both the Guri Sea Catfish (G. genidens) and Bay whiff (C. spi-
lopterus) presented heavy metal contents in their organisms. However,
the Guri Sea Catfish presented higher concentrations for all the ana-
lyzed metals in comparison to the Bay whiff. It can be assumed that the
metabolism of Bay whiff absorbs fewer heavy metals than Guri Sea
Catfish, since these animals inhabit the same environment, reside in the
bottom and have practically the same feeding behavior.
Taking into account the study of Moreira (2015), it is possible to
relate Baía de Sepetiba to the environment of Lagoa Tramandaí, in the
sense that the specimens inhabit the same site and are influenced by the
same levels of contamination by heavy metals present in the medium.
Therefore, we can associate higher values for the Bay whiff in relation
to the mobilization of hepatic and muscular glycogen with the taxo-
nomic difference of the species: the Guri Sea Catfish is more susceptible
to contamination by heavy metals and needs more of the glycogen re-
serves compared to the Bay whiff.
As already reported by Cheis (2013), the effects of heavy metals and
their accumulation vary from species to species, which may have had
an influence on the difference in the levels of glycogen consumed. The
values obtained for glycogen, glucose and lactate prove that these an-
imals have a different metabolic profile, and may be a consequence of
the taxonomic differences between them. They have the same feeding
behaviors, which are characteristic of species living at the bottom of the
estuaries and belonging to the same class, but to different order, family
and genus; that may cause the variations found in their metabolism.
It can be concluded that the presence of metallic ions found in the
water of Lagoa Tramandaí interferes in the carbohydrate metabolism of
Guri Sea Catfish (G. genidens) and Bay whiff (C. spilopterus). A reduction
of hepatic glycogen was observed in both species, whereas the muscular
glycogen decreases only in the Guri Sea Catfish: in the Bay whiff, in this
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Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49
tissue, the reserve has remained high. An increase in glucose and
plasma lactate in both species and the differences found in the gly-
cogen, glucose and lactate values show that these species have a dif-
ferent carbohydrate metabolism, each of which has its own character-
istics in relation to the environment.
It is suggested that the difference between species occurs in the
greater or lesser mobilization of reserves in the level of hepatic and
muscular tissue, since the plasmatic metabolites do not differ between
species.
The results were expressed as average ± standard error. Asterisks
(*) indicate significant differences between the parameters (p > 0.05
and n = 15).
Declarations of interest
None.
Acknowledgements
This work was supported by CAPES-PROSUP (Programa de Suporte
a Pós-graduação de Instituições de Ensino Particulares) through a
scholarship and UNILASALLE (Universidade La Salle Canoas).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.cbpc.2019.01.007.
References
Anama, 2015. Boletim Taramandahy 5. Disponível em: http://www.onganama.org.br/
Impressos/boletim_taramandahy_5-faseII_marco_2015_revisao_FINAL_04-03-2015.
pdf, Accessed date: 12 July 2016.
Arends, R.J., et al., 1999. The stress response of the gilthead sea bream (Sparus aurata L.)
to air exposure and confinement. J. Endocrinol. 163 (1), 149–157.
Barcellos, L.J.G., et al., 2010. The effects of fasting on cortisol, blood glucose and liver
and muscle glycogen in adult jundia Rhamdia quelen. Aquaculture 300 (1), 231–236.
Brasil, 2005. Dispõe sobre a classificação dos corpos de água e diretrizes ambientais para
o seu enquadramento, bem como estabelece as condições e padrões de lançamento de
efluentes, e dá outras providências. Resolução n. 357 de 17 de março de 2005, do
Conselho Nacional do Meio Ambiente – CONAMA. In: Diário Oficial da União,
(Brasília).
Brasil, 2012. Instrução normativa, N° 11, de 22 de maio de 2012. Plano Nacional de
Controle de Resíduos e Contaminantes - PNCRC. In: Diário Oficial da União.
Ministério da Agricultura Pecuária e Abastecimento, Brasília, DF 25 de maio de.
(seção 1 Página 7).
Carrión, Raúl Laiz, et al., 2005. Growth performance of gilthead sea bream Sparus aurata
in diffetent osmotic conditions: implications for osmoregulation and energy meta-
bolism. Aquaculture 250 (2), 849–861.
Castro, D., Mello, R.S.P., 2013. (Org.). Bacia Hidrográfica do Rio Tramandaí: Atlas
Ambiental. Porto Alegre, Via Sapiens (179 p.).
Castro, Dilton de, Rocha, Cacinele Mariana da, 2016. Qualidade das Águas da Bacia
Hidrográfica do Rio Tramandaí. Via Sapiens, Porto Alegre (172 p.).
CETESB, 2016. Mortandade de peixes. Disponível em: http://mortandadedepeixes.
cetesb.sp.gov.br/alteracoes-fisicas-e-quimicas/oxigenio-dissolvido, Accessed date: 2
November 2016.
Cheis, Daiana, 2013. Os danos que o Cromo Hexavalente pode causar à saúde. In: Revista
Tae: especializada em tratamento de água & efluentes, (São Paulo). Disponível em:
http://www.revistatae.com.br/noticiaInt.asp?id=6928, Accessed date: 7 November
2016.
Cicik, Bedii, Engin, Kenan, 2005. The effects of cadmium on levels of glucose in serum
and glycogen reserves in the liver and muscle tissues of Cyprinus carpio (L., 1758).
Turk. J. Vet. Anim. Sci. 29 (1), 113–117.
Cyrino, Edilson Serpeloni, Zucas, Sérgio Miguel, 1999. Influência da ingestão de carboi-
dratos sobre o desempenho físico. Revista da Educação Física/uem 10 (1), 73–79.
Deus, A.A. Lopes de, Rocha, D.F., Novelli, R., 2009. Dieta do bagre Genidens genidens (val.
1839) na lagoa de Iquipari, norte do Estado do Rio De Janeiro. Disponível em:
http://www.seb-ecologia.org.br/2009/resumos_clae/264.pdf, Accessed date: 25
August 2016.
Fischer, L.G., Vieira, J.P., Pereira, L.E.D., 2011. Peixes estuarinos e costeiros, 2. ed. Rio
Grande, Luciano Gomes Fischer.
IRGA, 2016. Médias Climatológicas. Disponível em: http://www.irga.rs.gov.br/
conteudo/766/medias-climatologicas, Accessed date: 10 October 2016.
Lermen, Carine Luísa, et al., 2004. Effect of different temperature regimes on metabolic
and blood parameters of silver catfish Rhamdia quelen. Aquaculture 239 (2), 497–507.
Li, Xiaoyu, et al., 2017a. Effects of exposure to multiple heavy metals on biochemical and
B.C. Petersen, et al.
histopathological alterations in common carp, Cyprinus carpio L. Fish Shellfish
Immunol. 461–472. ago.. Disponível em: https://www.researchgate.net/
publication/319197363_Effects_of_exposure_to_multiple_heavy_metals_on_
biochemical_and_histopathological_alterations_in_common_carp_Cyprinus_carpio_L,
Accessed date: 21 December 2018.
Li, Xiaoyu, et al., 2017b. Studies on seasonal pollution of heavy metals in water, sedi-
ment, fish and oyster from the Meiliang Bay of Taihu Lake in China. Chemosphere
626–638. out.. Disponível em: https://www.researchgate.net/publication/
320510029_Studies_on_seasonal_pollution_of_heavy_metals_in_water_sediment_fish_
and_oyster_from_the_Meiliang_Bay_of_Taihu_Lake_in_China, Accessed date: 21
December 2018.
Lissner, J.B., Gruber, N.L.S., 2009. Contaminação dos recursos hídricos e gestão integrada
no litoral norte do Rio Grande do Sul. 2009. Disponível em: http://seer.ufrgs.br/
index.php/paraonde/article/view/22096/12854, Accessed date: 3 November 2013.
Machado, Rodrigo, et al., 2015. Ocorrência de peixes não-nativos no sistema estuar-
inolagunar de Tramandaí, Rio Grande Do Sul, Brasil. Revista Eletrônica Científica da
Uergs, Porto Alegre 1 (1), 37–43. dez.. Disponível em: https://www.ufrgs.br/
ppgban/wp-content/uploads/2015/11/35-2313-1-PB-1.pdf, Accessed date: 22 June
2016.
Miron, Denise dos S., et al., 2008. Ammonia and pH effects on some metabolic parameters
and gill histoloy of silver catfish, Rhamdia quelen (Heptapteridae). Aquaculture 277
(1), 192–196.
Montserrat, Núria, et al., 2007. Distinct role of insulin and IGF-I and its receptors in white
skeletal muscle during the compensatory growth of gilthead sea bream (Sparus
aurata). Aquaculture 267 (1), 188–198.
Moreira, Vanessa de Almeida, 2015. Distribuição de metais em espécies de peixes da baía
de sepetiba – Rio De Janeiro. 2015. 130 f. Dissertação (Mestrado) Curso de
Programa de Pós-graduação em Geociências – Geoquímica, Instituto de Química,
Universidade Federal Fluminense, Niterói Disponível em: http://www.repositorio.
uff.br/jspui/bitstream/1/1607/1/Dissertação_Vanessa_de_Almeida_Moreira.pdf,
Accessed date: 11 November 2016.
Oruç, O.E., Üner, N., 1999. Effects of 2,4-diamin on some parameters of protein and
carbohydrate metabolisms in the serum, muscle and liver of Cyprinus carpio. Environ.
Pollut. 105, 267–272.
Peres, H., Gonçalves, P., Teles, A. Oliva, 1999. Glucose tolerance in gilthead seabream
(Sparus aurata) and European seabass (Dicentrarchus labrax). Aquaculture 179 (1),
415–423.
Petersen, Brunna Castilhos, Damin, Isabel Cristina Ferreira, 2016. Avaliação da qualidade
do pescado da lagoa Tramandaí/rs. In: 10° Simpósio Internacional De Qualidade
Ambiental, 10°, 2016, Porto Alegre. Anais…. Abes, Porto Alegre, pp. 1–15. Disponível
49
Comparative Biochemistry and Physiology, Part C 219 (2019) 42–49
em: http://www.abes-rs.org.br/centraldeeventos/_arqTrabalhos/trab_
20160902101515000000593.pdf, Accessed date: 12 November 2016.
Pretto, Alexandra, et al., 2013. Alterations in carbohydrate and protein metabolism in
silver catfish (Rhamdia quelen) exposed to cadmium. Ecotoxicol. Environ. Saf. 100,
188–192.
Rempel, Simone de Souza Borges, 2014. Alterações no metabolismo de carboidratos em
jundiás (Rhamdia quelen) expostos a agroquímicos e ao estresse. Curso de Avaliação
de Impactos Ambientais, Centro Universitário La Salle, Canoas 53 f. Dissertação
(Mestrado).
Rollant, J., et al., 2001. Pituitary and interrenal function in gilthead sea bream (Sparus
aurata L., Teleostei) after handling and confinement stress. Gen. Comp. Endocrinol.
121 (8), 333–342.
SEMA, 2016. O que é uma Bacia Hidrográfica? Disponível em: http://www.sema.rs.gov.
br/conteudo.asp?cod_menu=54, Accessed date: 9 April 2016.
Silveira, R.A., 2013. Variação temporal e espacial da assembleia de peixes na Laguna
Tramandaí, RS. Dissertação – Universidade Federal do Rio Grande do Sul, Imbé.
Silveira, U.S., Logato, P.V.R., Pontes, E.C., 2009. Utilização e metabolismo dos carboi-
dratos em peixes. Nutritime, Minas Gerais 6 (1), 817–836. jan.. Disponível em:
http://nutritime.com.br/arquivos_internos/artigos/079V6N1P817_836_JAN2009_.
pdf, Accessed date: 20 May 2015.
Sisinno, C.L.S., Oliveira-Filho, E.C., 2013. Princípios de Toxicologia Ambiental.
Interciência, Rio de Janeiro.
Smith, C.M., Marks, A.D., Lieberman, M., 2007. Bioquímica médica básica de Marks: uma
abordagem clínica, 2. ed. Porto Alegre, Artmed.
Souza, Carine de Freitas, et al., 2015. Rhamdia quelen (Quoy & Gaimard, 1824), submitted
to a stressful condition: effect of dietary addition of the essential oil of Lippia alba on
metabolism, osmoregulation and endocrinology. Neotropical Ichthyology 13 (4),
707–714.
Teles, M., Pacheco, M., Santos, M.A., 2004. Sparus aurata L. liver EROD and GST activ-
ities, plasma cortisol, lactate, glucose and erythrocytic nuclear anomalies following
short-term exposure either to 17h-estradiol (E2) or E2 combined with 4-nonylphenol.
Sci. Total Environ. 336 (1), 57–69.
Tramandaí, 2016. Aspectos Geográficos. Disponível em: http://www.tramandai.rs.gov.
br/index.php?acao=conteudo&conteudos_id=12, Accessed date: 6 June 2016.
Van Handel, E., 1965. Estimation of glycogen in small amounts of tissue (Anal. Biochem.).
65 (1), 256–276.
Zeppenfeld, Carla Cristina, et al., 2013. Physiological and biochemical responses of silver
catfish, Rhamdia quelen, after transport in water with essential oil of Aloysia triphylla
(L'Herit) Britton. Aquaculture 2 (3), 101–107.