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Toxic Effect of Insecticides Mixtures on Antioxidant Enzymes in Different Organs of Fish, Labeo rohita

PJZ_51_4_1355-1361

 

 

Toxic Effect of Insecticides Mixtures on Antioxidant Enzymes in Different Organs of Fish, Labeo rohita

Huma Naz1,*, Sajid Abdullah2, Khalid Abbas2, Wardah Hassan3, Moazama Batool4, Shakeela Perveen5, Sadia Maalik4 and Sajida Mushtaq4

1Department of Zoology, Cholistan University of Veterinary and Animal Sciences, Bahawalpur

2Department of Zoology, Wildlife and Fisheries, University of Agriculture, Faisalabad

3Department of Zoology, University of Sargodha, Sargodha

4Department of Zoology, Govt. College Women University, Sialkot

5Department of Zoology, Govt. Sadiq College Women University, Bahawlpur

ABSTRACT

In this study insecticides toxic effects of mixture of organochlorine (endosulfan) and organophosphate (chlorpyrifos) investigated on the activity of antioxidant enzymes viz. superoxide dismutase, peroxidase, catalase and glutathione S-transferase in different organs (liver, gills, kidney, brain, heart and muscle) of fish, Labeo rohita. The LC50 of chlorpyrifos+endosulfan mixture was calculated as 1.95±0.02 μgL-1 for 96 h with the 95% confidence limits. The fish expose to the mixture (1:1) for 96-h. The results obtained from this study showed that superoxide dismutase, peroxidase and glutathione S-transferase activities in the liver, gills, kidney, brain, heart and muscle were significantly (P<0.05) increased compared to control. The superoxide dismutase activity in organs of fish followed the order: liver>brain>kidney>gills>heart>muscle. The mean peroxidase activity in L. rohita followed the pattern: liver>brain>gills>kidney>heart>muscle. The glutathione S-transferse activity followed the order: brain>muscle>liver>gills>kidney>heart. However, catalase activity was significantly (P<0.05) increased in liver, gills and kidney of pesticides mixture exposed L. rohita as compared to control while it was decreased in brain, heart and muscle.


Article Information

Received 13 March 2018

Revised 02 June 2018

Accepted 06 July 2018

Available online 02 May 2019

Authors’ Contribution

HN executed the research. SA supervisor and planned the research. Ka facilitated in conducting the research work in his laboratory. WH and SP help in compiling data. MB,

S Maalik and S Mushtaq helped in writing the article.

Key words

Acute toxicity, Fish, Catalase, Glutathione S-transferase, Peroxidase, Superoxide dismutase, Pesticides mixture.

DOI: http://dx.doi.org/10.17582/journal.pjz/2019.51.4.1355.1361

* Corresponding author: dr.humanaz98@gmail.com

0030-9923/2019/0004-1355 $ 9.00/0

Copyright 2019 Zoological Society of Pakistan



Introduction

In present era, rapid development of industries and green revolution had led to serious environmental problems, water contamination being the most important (Samantha et al., 2005). The potentially harmful agrochemical chemicals such as pesticides are released in to the freshwater environment and had significantly unfavorable effects on non-target species like aquatic animals (John, 2007; Naz and Javed, 2012).

Endosulfan belong to organochlorine pesticides, is known be highly toxic to fish (Wan et al., 2005). Chlorpyrifos is widely used organophosphate pesticide, is a non-systemic insecticide designed to be effective by direct contact, ingestion and inhalation (Tomlin, 2006). This pesticide inhibits the AChE activity (Barata et al., 2004).

Fish are the keystone species which reflect the toxic effect of chemicals in water bodies (Slaninova et al., 2009). Pesticides may induce the production of reactive oxygen species (ROS) such as superoxide, hydrogen peroxide and hydroxyl radicals (Kumar et al., 2011). The production of ROS in aquatic organisms exposed to pesticides is linked with the existence of toxicants and causes oxidative stress a possible mechanism of toxicity (Oropesa et al., 2008). The defensive mechanism of fish against free radicals consists of superoxide superoxide dismutase, catalase, peroxidase and glutathione S-transferase (Guven et al., 2008). Superoxide dismutase is primary enzyme, responsible for transformation of the O-2 into H2O2. Hydrogen peroxide further transformed into oxygen and water by catalase. Peroxidase also converts the group of peroxides, including hydrogen peroxide (Hermes, 2004; Maran et al., 2009). Glutathione-S-transferase is involved in the biotransformation process of toxic substances into less toxic so fish can excrete easily from the body. In present research work, toxic effect of endosulfan and chlorpyrifos on antioxidant enzymes of fish Labeo rohita was observed.

 

Materials and methods

Experimental fish

For semi-static acute toxicity bioassay, fingerlings of fish, L. rohita (90-day old; Average weight, 8.24±0.32) were obtained from local Fish seed Hatchery and transferred to the Fisheries Research Farm, University of Agriculture, Faisalabad, Pakistan. Fish were acclimatized to laboratory condition for 14 days. During acclimatization period, L. rohita were fed with commercial feed (3% of wet body weight). After acclimatization, fish were shifted to glass aquaria containing 70-liter water.

Test chemicals

Technical grade pesticides viz. chlorpyrifos (CPF) and endosulfan (END) were used as test chemicals. The methanol was used to prepare stock-1 solution while solutions of CPF+END mixture of required concentrations (10ppm and 1:1 ratio) were prepared by its further dilutions in deionized water.

96-h LC50 and lethal toxicity tests

The acute toxicity tests (96-h LC50 and lethal concentration) of pesticides mixture for L. rohita were performed with three replicates. Sixteen concentrations (0.00, 0.20, 0.40, 0.60, 0.80, 1.00, 1.20, 1.40, 1.60, 1.80, 2.00, 2.20, 2.40, 2.60, 2.80 and 3.00 μg/L) of CPF+END mixture were used. All aquaria were supplied with exceeding aeration for 2 h in order to get a uniform concentration of the insecticides, and then 10 fish were shifted into each aquarium. Observation on fish mortality was assessed at 24, 48, 72 and 96 h after the start of experiment and dead fish were removed instantaneously. Probit Analysis method was applied to calculate the LC50 and lethal concentration of CPF+END mixture for L. rohita.

Antioxidant enzymes

After determination of 96 h LC50 concentration, a group (n=20) of fish were separately, exposed to this concentration for 4-days. For enzymatic study fish (n=5) sampling was done after 24, 48, 72 and 96-h. To calculate the antioxidant enzymes viz. superoxide dismutase (SOD), catalase (CAT), peroxidase (POD) and glutathione S-transferase (GST) were obtained from gills, liver, kidney, brain, heart and muscle of fish. All the organs were, separately, homogenized in cold phosphate buffer (pH 6.5, 0.2 M) by the ratio of 1:4 (w/v) using a blender. After that homogenates were centrifuged at 10,000 rpm and 4ºC for 15 min. Clear supernatants were obtained which were used for enzyme assay. The activity of SOD was checked according to the method of Giannopolitis and Ries (1977). CAT activity was measured by its ability to decrease the H2O2 concentration at 240 nm (Chance and Mehaly, 1977). The activity of POD was measured by following the procedure of Civello et al. (1995). The activity of GST was determined by following the method of Mannervik (1985).

Statistical analyses

Probit analysis method was applied to calculate the tolerance limits (LC50 and lethal concentration) of L. rohita for CPF+END mixture (Finney, 1971). ANOVA was performed on obtained data to find out the statistical differences among studied variables.

 

Table I.- Superoxide dismutase (SOD), catalase (CAT), peroxidase (POD) and glutathione S-transferase (GST) (UmL-1±SD) in gills of Labeo rohita during acute exposure of chlorpyrifos (CPF)+endosulfan (END) mixture.

Activity

Control

Treated

SOD

24 h

20.34±0.06b

41.79±0.07a

48 h

20.30±0.08b

57.41±0.23a

72 h

23.35±0.09b

73.17±0.12a

96 h

20.37±0.16b

102.29±0.18a

CAT

24 h

185.90±2.01b

210.75±11.69a

48 h

184.96±1.90b

218.09±11.05a

72 h

185.97±2.11b

232.95±11.55a

96 h

185.99±2.15b

244.67±12.35a

POD

24 h

1.46±0.07b

3.15±0.02a

48 h

1.47±0.13b

4.25±0.05a

72 h

1.48±0.09b

4.86±0.12a

96 h

1.49±0.11b

5.95±0.02a

GST

24 h

118.72±1.58b

224.70±1.61a

48 h

118.73±1.56b

262.48±1.99a

72 h

118.87±1.33b

313.56±1.85a

96 h

118.88±1.31b

380.67±1.66a

Means sharing similar letter in a row or in column are statistically non-significant (P>0.05).

 

Results and discussion

96-h LC50

The LC50 concentration for 96 h was calculated as 1.95±0.02 μgL-1 with the 95% upper and lower confidence limits as 1.685 and 2.144 μgL-1, respectively. The 96 h lethal concentration was estimated as 3.23±0.05 μgL-1 with the 95% upper and lower confidence limits as 2.906 and 3.858 μgL-1, respectively. It was observed that the fish mortality increased with increasing the exposure concentration. Water contamination by toxic chemicals caused mass mortality of aquatic fauna like fish (Kumari 2005; Gupta et al., 2012). Mortality of fish due to insecticides contact primarily depends upon its tolerance to the chemical, its dose and time of exposure (Al-Rudainy and Kadhim, 2012). Several authors have been conducted experiments on pesticides toxicity (organochlorines, pyrethroids organophospates and carbamides) for many fish species (Ambreen and Javed 2015; Ghazala et al., 2014; Shrivastava et al., 2002; Shailkh and Yeragi, 2004; Visvanthan et al., 2009).

 

Table II.- SOD, CAT, POD and GST (UmL-1±SD) in liver of Labeo rohita during acute exposure of CPF+END mixture.

Activity

Control

Treated

SOD

24 h

47.51±0.11b

90.40±0.12a

48 h

47.52±0.17b

102.25±0.29a

72 h

47.54±0.12b

117.32±0.21a

96 h

47.55±0.12b

129.15±0.27a

CAT

24 h

232.50±2.58b

254.17±11.73a

48 h

232.51±2.43b

269.70±11.65a

72 h

232.53±2.48b

273.38±11.90a

96 h

232.54±2.48b

291.05±12.53a

POD

24 h

1.95±0.03b

3.98±0.11a

48 h

1.96±0.13b

4.67±0.02a

72 h

1.97±0.18b

5.63±0.13a

96 h

1.99±0.09b

6.32±0.06a

GST

24 h

176.67±1.75b

267.57±1.92a

48 h

176.68±1.73b

301.83±1.47a

72 h

174.73±1.65b

394.55±1.96a

96 h

176.72±1.66b

425.35±2.30a

Means sharing similar letter in a row or in column are statistically non-significant (P>0.05).

For abbreviations, see Table I.

 

Table III.- SOD, CAT, POD and GST (UmL-1±SD) in kidney of Labeo rohita during acute exposure of CPF+END mixture.

Activity

Control

Treated

SOD

24 h

25.78±0.07b

55.65±0.08a

48 h

25.79±0.08b

74.49±0.021a

72 h

27.83±0.11b

96.08±0.18a

96 h

27.85±0.09b

117.25±0.23a

CAT

24 h

140.25±1.94b

164.25±10.13a

48 h

140.26±1.96b

176.95±10.58a

72 h

140.27±1.97b

183.33±10.47a

96 h

140.28±1.99b

194.55±11.79a

POD

24 h

1.22±0.09b

3.00±2.65a

48 h

1.23±0.04b

4.12±0.14a

72 h

1.21±0.09b

4.74±0.16a

96 h

1.24±0.12b

5.43±0.11a

GST

24 h

151.66±1.85b

234.66±1.85a

48 h

151.67±1.83b

292.71±1.76a

72 h

151.68±1.82b

361.42±2.27a

96 h

151.69±1.80b

401.00±2.99a

Means sharing similar letter in a row or in column are statistically non-significant (P>0.05).

For abbreviations, see Table I.

 

Antioxidant enzymes activities

SOD activity

Tables I-VI show effect of insecticide mixture on SOD, CAT, POD and GST in gills, liver, kidney, brain, heart and muscles, respectively of Labeo rohita. Results of this study showed that SOD activity significantly (P<0.05) increased in liver, gills, kidney, brain, heart and muscle of CPF+END exposed L. rohita compared to control (Tables I-VI). The SOD activity increased in selected organs of fish as following order: liver>brain>kidney>gills>heart>muscle. The increased SOD activity under oxidative stress induced by CPF may be due to conversion of superoxide radicals into hydrogen peroxide which is further transformed by CAT into oxygen and water (Sanchez et al., 2005). SOD is also a first crucial antioxidant enzyme which plays an important role to cope with oxiredicals and comprises a basic defense against the lethal effects of reactive oxygen species (ROS) (Kohen and Nyska, 2002). Oruc (2010) also reported the significant increase in the SOD activity in fish exposed to chlorpyrifos. According to Kumar et al. (2011) SOD activity increased in bronchi and hepatic tissue of Oreochromis mossambicus after acute exposure to endosulfan.

 

Table IV.- SOD, CAT, POD and GST (UmL-1±SD) in brain of Labeo rohita during acute exposure of CPF+END mixture.

Activity

Control

Treated

SOD

24 h

36.28±0.10b

68.74±0.09a

48 h

26.29±0.13b

85.23±0.23a

72 h

36.30±0.14b

99.76±0.15a

96 h

36.31±0.17b

113.34±0.20a

CAT

24 h

126.67±1.79a

110.58±10.01b

48 h

126.68±1.81a

96.66±10.02b

72 h

126.69±1.82a

81.11±9.77b

96 h

126.70±1.84a

72.23±9.42b

POD

24 h

1.75±0.07b

3.82±0.06a

48 h

1.77±0.05b

4.44±0.13a

72 h

1.78±0.10b

4.99±0.06a

96 h

1.79±0.08b

6.06±0.09a

GST

24 h

211.45±2.30b

370.98±1.39a

48 h

211.46±2.28b

406.17±1.06a

72 h

211.44±2.31b

473.35±2.47a

96 h

211.43±2.33b

521.75±1.79a

Means sharing similar letter in a row or in column are statistically non-significant (P>0.05).

For abbreviations, see Table I.

 

CAT activity

Tables I, II and III show that CAT activity significantly (P<0.05) increased in liver, gills and kidney of exposed L. rohita as compared to control while it was decreased in brain (Table IV), heart (Table V) and muscle (Table VI). The decreased in CAT activity changes the redox condition of the cells. Thus, increased level of CAT may be due to the removal of ROS from the cell generated by insecticides exposure (Stara et al., 2012). CAT activity in liver of common carp significantly increased in the presence of endosulfan (Salvo et al., 2012). According to Oruc and Usta (2007), CAT activity in muscle of C. carpio was inhibited after exposed to diazinon. Exposure of chloprpyrifos resulted in a significant reduction in CAT activity in the skeletal muscle and brain of Heteropneustes fossilis (Tripathi and Shasmal, 2010). Chlorpyrifos exposure caused reduction in gills, kidney and liver CAT activity of Ctenopharyngodon idellus (Kaur and Jindal, 2017).

 

Table V.- SOD, CAT, POD and GST (UmL-1±SD) in heart of Labeo rohita during acute exposure of CPF+END mixture.

Activity

Control

Treated

SOD

24 h

14.53±0.04b

30.67±0.06a

48 h

14.54±0.06b

41.20±0.19a

72 h

14.55±0.05b

52.31±0.12a

96 h

14.56±0.08b

66.28±0.16a

CAT

24 h

112.21±1.33a

92.17±5.81b

48 h

112.22±1.35a

79.24±5.08b

72 h

112.23±1.37a

69.32±4.84b

96 h

112.24±1.38a

57.73±4.18b

POD

24 h

1.09±0.08b

2.94±0.04a

48 h

1.09±0.43b

4.05±0.08a

72 h

1.07±0.07b

4.29±0.09a

96 h

1.1±0.26b

5.12±0.11a

GST

24 h

99.24±2.75b

187.10±2.99a

48 h

99.26±2.71b

220.26±2.70a

72 h

99.25±2.73b

264.18±2.86a

96 h

99.23±2.77b

294.26±2.72a

Means sharing similar letter in a row or in column are statistically non-significant (P>0.05).

For abbreviations, see Table I.

 

POD activity

Exposure of CPF+END mixture significantly (P<0.05) increased the POD activity in all selected organs of L. rohita as compared to control (Tables I-VI). The mean POD activity was more pronounced in liver (Table II) of L. rohita followed by that of brain, gills, kidney, heart and muscle. The higher POD activity in liver may be due to its role in detoxification of toxicants. The production of ROS during the biotransformation of toxicants can harm the cell through oxidation (Van der Oost et al., 2003). The increased POD activity might be expected to scavenge the ROS by converting hydrogen peroxide (Hinton et al., 2008). Alteration in peroxidase activity in liver of tilapia exposed to, 4-D+azinphosmethyl mixture was reported by Oruc and Uner (2000). A duration-specific increase in peroxidase activity in gills, brain, liver and muscle of L. rohita exposed to acute concentration of endosulfan was observed by Ullah et al. (2016).

GST activity

Results showed a significant increase in liver, gills, kidney, heart, brain and muscle GST activity of insecticides exposed L. rohita compared to control (Tables I-VI). The GST activity increase in the following order: brain>muscle>liver>gills>kidney>heart. These results are also confirmed by Kumar et al. (2011) who reported the significantly increased GST activity in gills and liver of tilapia after acute exposure to endosulfan. The activity of GST increased under certain agrochemicals exposure (Dorval et al., 2003; Monteiro et al., 2006). Exposure of chlorpyrifos increased the GST activity in common carp and zebra fish (Nunes et al., 2018). The increase in GST activity was due to the increase metabolism of lipoperoxides produced through Fenton reaction or due to the biotransformation of toxicants, representing the adaptive mechanism of fish (Modesto and Martinez, 2010). According to the Gonçalves et al. (2018) GST activity can be changed in contaminated area containing the organic chemical.

 

Table VI.- SOD, CAT, POD and GST (UmL-1±SD) in muscles of Labeo rohita during acute exposure of CPF+END mixture.

Activity

Control

Treated

SOD

24 h

7.75±0.03b

23.63±0.04a

48 h

7.76±0.03b

32.78±0.11a

72 h

7.77±0.03b

41.06±0.09a

96 h

7.78±0.05b

53.72±0.08a

CAT

24 h

194.10±2.35a

169.55±10.16b

48 h

194.11±2.36a

151.27±10.34b

72 h

194.13±2.39a

143.75±10.34b

96 h

194.16±2.44a

134.28±11.15b

POD

24 h

1.01±0.03b

2.88±0.04a

48 h

1.02±0.03b

3.95±0.76a

72 h

1.05±0.22b

4.02±0.10a

96 h

1.06±0.05b

5.00±2.64a

GST

24 h

155.67±2.60b

314.45±2.48a

48 h

155.66±2.12b

382.25±2.81a

72 h

155.65±2.13b

457.50±2.39a

96 h

155.64±2.15b

502.24±2.85a

Means sharing similar letter in a row or in column are statistically non-significant (P>0.05).

For abbreviations, see Table I.

 

Conclusion

This study showed that the exposure of insecticides in mixture form can lead to important alterations in antioxidant enzymes of fish. These enzymes can be used as valuable biomarker for identification of insecticides pollution in aquatic bodies. Results also indicated that the existence of pesticides in water bodies may be injurious to the health of aquatic animals especially for the fish.

 

Statement of conflict of interest

Authors have declared no conflict of interest.

 

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Pakistan Journal of Zoology

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Vol. 51, Iss. 6, Pages 1999-2399

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