Elsevier

Chemosphere

Volume 108, August 2014, Pages 396-404
Chemosphere

Impact of a short-term diazinon exposure on the osmoregulation potentiality of Caspian roach (Rutilus rutilus) fingerlings

https://doi.org/10.1016/j.chemosphere.2014.02.038Get rights and content

Highlights

  • Diazinon increased cortisol levels indicating stress in Caspian roach fingerlings.

  • Diazinon reduced thyroid hormone levels (TSH, T3, T4) in exposed fingerlings.

  • Kidney and gill tissues showed damage in diazinon-exposed fingerlings.

  • Diazinon affected whole-body electrolyte levels in exposed fingerlings.

  • Diazinon may impact adaptation to brackish water and restocking efforts.

Abstract

The stocks of Caspian roach (Rutilus rutilus), an economically important species in the Caspian Sea, are depleting. Each year millions of artificially produced fingerlings of this species are restocked in the mouth of rivers of the Southern Caspian Sea (e.g. Qare Soo River), where they are exposed to pesticides originating from regional rice and orchard fields. This early exposure to pesticides could affect the hypo-osmoregulatory ability of juvenile fish. Thus, in this study, Caspian roach fingerlings were exposed to environmentally-relevant concentrations of the organophosphate insecticide diazinon for 96 h in fresh water and then transferred to diazinon-free brackish water (BW) for another 96 h. We report that cortisol and glucose levels were significantly increased in all diazinon treatments at all sampling time points in comparison to the control group. Moreover, the thyroid hormone levels of TSH, T4, and T3 significantly decreased in diazinon-exposed fish even after the transfer to BW. The electrolytes were differentially affected during the exposure to diazinon and after the transfer to BW. The number of chloride cells in the gill tissue was significantly increased during diazinon exposure at the higher concentrations and decreased to control levels after transfer to BW. Finally, gill and kidney tissues showed many histopathological changes in diazinon-exposed fish even after 240 h in BW. These results suggest that the release of Caspian roach fingerlings into the diazinon-contaminated Caspian Sea regions may alter their physiology and jeopardize their survival, which could lead to a failure in rebuilding the Caspian roach stocks in the Caspian Sea.

Introduction

Agriculture of rice and orchard is the main source of income in the Southern Caspian Sea region (Northern parts of Iran). Due to the industrialization and optimization of agriculture, the use of pesticides, especially the organophosphate insecticide diazinon, has increased during the past decade. This pesticide has been shown to contaminate groundwater through drainage and affect non-target aquatic organisms, including fish and crab even at sub-lethal doses (Rudnicki et al., 2009). The highest concentration of diazinon in surface water of the Qare Soo River estuaries was reported at 3.1 ± 0.3 mg L−1 (Shayeghi et al., 2006).

The Caspian roach (Rutilus rutilus) is a native species of the Caspian Sea (Soleimani et al., 2012). This fish is an economically important species in the Caspian Sea region and is also a main prey for sturgeon species (Keyvanshokooh and Kalbassi, 2006). Similarly to other Caspian Sea fishes (e.g. sturgeons), Caspian roach is considered an endangered species due to over fishing, water pollution, and loss of habitat and spawning sites (Kiabi et al., 1999). Therefore, the Iranian Fisheries Organization decided to restock this species by releasing fingerlings into some of the Iranian river estuaries (e.g. Qare Soo River) flowing into the Southern Caspian Sea.

However, little is known about the impacts of aquatic contaminants, such as diazinon, on vital physiological processes, including osmoregulation, of the released Caspian roach fingerlings. Osmoregulation in fish fingerlings in river estuaries is regulated by several hormones. The seawater (SW)-adapting hormone cortisol increases SW endurance by increasing chloride cells number, which in turn increases the activity of the gill Na+, K+-ATPase (Staurnes et al., 1993, McCormick, 2001). Cortisol has also been reported to stimulate downstream migratory behavior in Masu salmon (Oncorhynchus masou) (Munakata et al., 2007). In addition to its osmoregulatory role cortisol is responsive to various types of stress in anadromous species and is used as an indicator of endocrine status in migratory species (Waring and Moore, 2004). The thyroid hormones thyroxine (T4) and triidothyronine (T3) have been shown to have a supportive role during SW acclimation by potentiating the action of cortisol in the gill Na+, K+-ATPase at least in some species (Folmar and Dickhoff, 1981, McCormick, 2001, Arjona et al., 2008). Generally the increase in the levels of these hormones prior to the entry into SW facilitates the attainment of salt tolerance (Hoar, 1988, Lerner et al., 2007a).

The two main sites of osmoregulation in fish are the gills and the kidney. The gills are responsible for the active exchange of electrolytes by the chloride cells. Several pollutants, including pesticides, have been shown to affect the proper function of these highly specialized cells (Wendelaar Bonga and Lock, 1991). On the other hand, the fish kidney, similarly to higher vertebrates, is involved in electrolyte and water balance and plays an important role in maintaining stability of the organism’s internal environment. Additionally, kidney is involved with the excretion of soluble waste products resulting from the metabolism of nitrogen such as ammonia, urea, and creatinin (Das and Mukherjee, 2000), as well as the excretion of soluble/solubilized xenobiotic compounds and/or their metabolites (Christiansen et al., 1996). The kidney function was shown to be negatively impacted by pollutants (Das and Mukherjee, 2003, Cengiz, 2006, Xing et al., 2012). Given that proper regulation of electrolytes is vital for various buffer systems and pH balance, the ability of certain pollutants to disrupt it by affecting the gill or the kidney functions (Wendelaar Bonga and Lock, 1991, Tipsmark et al., 2002, Suvetha et al., 2010) should be further investigated to improve the aquaculture industries and restocking activities. The physiological changes in osmoregulation during the release of fingerlings into river estuaries are especially important, since this period is considered one of the more sensitive life stages to be exposed to contaminants (Rosseland et al., 2001, Lerner et al., 2007a, Monette and McCormick, 2008) including diazinon.

Therefore, this study investigated the effects of a short-term exposure to sub-lethal concentrations of diazinon on osmoregulation potentiality in Caspian roach fingerlings. To this end we measured the levels of (1) cortisol, (2) thyroid stimulating hormone (TSH), which stimulates the thyroid gland to release thyroid hormones (Chiamolera and Wondisford, 2009), and (3) thyroid hormones (T4 and T3). The levels of electrolytes and glucose were also assessed. Lastly, histopathological examinations of the gill and kidney tissues were performed.

Section snippets

Fish maintenance and exposure

Twelve hundred Caspian roach fingerlings (1.66 ± 0.05 g) were acquired from the Sijowal Fish Reproduction Center (Golestan province, Northeast Iran). Fish were maintained under a 14:10 h light–dark photoperiod in a 1000 L experimental tank for at least one week and then randomly assigned to 100 L fiberglass tanks with 100 fish per tank (3 replicate tanks per treatment). Freshwater (FW) temperature, dissolved oxygen, pH, and salinity were respectively maintained at 25.3 °C, 7.01 mg L−1, 7.8, and 3.2 PSU.

Hormone levels

Whole-body cortisol levels were significantly increased (p < 0.01) by all diazinon treatments at all sampling time points in comparison to the control group (Fig. 1A). However, when fish were transferred to diazinon-free BW the cortisol levels in exposed fish dropped to the control levels by 96 h (Fig. 1B).

The whole-body TSH levels significantly decreased (p < 0.01) in fingerlings exposed to diazinon in comparison to the control group in FW. This reduction occurred at 24 h and continued until 96 h in

Discussion

This study assessed the ability of the organophosphate insecticide diazinon to affect osmoregulation and seawater (SW) acclimation in Caspian roach fingerlings. We demonstrate for the first time that a 96 h diazinon exposure of Caspian roach fingerlings in freshwater (FW) altered the whole-body levels of thyroid and cortisol hormones. This study shows that the levels of thyroid stimulating hormone (TSH), thyroxine (T4), and triidothyronine (T3) significantly decreased in diazinon-exposed fish.

Conclusions

In the present study it was concluded that a short-term exposure to sub-lethal doses of diazinon, could affect osmoregulation and adjustment to BW in Caspian roach fingerlings. We suggest that these changes involve the decrease in TSH, T4, and T3 levels, increase in cortisol levels, differential changes in electrolyte and glucose levels, increase in the number of chloride cells in the gill, and histopathological changes of gill and kidney tissues. We therefore suggest that the diazinon-induced

Acknowledgments

The present work was supported by University of Tehran and Iranian Fisheries Research Organization. The authors are thankful to Ramzan Khosravi for his kind support to perform the experiments described herein.

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