Elsevier

Aquatic Toxicology

Volume 126, 15 January 2013, Pages 306-313
Aquatic Toxicology

Carbaryl exposure and recovery modify the interrenal and thyroidal activities and the mitochondria-rich cell function in the climbing perch Anabas testudineus Bloch

https://doi.org/10.1016/j.aquatox.2012.09.014Get rights and content

Abstract

We examined the effects of carbaryl (1-naphthyl methylcarbamate; sevin), a carbamate pesticide, on interrenal and thyroid activities and mitochondrial rich (MR) cell function in climbing perch to understand the physiological basis of toxicity acclimation in this fish to the chemical stressor. Carbaryl exposure (5–20 mg L−1) for 48 h increased cortisol and glucose, but decreased the T3 level without affecting T4 concentration in the plasma. These responses of the carbaryl-exposed fish were nullified and a rise in plasma T4 occurred in these fish when they were kept for 96 h recovery in clean water. A tight plasma mineral control was indicated in the carbaryl-exposed fish as reflected by the unchanged plasma Na, K, Ca and inorganic phosphate levels. The ouabain-sensitive Na+, K+-ATPase activity showed an increase in the gills but the intestinal and renal tissues showed little response to carbaryl treatment. However, substantial increases in the intestinal and renal Na+, K+-ATPase activities occurred in the recovery fish. The MR cells in the branchial epithelia showed a strong Na+, K+-ATPase immunoreactivity to carbaryl treatment indicating an activated MR cell function. The numerical MR cell density remained unchanged, but stretching of secondary gill lamellae as part of gill remodeling occurred during carbaryl exposure. The increased surface of these lamellae with abundant MR cells as a result of its migration into the lamellar surface points to marked structural and functional modifications of these cells in the carbaryl-treated fish which is likely to a target for carbaryl action. The rise in plasma T4 and the restoration of normal branchial epithelia in the recovery fish indicate a thyroidal involvement in the recovery response and survival. Our data thus provide evidence that carbaryl exposure and its recovery evoke interrenal and thyroid disruption in this fish leading to a modified osmotic response including an altered MR cell function.

Highlights

► The physiologic responses of climbing perch to carbaryl was studied. ► Carbaryl exposure produced interrenal and thyroidal disruption in this fish. ► These responses of the carbaryl were reversed when kept for recovery. ► MR cells show marked structural and functional modifications and act as a target for carbaryl action.

Introduction

Indiscriminate pesticide use in agriculture and the resulting widespread distribution of pesticide residues evoke a threat to non-target organisms including fishes. The neurotoxic pesticide N-methyl carbamate like carbaryl, is known for its inhibitory action in acetyl cholinesterase system that can impose adverse effects on many physiological processes of fish (Tierney et al., 2006, Kavitha and Rao, 2007, Mdegela et al., 2010). Because of the vulnerability of fish to aquatic toxicants, many of these chemical stressors have frequently been shown to disrupt their water and ion regulation (Leji et al., 2007, Lock and Wendelaar Bonga, 2008, Adeyemi et al., 2012). Similarly, exposure of fishes to pesticides (Sancho et al., 1997, Hontela et al., 2008, Lock and Wendelaar Bonga, 2008, Peter et al., 2009), acids (Brown et al., 1990, McCormick et al., 2009, Peter and Rejitha, 2011), industrial waste (Leji et al., 2007, Peter et al., 2007), ammonia, and metals (Dang et al., 2001, Chowdhury and Wood, 2007) induces changes in the branchial epithelium and alters the activity of Na+, K+-ATPase thereby modifying the normal flow of ions. Acute and chronic exposures of fish to insecticides affect plasma ion concentrations (Mishra et al., 2001, Singh et al., 2002) and ion transporting ATPases including Na+, K+ ATPase (Kakko et al., 2003, Agrahari et al., 2007).

Fishes possess complex neuroendocrine mechanisms which allow them to combat the disturbed physiological homeostasis particularly during the exposure to chemical stressors (Wendelaar Bonga, 1997, Iwama et al., 2006, Peter et al., 2007, Schreck, 2010, Peter and Peter, 2011). Changes in hydromineral processes and energy metabolism are important adaptive modifications that fish show during stress (Peter et al., 2004, Peter et al., 2007, Peter et al., 2009, Lock and Wendelaar Bonga, 2008, Adeyemi et al., 2012, Peter and Peter, 2011). Cortisol, the end product of corticosteroidogenesis that occurs in the interrenal cells of head kidney of teleostean fishes, has been associated with metabolic and hydromineral control (Vijayan et al., 1997, Vijayan et al., 2003, Dang et al., 2000). This primary stress hormone in teleosts that stimulates the synthesis of energy substrates (Vijayan et al., 1997), and many other physiological processes (Wendelaar Bonga, 1997, Mommsen et al., 1999, Babitha and Peter, 2010), shows sensitivity to many endocrine disrupting chemicals (Hontela, 2005, Lock and Wendelaar Bonga, 2008). Similar to the interrenals, the thyroid gland that releases thyroxine (T4) and triiodothyronine (T3) as the primary thyroid hormones (THs), is also involved in the regulation of a wide range of biological processes in fishes, including energy metabolism and hydromineral regulation (Peter et al., 2000, Peter et al., 2011, Power et al., 2001, Arjona et al., 2008, Peter and Peter, 2009). Thyroid function in fish often shows sensitivity to many environmental variables and chemical stressors including endocrine disrupting chemicals (Leatherland, 1994, Peter et al., 2007, Peter and Rejitha, 2011, Feng et al., 2012) and now it is clear that THs are involved in stress response of fish (Peter, 2011, Peter and Peter, 2011).

Gills, the main sites for gas exchange, hydromineral regulation and nitrogenous excretion, are especially vulnerable to aquatic contaminants including pesticides (Evans et al., 2005, Lock and Wendelaar Bonga, 2008, Peter and Rejitha, 2011). The resulting disturbance may trigger physiological and morphological alterations that will lead to restoration of branchial functions (Evans et al., 2005, Lock and Wendelaar Bonga, 2008). Exposure of fishes to pesticides leads to gill lesions including hyperplasia and thrombosis in the secondary lamellae (Rao et al., 2005). Mitochondria-rich cells (MR) in the branchial epithelia that possess Na+, K+-ATPase, the biochemical equivalent to the sodium pump, is a target cell for aquatic toxicants (Li et al., 1998, Dang et al., 2000). The activity of this enzyme that serves as a biomarker to contaminants is sensitive to many pesticides and industrial effluents (Dang et al., 2000, Leji et al., 2007). For example, a reduction in the gill Na+, K+-ATPase activity was observed in European eels (Anguilla anguilla) treated with fenitrothion or thiobencarb (Sancho et al., 1997, Sancho et al., 2003) or monocrotophos (Agrahari et al., 2007). On the contrary, in climbing perch an upregulation of Na+, K+-ATPase activity occurred when exposed to coconut husk retting effluents (Leji et al., 2007) or kerosene (Peter et al., 2007).

As the process of accommodation of environmental and biological challenges, acclimation imposes physiological and structural modifications in fishes (Peter and Peter, 2011, Peter and Rejitha, 2011). Toxic acclimation of fish to chemical stressors is complex and it is likely that changes in the interrenal and thyroid activities followed by the compensatory hydromineral modification might contribute to this process (Leji et al., 2007, Peter et al., 2007, Peter et al., 2009, Lock and Wendelaar Bonga, 2008, Peter and Peter, 2011). It is hypothesized that in response to pesticides, fish may modify their osmotic competence, branchial structure and MR cell function and alter hormones of thyroid and interrenal glands. The purpose of the study was to test this hypothesis in the climbing perch Anabas testudineus after exposing them to carbaryl, a carbamate pesticide which is moderately toxic to aquatic organisms including fishes (Tierney et al., 2006, Ferrari et al., 2007, Mdegela et al., 2010).

Section snippets

Animals

Tropical freshwater air-breathing fish commonly known as climbing perch (A. testudineus Bloch) belonging to order Perciformes and family Anabantidae was used as the test species. This native teleost fish inhabiting in the backwaters of Kerala in Southern India is an obligate air-breathing fish equipped to live in demanding environmental conditions with its well-defined physiological and biochemical mechanisms (Peter et al., 2007, Peter et al., 2011). These fish in their post-spawning phase were

Plasma glucose, cortisol, T3 and T4

Exposure of climbing perch to carbaryl (20 mg L−1) for 48 h produced significant (P < 0.001) increases in plasma glucose (Fig. 1A and B), plasma cortisol (P < 0.05; Fig. 2A and B) and a decrease in plasma T3 (P < 0.05; Fig. 3A and B), whereas a low concentration of carbaryl (5 mg L−1) did not affect these parameters. Plasma T4, however, remained unaffected by these concentrations of carbaryl (Fig. 3A). Plasma glucose and plasma cortisol declined significantly (P < 0.05) in the fish kept for 96 h recovery

Discussion

Many pesticides act as endocrine disrupting chemicals and alter the endocrine functions of fishes including the hypothalamo-pituitary-interrenal axis (Leblond et al., 2001, Hontela, 2005, Norris and Carr, 2006, Tierney et al., 2006, Lock and Wendelaar Bonga, 2008, Peter and Peter, 2011). Cortisol response to pesticides is therefore critical in fish as this stress hormone directs many compensatory physiological modifications in fish. For example, cortisol has a crucial role in the adaptation of

Conclusion

We conclude that carbaryl induces a stress response in climbing perch, since cortisol and glucose were elevated during exposure to this chemical. The inverse relationships between cortisol and T3 or with T4 occurring probably due to disruption of interrenal and thyroid, during carbaryl exposure and recovery period, suggest that both these hormones interact and promote the toxic acclimation of fish to carbaryl. The substantial compensatory modifications in the perch gills during carbaryl

Acknowledgements

We thank University Grants Commission, New Delhi (MRP F-30-205/2010(SR)). The UGC-SAP facility of the Department of Zoology of the University of Kerala is acknowledged for providing facilities. VSP acknowledges UGC for granting research award.

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