Biotransformation and Oxidative Stress Responses in Captive Nile Crocodile (Crocodylus niloticus) Exposed to Organic Contaminants from the Natural Environment in South Africa.

Augustine Arukwe,Aina O. Adeogun,Håkon A. Langberg,Annette Venter,Maura Benedetti,Randi Røsbak,Jan Myburgh,Christo Botha,Francesco Regoli,Hans-Joachim Lehmler

doi:10.1371/journal.pone.0130002

Abstract

In the present study, the biotransformation and oxidative stress responses in relation to chemical burden in the liver of male and female Nile crocodiles—Crocodylus niloticus—from a commercial crocodile farm passively exposed to various anthropogenic aquatic pollutants was investigated. In general, the data showed that male crocodiles consistently produced higher biotransformation and oxidative stress responses compared to females. Relationships between these responses and concentrations of aliphatic hydrocarbons and polycyclic aromatic hydrocarbons (PAHs) were also observed. Specifically, the catalytic assays for EROD and BROD (not PROD and MROD) showed sex-differences between male and female crocodiles and paralleled immunochemically determined CYP1A and CYP3A protein levels; the relatively similar levels of PAHs in both sexes suggest an estrogen-mediated reduction of this pathway in females. The antioxidant system exhibited higher levels in male crocodiles with slight or significant higher values for catalase (CAT), glutathione reductase (GR), glutathione peroxidases-H2O2 (GPx-H2O2), glutathione peroxidases-Cu (GPx-Cu), total antioxidant capacity towards peroxyl radicals (TOSC-ROO) and hydroxyl radicals (TOSC-HO), total glutathione (GSH) and malondialdehyde (MDA). On the other hand, the activities of acyl-CoA oxidase (AOX) and glutathione S-transferases (GST) were significantly higher in females. Principal component analysis (PCA) produced significant groupings that revealed correlative relationships (both positive and negative) between biotransformation/oxidative stress variables and liver PAHs and aliphatic hydrocarbon burden. The overall results suggest that these captive pre-slaughter crocodiles exhibited adverse exposure responses to anthropogenic aquatic contaminants with potentially relevant effects on key cellular pathways, and these responses may be established as relevant species biomarkers of exposure and effects in this endangered species.

Highlights

The release of environmental contaminants, including polycyclic aromatic hydrocarbons (PAHs), pharmaceuticals and other persistent organic pollutants (POPs) to the terrestrial and aquatic environments has been of concern for several decades [1,2,3]
Among PAHs, the low-molecular weight (LMW; Fig 2A) hydrocarbons were significantly higher in female crocodiles, while no sex-related differences were observed for the sum of high molecular weight (HMW; Fig 2B) PAHs despite some variations in individual compounds (Table A in S1 Dataset and Fig. A in S1 Dataset)
Total PAHs ranged from 3900 ± 1820 μg/g dw in female to 2900 ± 1940 μg/g dw in male crocodiles (Fig 2C)

Summary

Introduction

The release of environmental contaminants, including polycyclic aromatic hydrocarbons (PAHs), pharmaceuticals and other persistent organic pollutants (POPs) to the terrestrial and aquatic environments has been of concern for several decades [1,2,3]. Environmental contaminants, including PAHs and pharmaceuticals may be excreted both unmetabolized or as metabolites [4,5]. Phase 1 reactions result in loss of pharmacological activity of the xenobiotics through the introduction or exposure of a functional group on the parent compound [8], while phase 2 reactions introduce a covalent linkage between the functional group and an endogenous water soluble conjugate such as glucuronic acid to facilitate excretion [9]. The cytochrome P450 (or CYP) enzyme systems play an integral role in the biotransformation process [10]

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Conclusion