Abstract
Water is one of our most precious resources and yet aquatic ecosystems, specifically freshwater ecosystems are increasingly impacted by pollutants such as pesticides, heavy metals, pharmaceuticals, personal care products and industrial and sewage effluents. Aquatic organisms, specifically fish are exposed to these pollutants. Humans, who may be consuming these fish or drinking polluted water are also at risk. Certain chemicals present in aquatic systems can disrupt the endocrine system. These chemicals are referred to as endocrine disrupting chemicals (EDCs). Endocrine disrupting chemicals act by mimicking or inhibiting the action of endogenous hormones, resulting in disruptions in the concentrations of active hormones or stimulation or inhibition of cellular pathways in target cells. There is a wide variety of chemicals that are categorised as EDCs including persistent organic pollutants, pesticides, plasticizers, some heavy metals, pharmaceuticals and personal care products. The present study, focused on pesticides and heavy metals with endocrine disrupting properties i.e., cadmium, lead, arsenic and mercury.
Pesticides is an umbrella term referring to herbicides, fungicides and insecticides. These are compounds that are produced to control unwanted pests, plants, insects or fungi and are mostly used in agricultural and farming activities. Heavy metals have both natural and anthropogenic origins. Agricultural, industrial and mining activities contribute to the presence and bioavailability of heavy metals in the environment. Pesticides and metals enter aquatic systems through wastewater effluents, leachate, surface runoff or aerial deposition following applications, where they can affect aquatic organisms. A large variety of these chemicals are lipophilic and can therefore accumulate in the mesenteric fat of organisms. Endocrine disruption has been associated with various health effects on fish including physiological changes, changes in sexual behaviours, disruption of sexual differentiation, intersex and infertility. Freshwater fish are particularly vulnerable to endocrine disruption.
The first case of histological evidence of intersex in a South African water source was reported in 2004 in the Rietvlei (RD) and the Marais dams (MD) in the Rietvlei Nature Reserve (RNR) in Pretoria, South Africa. A range of pesticides has been previously detected in the dams and mesenteric fat of sharptooth catfish, Clarias gariepinus, (Burchell, 1822) inhabiting the dams. These dams receive effluent from a wastewater treatment plant, as well as industrial, agricultural and domestic activities. The RD supplies the City of Tshwane with some of its drinking water and is used for angling and sailing activities. Literature from within the last two decades on the current health of these systems and the fish residing within them is lacking. The continuous monitoring and management of these systems is important as they provide
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various ecological and social benefits. It is important to determine how these systems and fish health have changed within the last two decades.
Therefore, the present study aimed to determine the reproductive health of C. gariepinus inhabiting the dams and to determine the concentrations of selected pollutants in the dam water. Clarias gariepinus (n = 70) were collected from the RD and the MD using gillnets and fyke nets. The fish were weighed and measured for the calculation of biometric (Cf) and gonadosomatic indices (GSI). Blood samples were collected for haematological analysis. The fish were euthanised and a standard necropsy was performed. The gonads were removed and processed for histological analysis, where a qualitative and semi-quantitative analysis was performed. Mesenteric fat samples were collected for pesticide analysis. The results were compared to a laboratory-bred reference group and statistical analyses were conducted. Water parameters were measured in situ and water and sediment samples were collected for chemical analyses.
Chemical analyses indicated a range of pesticides, primarily atrazine, metolachlor and propoxur present in the dam water, as well as arsenic and lead in the sediment. These pesticides are registered in South Africa. They enter aquatic systems through surface runoff and spray drift. There are various agricultural, farming and mining activities as well as a wastewater treatment plant near the RD and the MD. These activities and effluents are most likely contributing to the presence of the EDCs that were detected in water samples. Pesticides (piperonyl butoxide, bifenthrin and 4.4’–DDE) were also detected in the mesenteric fat of the fish. The accumulation of pesticides in the fat tissue of fish is one of the more concerning characteristics of EDCs as fish can be exposed to them internally over long periods, even after the chemicals have been removed from the water.
Some macroscopic gonadal abnormalities were observed, mainly in the male fish. This included discolouration, nodules and irregularly appearing testes. One of the female fish presented with abnormally shaped ovaries and a pale region on the ovary. There was also slight discolouration of the urogenital papillae of some females. There was a significant increase in the Cf of fish collected from the two dams compared to the reference group, although, Cf is considered a general indication of body condition as opposed to a reliable indicator of fish health. The GSI of the RD males increased, and decreased for the MD, compared to the reference group, whereas the females of both dams decreased. However, none of these differences were significant (p > 0.05). Haematological parameters were within the normal range, except for haemoglobin which was lower than the stipulated normal range for adult catfish.
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Developmental staging during histological analysis indicated that most of the fish were at mid- or late development, implying that sexual development is not being hindered by the pollutants present in the water. A range of histological alterations were identified in the males including testicular oocytes, vacuolation, neoplasms, increased melanomacrophage centers (MMCs), inflammation and increased connective tissue. A few histological alterations were observed in females, including increased MMCs, inflammation, structural alterations of the chorion and the accumulation of a proteinaceous substance in the interstitium. While it is difficult to attribute any particular alteration to any of the specific pollutants that were detected, as aquatic systems are impacted by a variety of factors, literature has associated these findings with the pesticides and metals present in the dam. The MD is a sludge dam and is upstream of the RD, with a wetland between the two dams. For this reason, it was expected that the concentration of pollutants in the RD would be lower, and fish health would be less affected than the MD. This was not the case as statistical analysis indicated there were no significant differences (p > 0.05) between the dams.
Analysis of plasma VTG concentrations also displayed reduced VTG levels in females, and elevated levels in males. A Spearman’s Rank Order Correlation indicated there was no correlation between VTG concentrations and histological alterations, body mass or the stage of gonadal development. These results suggest the dam water has oestrogenic effects on the fish. The present study did not observe any macroscopic indications of intersex, only the presence of microscopically visible testicular oocytes in a small percentage of the fish collected. The prevalence of intersex (in the form of testicular oocytes) has decreased compared to previous studies conducted on the RD and the MD, although it is clear that the reproductive health of C. gariepinus is still affected by the polluted water they inhabit.