Evaluation of histopathological alterations in the gills of Vardar chub (Squalius vardarensis Karaman) as an indicator of river pollution
Graphical abstract
Introduction
Nowadays, aquatic environments are exposed to extreme pressure, as final recipients of numerous contaminants (e.g. inorganic, organic, microbiological, and pharmaceutical) from various sources (e.g. industry, mining, municipal wastewaters, and agricultural runoff). According to environmental agencies, mining effluents and agricultural runoff can be considered as the most serious threats to freshwater ecosystems (Environment Agency, 2006), the former due to high acidity and high metal concentrations and the latter mainly as a source of different types of organic contaminants. In Macedonia, mining is still one of the most important industries, with lead and zinc ores in the north-eastern part of the country being the most significant mineral deposits for exploitation (Midžić and Silajdžić, 2005). The influence of two currently active lead/zinc mines (Zletovo and Toranica) on the water quality of rivers in that region (Zletovska and Kriva) was detected, referring to contamination with number of metals and changed physico-chemical characteristics (Ramani et al., 2014). However, the sole information on water contamination is not sufficient for evaluation of the risks for health and for survival of aquatic organisms inhabiting such environments. Supplementary indicators should be analysed simultaneously, to obtain the information on effects which have arisen as a consequence of exposure of aquatic organisms to identified contaminants. Such approach to monitoring of natural waters, which links water contamination with its effects on aquatic life, is indispensable for prevention of further deterioration of affected ecosystems and for preservation of biodiversity.
Usually, the effect of contaminants is evaluated by analyses of numerous biochemical and molecular biomarkers. However, histopathology should not be overlooked in monitoring of contaminant effects, since it provides an opportunity for rapid detection of consequences of exposure to contaminants by localisation, description and even quantification of lesions that occur on selected organs of bioindicator organism (Bernet et al., 1999, Reddy and Rawat, 2013). It is, however, essential to choose wisely both bioindicator and the organ which will be examined. For this study, fish species Vardar chub (Squalius vardarensis Karaman) was selected for two reasons: first, fish are at the top of the aquatic food chain, and therefore mirror the combination of the biotic and abiotic conditions in the particular aquatic environment (Chovanec et al., 2003, Dragun et al., 2007), and second, this specific species as a member of genus Squalius, which is wide spread in European rivers, provides the possibility for comparison among distant geographical regions. Selection of appropriate organ for histopathological analyses, on the other hand, was governed by the wish to recognise the consequences of contamination events promptly after they occur. Although, the exposure of fish to chemical and microbiological contaminants could induce a number of lesions in different organs, we have chosen gills, which have been described as good indicator of current environmental conditions (Amiri et al., 2011), due to their direct and permanent contact with contaminants in the water (Bernet et al., 1999, Amiri et al., 2011), their fast response and high sensitivity even to low concentrations of pollutants (Monteiro et al., 2008).
The main aim of this study was to evaluate the possibility to use combination of qualitative and quantitative histopathological examination of Vardar chub gills as a supplementary indicator of water pollution in mining impacted rivers applying the procedure according to Bernet et al. (1999). That procedure has been widely accepted and applied for histopathology-based evaluation of water pollution (Liebel et al., 2013, Lujić et al., 2015, Rašković et al., 2015). Since chemical and microbiological water quality of three rivers in north-eastern Macedonia which were selected for this study, Bregalnica, Zletovska and Kriva, was determined simultaneously with chub sampling (Ramani et al., 2014), we were able to associate observed histopathological alterations to specific degrees and types of water contamination. Additional benefit of this study, being conducted in the field, is that it provided the possibility to assess the effect of complex mixture of contaminants on the fish showing adapted behaviours (e.g. avoidance, feeding) and physiology whilst living under realistic, natural conditions in a contaminated ecosystem (Flores-Lopes and Thomaz, 2011, Bernet et al., 2004). The importance of such approach is supported by the fact that recently several other field surveys of contamination of aquatic ecosystems, which were based on gill histopathology, have been performed in different regions in the world: in Egypt, using Nile catfish (Clarias gariepinus; Authman et al., 2013), in Pakistan, using Mozambique tilapia (Oreochromis mossambicus; Jabeen and Chaudhry, 2013), in Brasil, using fish species Astyanax aff. fasciatus and Nile tilapia (Oreochromis niloticus; Liebel et al., 2013), and in Serbia, using pike (Esox lucius), zander (Sander lucioperca) and Wels catfish (Silurus glanis; Lujić et al., 2015), as well as barbel (Barbus barbus) and sterlet (Acipenser ruthenus; Rašković et al., 2015). Since our study was conducted in two periods, spring and autumn of 2012, which differed concerning fish physiology and physico-chemical characteristic of the river water, seasonal variations of histopathological alterations on Vardar chub gills were also assessed.
Section snippets
Fish sampling
Vardar chub (158 specimens) were sampled in spring (May/June) and autumn (October) of 2012 in three rivers in north-eastern Macedonia: the Bregalnica River as the least contaminated freshwater system or a reference site, and the Zletovska and Kriva rivers as the rivers under direct influence of active Pb/Zn mines Zletovo and Toranica, respectively. The map, detailed description of the sampling area, as well as detailed physico-chemical and microbiological characterisation of the river water of
Results and discussion
Histopathological characteristics of an organ can be influenced by several other factors along with pollution (for example, fish age and size; Bernet et al., 1999). Therefore, histological examinations in this study were performed on chub of comparable size, thus including approximately one third of sampled fish (total of 52 specimens), whereas very small and big specimens were excluded (Table 1). Still, the chub from the Zletovska River were somewhat smaller and had lower condition indices
Conclusions
Histopathological alterations on the gills of Vardar chub from all three studied rivers indicated in general low water quality status of all selected freshwater ecosystems in north-eastern Macedonia. However, the reference, agriculturally impacted, Bregalnica River was characterized with the mildest changes on chub gills, among which only reversible circulatory disturbances were comparably severe as in the other two more heavily contaminated rivers. The impairments on the gills of chub from two
Acknowledgements
The financial support by the Ministry of Science, Education and Sport of the Republic of Croatia (Project nos. 098-0982934-2721 and 098-1782739-2749) is acknowledged. The sampling was carried out as a part of two Croatian-Macedonian bilateral projects: “The assessment of availability and effects of metals on fish in the rivers under the impact of mining activities”, and “Bacterial and parasitical communities of chub as indicators of the status of environment exposed to mining activities”.
References (52)
- et al.
Fish as bioindicators
- et al.
The influence of the season and the biotic factors on the cytosolic metal concentrations in the gills of the European chub (Leuciscus cephalus L.)
Chemosphere
(2007) - et al.
The impact of organochlorines and metals on wild fish living in a tropical hydroelectric reservoir: bioaccumulation and histopathological biomarkers
Sci. Total Environ.
(2014) - et al.
Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity and management implications
Fish. Res.
(2003) - et al.
Toxic effects of mining effluents on fish gills in a subarctic lake system in NW Russia
Ecotoxicol. Environ. Saf.
(2004) - et al.
Histopathological alterations of white sea bass, Lates calarifera, in acute and subchronic cadmium exposure
Environ. Pollut.
(2003) - et al.
Histopathology of rainbow trout exposed to sublethal concentrations of methiocarb or endosulfan
Toxicol. Pathol.
(2007) - Amiri, S., Vahabzadeh Roudsari, H., Kazemi, R., 2011. Histopathological studies on gill tissue of Caspian vimba (Vimba...
- et al.
Heavy metals pollution and their effects on gills and liver of the Nile catfish Clarias gariepinus inhabiting El-Rahawy drain, Egypt
Global Vet.
(2013) - Belicheva, L.A., Sharova, J.N.,. 2011. Assessment of fish health status under long-term water pollution: Vygozero...
Histopathology in fish: proposal for a protocol to assess aquatic pollution
J. Fish Dis.
Evaluation of two monitoring approaches to assess effects of waste water disposal on histological alterations in fish
Hydrobiologia
Effects of sodium fluoride in gill epithelium of Guppy fish (Poecilia vivipara)
Braz. J. Vet. Res. Anim. Sci.
Effects of the copper in the survival, growth and gill morphology of Danio rerio (Cypriniformes, Cyprinidae)
Acta Limnol. Bras.
Effects of cadmium chloride on oxygen consumption and gill morphology of Indian flying barb, Esomus danricus
J. Environ. Biol.
Histopathological alterations in gill and liver anatomy of fresh water, air breathing fish Channa punctatus after pesticide Hilban® (Chlorpyrifos) treatment
Adv. Biores.
Effect of chronic ammonia exposure on growth performance, serum growth hormone (GH) levels and gill histology of Nile tilapia (Oreochromis niloticus)
J. Microbiol. Biotechnol. Res.
Histopathological alterations observed in fish gills as a tool in environmental monitoring
Braz. J. Biol.
Cadmium tolerance in the Nile tilapia, Oreochromis niloticus following acute exposure: assessment of some ionoregulatory parameters
Environ. Toxicol.
Atlas of Fish Histology
Metal uptake and histological changes in gills and liver of Oreochromis mossambicus inhabiting Indus River
Pak. J. Zool.
Assessment of heavy metal (Cu, Ni, Fe, Co, Mn, Cr, Zn) pollution in effluent dominated rivulet water and their effect on glycogen metabolism and histology of Mastacembelus armatus
SpringerPlus
Cited by (52)
The study of acidic/basic nature of metallothioneins and other metal-binding biomolecules in the soluble hepatic fraction of the northern pike (Esox lucius)
2024, International Journal of Biological Macromolecules