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Size-dependent heavy metal and parasite bioaccumulation in Mugil cephalus from lake manzala: human health risks and fish histopathological lesions - Scientific Reports


Size-dependent heavy metal and parasite bioaccumulation in Mugil cephalus from lake manzala: human health risks and fish histopathological lesions - Scientific Reports

Pollutants, such as heavy metals (HM) and parasites, pose significant threats to aquatic environments. These contaminants can gather in fish, adversely affecting their health and potentially posing health risks to human consumers. Understanding the dynamics of these pollutants and their accumulative impact on fish of different sizes and the associated human health is crucial for the sustainability of aquatic ecosystems and food security. This study investigated the bioaccumulation of HM in the muscles of three different sizes of Mugil M. cephalus from the northeastern part of Lake Manzala, revealing significant size-related variations. Small-sized fish showed the highest levels of iron (Fe) and zinc (Zn), followed by medium-sized fish, while large-sized fish exhibited the lowest Fe and Zn concentrations. Conversely, larger fish accumulated higher levels of copper (Cu) and cadmium (Cd) compared to medium- and small-sized fish. Across all size groups of M. cephalus, the levels of both Fe and Cu exceeded the guidelines established by the Egyptian Organization for Standardization (EOS, 2005). The Metal Pollution Index (MPI) indicated that small-sized fish accumulate more HM, with medium- and large-sized fish showing lower MPI values compared to small-sized fish. In small- and medium-sized fish, Fe recorded the highest EDI values, followed by Zn > Cu > Pb > and Cd. In contrast, large-sized fish exhibited an EDI pattern of Fe > Cu > Zn > Pb > Cd for both normal and habitual consumers. Pearson correlation coefficients indicated strong negative correlations for Fe and Zn with fish size and strong positive correlations for Cd and Cu, while Pb showed a weak positive correlation. Principal Component Analysis (PCA) identified Cd, Cu, and Zn as primary contributors, with Fe and Zn showing negative loadings associated with smaller fish, and Pb had a significant positive loading in larger fish. The Target Hazard Quotient (THQ) and Hazard Index (HI) values revealed a size-related variation in health risks. Small-sized fish posed the highest non-carcinogenic risk for normal consumers; habitual consumers revealed significant health hazards (HI > 1) across all fish sizes, but it is particularly pronounced in consumers of small-sized fish. Although normal consumers recorded negligible carcinogenic risk, habitual consumers recorded low risk. The histological investigation showed significant alterations in the gills, liver, and kidneys of M. Cephalus is related to Myxobolus infection and HM accumulation, particularly Cd and Cu. Medium- and large-sized fish displayed more severe tissue alterations associated with higher HM load and increased prevalence of Myxobolus parasites. The findings emphasize that fish size is a critical factor affecting the synergistic interactions among heavy metal load and associated human health risks, parasitic infection, and histopathological lesions in fish. Underscoring the importance of continuous monitoring and risk assessment of HM and parasitic infections in aquatic ecosystems.

Heavy metals (HMs) are recognized as pervasive pollutants in various aquatic environments. Their prevalence is largely attributed to numerous anthropogenic activities, including industrial processes, agricultural practices, and urban development. In aquatic environment, fish accumulate pollutants that exist in the surrounding environment by several time in their tissue. At safe levels, essential HM including iron (Fe), zinc (Zn), and copper (Cu) are needed for fish survival and growth. However, the biological contribution of other HM such as Pb and Cd is still unidentified. HM are mostly absorbed through adjacent water, sediments, and food and accumulated in fish tissue.

Consuming HM-polluted fish can cause severe health problems. Lead (Pb) exposure can damage the brain and kidneys, causing learning difficulties and behavioral issues in children, while cadmium (Cd) is associated with kidney dysfunction, bone weakening, and cancer risks. Chronic ingesting of contaminated fish leads to bioaccumulation in the human body, increasing the risk of skin lesions, organ damage, and carcinogenesis and immune suppression.

Fish accumulate HM based on the concentration of metals, duration of exposure, habitat, feeding habits, and characteristics of the surrounding water and sediment. Moreover, some biological requirements and properties of fish such as size, which have been recognized to affect the HM accumulation rate. Consequently, advanced understanding on the associations between the biological and biometric properties of fish and HM bioaccumulation load could be beneficial from the ecological and human health perspective.

Manzala Lake contributes over 30% of Egypt's commercial fish supply. However, in the past six decades, the lake has experienced significant pollution from various sources, including agriculture, sewage, and industrial wastewater, particularly along its southern and western borders. These contaminants have severely polluted the lake, leading to a substantial decline in commercial fish production and the degradation of fish health and natural resources.

Lake Manzala receives drainage water from six major heavily polluted drains: Bahr El-Baqar, Hadous, El-Serw, Ramsis, Mataria, and Faraskur, with a combined total discharge of approximately 4000 million m per year. The Bahr El-Baqar and Hadous drains contribute approximately 75% of the total waste input into Lake Manzala, with pollution sources including both treated and raw industrial wastewater, sewage, and agricultural drainage. Additionally, the Hadous, El-Serw, Ramsis, and Faraskur drains primarily discharge agricultural water into the lake, while the Mataria drain is responsible for discharging sewage waste.

Mugilids, belonging to the Teleostei family Mugilidae, are a diverse group of fish known for their high opportunism and their presence in a wide range of habitats worldwide. They exhibit a remarkable ability to tolerate varying abiotic conditions, including salinity, temperature, sedimentary regimes, turbidity, and dissolved oxygen levels. Consequently, mullets are commonly found in coastal areas, estuaries, lakes, and lagoons, spanning both tropical and temperate regions.

The adaptability and ubiquity of mullets contribute to their exceptional survival skills and significant ecological roles. They serve as vital participants in the transfer of matter and energy between trophic levels, playing a key role in ecosystem functioning. Mullets are involved in nutrient cycling and energy flow due to their consumption of detritus, algae, plankton, and benthic organisms.

Guimarães stated that the wide distribution and significant ecological role of mullets make them susceptible to parasitic infections and diseases, as they are susceptible for various pathogens, including parasites, bacteria, and viruses. Moreover, stressful conditions such as overpopulation, poor water quality, and pollutants further increase their vulnerability.

Mullet farming in Egypt predominantly depends on the collection of wild seeds. Initially, the government set up seed collection stations to provide fingerlings to licensed fish farms. Over time, this activity has transitioned into a private enterprise with minimal government involvement. The three most commonly farmed mullet species in Egypt are grey mullet (M. cephalus), thin-lipped grey mullet (Liza ramada), and dotted grey mullet (V. seheli) are preferred due to their fast growth rates and high market demand. The striped mullet (M. cephalus) holds significant importance as a key fish species and serves as a primary cash crop for traditional artisanal fisheries scattered across various regions of Egypt.

Myxozoans are parasitic cnidarians that extensively spread in aquatic ecosystems, using fish as a temporary vertebrate host. Given the ecological and economic threats posed by many species in this group to wild and reared fish populations, studying myxozoan biodiversity in mullets is essential for sustaining natural stocks and enhancing aquaculture production.

Infected mullets with myxobolid parasites do not experience any noteworthy adverse effects other than the presence of the parasites, without instances of mortality. However, in the context of fish farms, an infection by these parasites could pose a potential risk, although the specific risks are not specified in the available information.

The life cycle of myxobolid parasites involves migrating through the fish's vasculature and establishing a persistent coelozoic sporogonic phase within the renal tubules of the posterior kidney. Tolerant hosts excrete mature malacospores into the environment, which can infect bryozoans and complete the life cycle. Surviving fish can develop a certain level of protective immunity and may be able to clear the infection and regenerate damaged tissues.

Ecoxicological research have mostly focused on the HM load of raw muscle in fish species; however, the changes of such toxic components and the related health hazards have yet to be thoroughly addressed. Continuous assessment of HM and pathogens such as myxobolid parasites in aquatic ecosystems is essential due to the significant ecological and health risks associated with these contaminants. Previous study reported that HM contamination can influence the prevalence and intensity of parasitic infections in fish, suggesting that HM may impact the immune response of fish, making them more susceptible to parasitic infections. This fish-parasite-metals interactions have been anticipated as an effective monitoring technique for evaluating the health of the fish ecosystem, with parasites signifying the presence of numerous pollutants in aquatic habitats, including noxious metals and sewage contaminants. Understanding this link is crucial for developing effective strategies to manage both HM pollution and parasitic infections in aquatic ecosystems.

This study was conducted to multifaceted an approach provides comprehensive insights into the environmental and health impacts of heavy metal contamination and parasitic infections on this crucial fish species. Through assessing the accumulation of heavy metals in various sizes of M. cephalus from the northeastern part of Lake Manzala. The primary objectives were to investigate the relationship between heavy metal accumulation and fish size and to evaluate the associated health risks of consuming these fish. Additionally, the study aimed to establish a link between Myxobolid parasite infections, fish size, heavy metal load, and histopathological lesions in the gills, liver, and kidney of M. cephalus.

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