The Nile River is a vital source of life in Egypt, particularly in the Greater Cairo area, where many human activities take place along the river's banks. While these activities have a detrimental impact on the water quality and biodiversity of the Nile, they also represent a potential source of parasitic infections, especially with schistosomiasis, a disease that has a long history with Egyptian human beings. Therefore, it is crucial to investigate any risks of schistosomiasis transmission represented by the presence and distribution of snails, the intermediate hosts or cercariae, the human infective stages. The distribution of the snails that transmit schistosomiasis is controlled by various biotic and abiotic factors (Gilioli et al. 2017; Habib et al. 2021) and it delineates the epidemiology of the disease (Habib et al. 2016; Habib et al. 2021). Moreover, the abundance and distribution of snails are unpredictable, making it challenging to understand their impacts on indigenous freshwater populations (Larson et al. 2020).
The chemical parameters of water for the surveyed sites along the Nile River in Greater Cairo revealed that water temperature tends to increase during the spring season (26.4–29.4ºC), which was nearly equal to that recorded during the summer season (25-31.5°C) in the current study. These results exceeded the concern level determined by the National Recommended Water Quality Criteria for temperature (25ºC) (EPA 2009). Although summer was the highest season in terms of snail numbers collected (669 snails), there was no association between temperature and the number of snails collected. This was obvious in spring, for example, where the mean temperature from all sites was 28.02°C and the number of snails collected was the lowest (179 snails) of all seasons. Temperature is a major contributor to ongoing climate change (Stocker, 2014). The change in temperature has an evident effect on schistosomiasis as it controls the distribution and reproduction of the snail intermediate hosts (Campbell-Lendrum et al. 2015). Opisa et al. (2011) found a positive correlation between temperature and the abundance of B. pfeifferi, B. sudanica, and Bulinus globosus. Mathematical modeling indicates that the effect of small temperature rises in areas where schistosomiasis is prevalent will be determined by the species of snail acting as an intermediate host. For example, the temperature range for the survival of simulated B. alexandrina populations was 12.5-29.5°C compared to 14.0-31.5°C for B. pfeifferi populations. In areas where B. alexandrina is the host, a 2°C increase in temperature can more than double the risk of S. mansoni infection (McCreesh and Booth 2014).
Under laboratory conditions, both B. alexandrina and B. truncatus have the same optimum temperature for growth and reproduction (26-28°C) (El-Emam and Madsen 1982). However, El-Khayat et al. (2009) declared that B. alexandrina and B. truncatus could tolerate a wide range of temperatures reaching 34°C. Furthermore, Joof et al. (2021) observed that water temperatures ranged from 22.1 to 38.3˚C did not show any statistically significant association with the seasonal abundance of Bulinus spp. Bulinus snails can tolerate higher temperatures due to their ability to aestivate and adapt, which explains the occurrence of S. haematobium in warmer areas than S. mansoni (Rubaba et al. 2016). Schistosomiasis transmission can occur at lower or higher threshold temperatures. For instance, S. mansoni can maintain its life cycle at low temperatures of as low as 11.5°C and high temperatures of up to 40°C (Pflüger 1982). Studies on the effect of temperature on Schistosoma japoniucm and its snail host, Oncomelania hupensis, revealed that the rise in temperature could expand the potential transmission areas of schistosomiasis japonica (Yang et al. 2005; Zhou et al. 2008). However, Stensgaard et al. (2013) expected that climate change and global warming will reduce the habitats suitable for schistosomiasis vectors in Africa.
The pH of the water was found to be neutral at all the investigated sites during different seasons. Spring and summer showed the highest and lowest snail abundance, respectively, and yet both were identical in their pH values. The impact of pH on snails’ abundance remains a controversial issue. Marie et al. (2015) found that the highest percentage of snails was recorded in the neutral pH range, while it decreased when pH was below 7 and higher than 9. Also, Makela and Oikari (1992) reported that an acidic pH level was shown to be unfavorable to the occurrence of molluscs. Similarly, Joof et al. (2021) found the abundance of Bulinus snails to increase with a decrease in water pH. Furthermore, Logronio (2020) observed that pH was negatively correlated to the number of infected snails and declared that the highest level of water pH may lead to a decrease in infection level. However, Opisa et al. (2011) did not find any correlation between pH (at 6.7–11.2) and the abundance of B. pfeifferi, B. sudanica, and Bulinus globosus.
The present work showed that dissolved oxygen was recorded at the lowest level during the summer season range of 4.25–5.92 mg/L. Previous research has found that the optimal dissolved oxygen concentration for snail intermediate hosts is between 0.4 and 16.0 mg/L (Harman and Berg 1971; Yirenya-Tawiah et al. 2011). These findings are in accordance with the present results of snail surveying, where the highest snail abundance (669) was recorded during the summer season. B. pfeifferi, B. sudanica, and L. natalensis snails prefer sites with low dissolved oxygen (Olkeba et al. 2020). The negative correlation between snail abundance and the high ration of dissolved oxygen may be attributed to the snails’ ability to occupy sites rich in organic matter (Gallardo-Mayenco and Toia 2002). With regards to total dissolved solids (TDS), the highest mean value was recorded in the autumn season, with a concentration of 273 mg/L. Biomphalaria snails can be found in habitats with extremely variable TDS concentrations. For example, Barbosa et al. (2017) found B. straminea and B. glabrata in breeding sites with TDS ranging from 148 to 661 ppm. Moreover, Allan et al. (2020) found a positive correlation between the presence of intermediate host snails and total dissolved solids. The present study indicated that the summer season had the lowest conductivity with 340.5 µmohs/cm. This is correlated with the observed highest abundance of snails during the summer season. A positive correlation was also observed with the abundance of different Biomphalaria species and low conductivity (Kazibwe et al. 2006; Rowel et al. 2015; Trienekens et al. 2022).
Melanoides tuberculata and Bellamya unicolor were the most abundant snails recorded (16.2 and 17.1%, respectively) in the current study. These findings are partially consistent with El-Khayat et al. (2017), who found M. tuberculata and B. unicolor abundances in the Nile River to be 13.9 and 16.7%, respectively. Meanwhile, the most common medically important snail species was B. truncatus, and this result agrees with the findings of Ibrahim et al. (2005), who revealed that B. alexandrina was less abundant than B. truncatus in the Nile River at Greater Cairo. On the other hand, other species of competitor snails such as Pomacea glauca, Marisa cornuarietis, Melanoides tuberculata, and Helisoma duryi may also have a role in the control of medically important snail populations (Pointier et al., 2000; Frandsen and Madsen, 1979). Also, Pointier et al. (1994) attributed the absence of B. glabrata, snail host of S. mansoni, to the invasion of Thiara granifera and M. tuberculata in the rivers of the littoral central region of Venezuela.
Several factors have been reported to introduce invasive freshwater snails into new water bodies (Yirenya-Tawiah et al. 2011; Oladejo et al. 2021). In the present work, the invasive snails, T.a scabra, were found during all seasons, with a total number of 91 individuals and an abundance percentage of 6.8%. Previous surveys have shown that the genus Thiara (Roding, 1798) was not considered to be represented in the molluscan fauna of Egypt (Ibrahim et al. 2006; Hussein et al. 2011; Abd Elwakeil et al. 2013; Abdel-Gawad and Mola 2014; Lotfy and Lotfy 2015). However, T. scabra as an invasive snail has been recorded for the first time in the Nile stream, Upper Egypt by Moustafa and Hussien (2018). These findings may be the interpretation of the current abundance of T. scabra snails at investigated sites in the Nile River. T. scabra is native to Asia with a distribution range from South and Southeast Asia, South China, and western Pacific Islands (Brandt, 1974). Its introduction to the Nile River still unknown until now. However, it might be introduced by some migratory birds. Recently, there has been an increasing interest among parasitologists in the Thiaridae family for harboring numerous species that serve as intermediate hosts of human and animal diseases. T. scabra acts as an intermediate host for different trematode species. The most dangerous ones are the lung flukes of the genus Paragonomus and the intestinal flukes (Jayawardena et al. 2010; Krailas et al. 2011; Chontananarth et al. 2017). In the present study, the findings revealed that the invasive snails were less than the indigenous species. On the contrary, Oladejo et al. (2021) found that the invasive freshwater snails were more abundant (82.15%) than indigenous species (17.85%). Also, Oloyede et al. (2017) recorded 77.17% of invasive freshwater snails at Eleyele dam, southwest Nigeria.
According to the calculated diversity index, the present results indicated that the structure of snails’ habitats was poor, while the Evenness index indicated that the individuals were not distributed equally. These results are in parallel with Mahmoud and Sayed (2018), who found 13 species of snails at 5 sites in the Damietta Governorate with a diversity index ranging from poor to bad. Also, El-Zeiny et al. (2021) studied the five stations in Damietta Governorate, Egypt, and discovered that the diversity index ranged from poor to bad. Many agricultural chemicals, the degree of aquatic pollution (Ojija 2015), and the speed of the water may lead to changes in the status of snail habitats and cause adverse effects on their distribution and population (Mahmoud et al. 2018).
No schistosome cercariae were recovered from neither B. alexandrina nor B. truncatus snails collected during the present snail survey. However, cercariometry identified Schistosoma cercariae in the investigated sites during the spring season (100% cercarial distribution), followed by autumn (42%), then summer (25%), and winter (8%). Cercariometry is a technique for determining the diurnal, seasonal, and spatial distribution of cercariae in natural water bodies. Cercariometry has some flaws in its practices and data analysis, but it does provide valuable information on active schistosomiasis transmission sites (Aoki et al. 2003). The results of cercariometry and snail sampling were significantly different. The distribution of cercariae was not positively correlated with B. alexandrina or B. truncatus numbers or the occurrence of natural infection. We couldn’t confirm whether the recovered cercariae belong to S. mansoni or S. haematobium, but we suggest that these cercariae belong to schistosomiasis haemtaobia because B. truncatus was found during all seasons while B. alexandrina was found only in the summer season. These findings show that cercariometry is more sensitive than other methods for detecting potential schistosomiasis transmission sites. This is in accordance with Yousif et al. (1996), who found that snail sampling revealed only 7 positive sites in the governorates of Kafr El-Sheikh, Ismailia, and El-Minia, whereas cercariometry revealed 45 positive sites. In Kwale, Kenya, Muhoho et al. (1997) observed an apparent discrepancy between cercariometry and snail sampling results. However, Ouma et al. (1989) discovered a moderately positive relationship between S. mansoni cercariae recoveries and the number of infected B. pfeifferi detected by sampling. Because of the complexities of transmission foci, water velocity, snail distribution, and cercarial shedding patterns from snails, establishing a precise relationship between cercarial densities and the number of infected snails is likely difficult. Furthermore, the majority of malacological surveys used to determine the natural infection of vector snails rely on a single annual sample of densely packed snail populations spread across a large area. In transmission foci where snail host species sampling is the only method used, this method may underestimate the true level of infectivity. Schistosomiasis transmission in large bodies of water such as the Nile is likely seasonal (Kloetzel and Schuster 1988). As a result, both cercariometry and snail surveys are recommended for pinpointing schistosomiasis transmission sites (Aoki et al. 2003).