Abundance and annual distribution of freshwater snails and some trematode cercariae at Damietta Governorate, Egypt

Freshwater snails have vital roles in life where they represent a food source, contribute in recycling nutrients, and serve as bioindicators of metals in the ecosystem (Elder & Collin, 1991).

Moreover, snails are considered one of the influencing invertebrates and they have economic importance (Sharma et al., 2013). They help in maintaining good water quality for other benthic aquatic invertebrates by consuming harmful algal blooms, detritus, and organic matter (Ukam et al., 2018). However, some snail species can cause economic losses, for example the invasive golden apple snails (Pomacea canaliculata) have caused a significant ruin to the newly planted rice fields (Joshi et al., 2001; Greene, 2008). Besides, several species of the apple snails (Pomacea canaliculata and Pila polita) may also serve as intermediate hosts for larval nematodes, e.g. Angiostrongylus cantonensis that causes eosinophilic meningitis in human (Tesana et al., 2008 & Chen et al., 2011).

Most species of snails act as intermediate hosts, in which several developing larval stages such as sporocysts, rediae, and cercariae are formed (Elsheikha & Elshazly, 2008). These snails are infected by the penetrating miriacidia or by ingesting the eggs (Bdir & Adwan, 2011). Larvae of trematodes (cercariae) emerge from the snail tissue and might find the suitable secondary intermediate host or definitive host (Bdir & Adwan, 2011; Chantima et al., 2018). The genera of Biomphalaria, Bulinus, Lymnaea, Melanoides, Pomacea, and Asolene are important intermediate hosts for the trematode parasites Schistosoma, Stomylotrema, Echinochasmus, Phaneropsolus, and Fasciola (Besprozvannykh et al., 2013; Dida et al., 2014; Pinto et al., 2015; Dellagnola et al., 2019). Therefore, freshwater snails perform significant roles in the human and veterinary health (Okafor & Ngang, 2004).

Snail control methods are, thus, a requisite in order to reduce the parasites and the diseases transmitted by them (Madsen & Hung, 2014). Several biological control programs used the snail Melanoides tuberculatus as a competitor of the snail intermediate hosts of Schistosoma (Pointier & Jourdane, 2000). Furthermore, the freshwater apple snail Lanistes varicus has been considered for many years as effective biological control against snail intermediate hosts of schistosomiasis (Pointier & Jourdane, 2000; Anto & Bimi, 2017).

Environmental factors are known to affect the distribution patterns, life cycles, and population dynamics of snails (Rollinson et al., 2001). There are several biotic and abiotic factors that affect the distribution and the ecology of snails. The abiotic factors include physical factors such as water current, temperature, turbidity, transparency, and distribution of suspended solids and chemical factors such as ion concentration and dissolved gases in water. The biotic factors include availability of food, competition, and predator-prey interactions (Ofoezie, 1999). Moreover, the aquatic macrophytes (vegetation) have been shown to play vital roles in the distribution of snails in different parts of Africa (Ofoezie, 1999). One of the two River Nile branches in Egypt, Damietta Nile Branch, runs for about 242 km from Delta Barrage to the Mediterranean Sea. This branch serves as the major source of water for municipal, industrial, and agricultural uses and enriches many governorates such as El-Qalubia, El-Gharbyia, El-Dakahlyia, and Damietta (El-Amier et al., 2015). Unfortunately, freshwater ecosystem of Damietta governorate receives polluted waters from different sources including industrial, agricultural and urban sewage (Badr et al., 2013; El-Amier et al., 2015). Freshwater snails were the most dominant and evident individuals of the freshwater biota at different regions in Damietta Governorate; Bostan, Adlyia, Damietta, El-kashf, and El-Serw drainage stations (Mahmoud & Sayed 2018).

Surveying snails, especially the species involved as intermediate hosts of digenetic trematodes, are needed for disease control (Rozendaal, 1997). It is crucial to know the habitat, ecological factors, and distribution of the freshwater snails especially the medically and economically important species. Unfortunately, few studies addressed the ecology and population dynamics of the freshwater snails in Egypt (Hussein et al., 2011; Marie et al., 2015; El-deeb et al., 2017; Mahmoud & Sayed 2018). Because of this and the unique freshwater ecosystem of Damietta governorate, the present study aimed to (1) survey the freshwater snails in selected sites at Damietta governorate, (2) determine the abundance of these snails and the seasonal changes in their abundance, (3) investigate whether there is a correlation between the abundance of these snails and some physicochemical parameters, and (4) address the seasonal changes in the snails’ cercarial contents and investigate whether there is a correlation between their prevalence and some physicochemical parameters.

In the present study, seven different freshwater snail species were identified and their distribution was evaluated at 5 different collection sites. The relation between the abundance of these snail species and the physico-chemical water quality was also studied. The Shannon diversity index status of the present investigation at 5 the study sites ranged from poor to bad status. The snails at Al-Inaniyyah and Izbat Al-Basartah villages were almost similarly distributed with high snail diversity and richness. While, the snails at EL-shenawy village, EL-Serw, and Kafr EL-Manazlla village were distributed with low diversity and richness. The same results were also confirmed by the multivariate analysis (CCA). In a recent study, Mahmoud & Sayed (2018) recorded 13 species of snails at 5 sites in Damietta governorate with a diversity Index (H′) status ranging from poor to bad status. Although the study was conducted in the same governorate but at different study sites its results coincides with our data. This may give an indication of stable snail coexistence in the same ecosystem. According to Dung et al. (2010), Mohammed et al. (2016), and El-deeb et al. (2017), many factors affect the density and distribution of snail species. These factors include, but not limited to, the use of agriculture’s chemicals, degree of pollutants, and the speed of the water that may be high during the initial period after an irrigation cycle.

Lanistes carinatus was the most predominant snail species in the study with 56.4 % abundance. Consistent with this result, Lanistes carinatus was reported as the most abundant snail species at three Egyptian governorates; Giza, Damietta, and Minya (Mahmoud & Sayed, 2018). Inconsistent with these reports, Hussein et al. (2011) found that the majority of the collected snails at El-Kelabia irrigation canal and the River Nile at Qena Governorate in the south of Egypt was of the species Cleopatra bulimoides (1704 specimens, 25.17 %). In Africa, Igbinosa et al. (2015) reported the abundance of the snail species Lanistes varicus, which constituted 44.6 % of the collected snails at Ovia, Edo state in Nigeria. Outside Africa, Chantima et al. (2018) reported that about half of all snails collected from August 2016 to October 2017 in Mae Lao agricultural basin, Chiang Rai in Thailand, were of the species Bithynia siamensis (54.6 %).

In the current study, only two cercarial types (gymnocephalus cercariae and xiphidiocercariae) were detected in Lanistes carinatus at the 5 different study sites. The external features of the gymnocephalus cercaria in the present investigation were consistent with the characteristics of the gymnocephalus cercariae emerging from Bellamya aeruginosa (Xiao et al., 2005). The morphological features of the xiphidiocercariae in the current study were also consistent with the characteristics of the xiphidiocercaria harvested from Asolene platae (Dellagnola et al., 2019). Based on our results, only Lanistes carinatus was intermediate host for transmitting trematodes larvae at Damietta Governorate. On the contrary of this, Yousif et al. (2010) recorded four main cercarial types (xiphidiocercariae, furcocercous cercariae, pleurolophocercous, and gymnocephalus cercariae) in the snail Melanoides tuberculata that was the most infected snail at the irrigation canal and the River Nile at Giza Governorate in Egypt. In the present study, the highest prevalence of cercariae was detected at the Nile’s Damietta Branch in Kafr EL-Manazlla village, (4.53 %). Similar to our results, Mohammed et al. (2016) reported xiphidiocercariae as the most common type of cercariae (44.3 %) but from the snail Bulinus truncates at the irrigation canal in the East Nile, Khartoum, Sudan. In addition, Mereta et al. (2019) reported the highest infection rate of xiphidiocercariae (1.5 %) emerging from Lymnaea natalensis at wet land of Omo-Gibe River Basin, southwest Ethiopia. According to Mereta et al. (2019), human activities such as open field defecation, urination, livestock grazing, farming, and swimming were highly correlated with trematode infection. Being industrial and agricultural governorate, it is unlikely that the latter factors only determine trematode prevalence and diversity in Damietta Governorate.

Our results showed that the prevalence of snail species varied during the four seasons. The highest snail abundance was recorded during summer while the lowest abundance was during winter. CCA analysis revealed that the density of the most snail species was high during summer and spring except Pila wernei, which was high during winter. The feeding habits of each snail species could affect its seasonal occurrence. The higher density of snails recorded in the dry season was thought to be due to the occurrence of microflora (food supply) and aquatic macrophytes (Salawu & Odaibo 2014). According to Kazibwe et al. (2006) and Oloyede et al. (2017), some freshwater snails are herbivores and more abundant during the late rainy seasons due to increase in light intensity and hence, the increased photosynthesis and the more abundance of the aquatic macrophytes. Similar to our results, Igbinosa et al. (2015) recorded an increase in the abundance of Lanistes varicus from August to September at Ovia, Edo state, Nigeria. These authors believed that the feeding habits and light are important factors in the seasonal fluctuations of the snail prevalence. Based on a study in the south of Egypt, Hussein et al. (2011) reported varied snail densities during the different seasons, with the highest seasonal peak recorded during autumn while the lowest was during winter. It is noteworthy to report the considerable increase in the temperature in the south of Egypt compared to the north. According to Hussein et al. (2011), Lanistes carinatus showed a maximum reproduction during summer, the highest number of Gabbiella senaariensis was recorded during winter, while Biomphalaria alexandrina showed March – May peak and reached the highest number in April. Our findings are in consistence with the report of Marie et al. (2015) that the snails Biomphalaria alexandrina and Lanistes carinatus showed the highest peak in spring at four northern Egyptian governorates; Giza, Ismailia, Menoufia, and Gharbia. Pointier et al. (1993) recorded a maximum reproduction of Melanoides tuberculata between June and November. Beyond the feeding habits, Islam et al. (2015) reported that late summer provides an optimum temperature for the breeding and reproduction of snails. According to our results the gymnocephalus cercariae disappeared during winter and the highest prevalence of these cercariae was recorded during spring. While, the xiphidiocercariae were detected during the four seasons with the highest prevalence was during summer. The effect of climatic changes on trematode occurrence has been documented in several studies. Islam et al. (2015) revealed that the prevalence of the gymnocephalus cercariae emerging from Lymnaea sp. varied significantly with seasonal changes and reached a peak in April – October then decreased in February – March, and disappeared in November – January. The higher abundance of snails during summer, as recorded in the current study, and dry seasons in general might lead to increased cercarial prevalence as it will be easier for the miriacidia to find new snails for infection. The mean value of water temperature in the current study was slightly similar between the 5 sites and ranged from 21.75 – 22.29°C. This temperature is thought to be suitable for increasing the population density of snails and the emergence of cercariae from snails. According to Yirenya-Tawiah et al. (2011), the temperature ranging from 27.4 – 33°C is suitable for the survival of snails. Marie et al. (2015) revealed that the mean values of water temperature ranged from 23.5 – 25.7°C at seven sites in the four northern Egyptian governorates; Giza, Ismailia, Menoufia, and Gharbia. The highest occurrence of the snail Biomphalaria alexandrina was recorded at 28°C and 31°C in two northern Egyptian governorates; Giza and Kafr El Shiekh (El-deeb et al., 2017). Salawu & Odaibo (2014) reported the suitability of the water temperature range 21.7 – 29°C in all river bodies at Ogun state, Nigeria, for the survival of aquatic snail species. Islam et al. (2015) revealed that the suitable water temperature needed for the development of gymnocephalus cercariae in Lymnaea sp. was 18 – 34 ºC, while Mohammed et al. (2016) suggested that the proper mean value of water temperature needed for the development of xiphidiocercariae in Lymnaea natalensis and Bulinus truncatus was 16 – 28 ºC. The distribution of most snail species (except Pila wernei and Segmentorbis angustus) and the two types of cercariae in the current study were positively correlated with water temperature. Our findings are consistence with Hussein et al. (2011) study, which revealed a positive correlation between water temperature and the abundance of Lanistes carinatus, Melanoides tuberculata, and Biomphalaria alexandrina.For the snails Segmentorbis angustus, Salawu & Odaibo (2014) observed a negative correlation between the water temperature and the abundance of the snail. Sunita et al. (2012) reported a direct correlation between the prevalence of gymnocephalus cercariae emerging from Lymnaea snails were and the water temperature. Also, Mohammed et al. (2016) reported a direct correlation between the distribution of xiphidiocercariae emerging from Lymnaea natalensis and Bulinus truncatus and water temperature. In addition to its influence on the abundance of aquatic snails, water temperature is thought to influence the rate of parasite development in the snail host, and probably the distribution of the related disease (McCreesh & Booth 2014).

In the current study, the mean value of water dissolved oxygen ranged from 6.44 – 7.02 mg/l. Several reports have addressed the importance of a suitable range of oxygen concentration for the snail activity, feeding, and reproduction. Salawu & Odaibo (2014) recorded mean dissolved oxygen of 6.1±4.6 mg/L at Ogun state, Nigeria. According to our results, the distribution of most snails, except Pila wernei and Segmentorbis angustus, were negatively correlated with the value of dissolved oxygen. These results are supported by Hussein et al. (2011) who revealed that the water DO was negatively correlated with the abundance of Lanistes carinatus, Melanoides tuberculata, and Gabbiella senoriansis, and that DO was positively correlated with the abundance of Biomphalaria alexandrina. According to Sharma (1986), some snails could survive in very low oxygen conditions. However, Ofoezie (1999) reported that the density of some pulmonate snails, e.g. Bulinus sp. and Lymnaea natalensis, increased with the increase in DO value. Our results showed a positive correlation between the distribution of gymnocephalus cercariae and the value of DO, while xiphidiocercariae distribution was negatively correlated with DO. Similar to our results, Mereta et al. (2019) reported a negative correlation between the prevalence of the xiphidiocercariae emerging from Lymnaea natalensis and water DO. However, Sunita et al. (2012) recorded a negative correlation between the prevalence of gymnocephalus cercariae and water DO ranging (1 – 6.02 mg/l). This discrepancy could be due to the difference in concentration and range; in the study of Sunita et al. (2012) the DO ranged from 1 to 6.02 mg/L

According to our results the mean values of TDS and EC of the collected water samples ranged from 385.5 – 823.58 ppm and 570 – 1380 μS/cm, respectively. Close to our results, Marie et al. (2015) revealed that the values of TDS and EC ranged from 369.5 – 1221 ppm and 530 – 2155 μS/cm, respectively, at eight sites in the northern Egyptian governorates Giza, Ismailia, Menoufia, and Gharbia. However, Hussein et al. (2011) indicated that the values of TDS and EC ranged from 145 – 638 ppm and 240 – 930 μS/cm, respectively, at six sites in Qena Governorate in the south of Egypt. The latter values reflect the different nature of water at the southern governorates (e.g. Qena) in Egypt, where the river Nile starts its journey in Egypt and the water quality is considerably different. Rowel et al. (2015) observed that the values of TDS and EC ranging from 58 – 568 ppm and 112 – 1081 μS/cm, respectively, are suitable for the survival of Biomphalaria at six locations in Ugandan shores of Lake Albert and Lake Victoria. Yirenya-Tawiah et al. (2011) revealed that a total EC range from 70 – 122 μS/cm is suitable for the survival of the snail intermediate host for schistosomiasis. Based on our results, the distribution of most snail species Lanistes carinatus, Lanistes varicus, and Melanoides tuberculata was negatively correlated with the mean values of TDS and EC. These snail types might be detected at a wide range of water TDS and EC. Similar to our findings, Yigezu et al. (2018) observed an association of the distribution of snail species with the highest EC values. Hussein et al. (2011) observed a negative correlation between the abundance of Lanistes carinatus, Gabbiella senaariensis, Melanoides tuberculata, and Biomphalaria alexandrina and TDS and EC. Also, Salawu & Odaibo (2014) observed a negative correlation between the abundance of Lanistes lybicus and Melanoides tuberculata and TDS and EC. Moreover, Rowel et al. (2015) and Marie et al. (2015) detected a negative correlation between the abundance of Biomphalaria alexandrina and EC and suggested that this snail species might have a limit range of water conductivity permitting it to live whatever in the flowing or stagnant water. The distribution of gymnocephalus cercariae and xiphidiocercariae was negatively correlated with the values of TDS and EC. Similarly, Mereta et al. (2019) revealed that the prevalence of the xiphidiocercariae emerging from Lymnaea natalensis was negatively correlated with water conductivity and were detected at 159 μS/cm, while echinostome cercariae were found at 181 μS/cm of water conductivity.

The mean value of pH in the current study ranged from 7.47 – 7.74. This range is slightly alkaline and might be suitable for the existence of the different snail and cercariae species. El-deeb et al. (2017) revealed that Biomphalaria alexandrina survived in almost the same range of water pH 7.22 – 7.33 in the two northern Egyptian governorates Giza and Kafr El Shiekh. Hussein et al. (2011) recorded pH values ranging from 6.4 – 7.9 at six sites in Qena Governorate in the south of Egypt. In addition, Opisa et al. (2011) found that snails survive at a wide range of water pH (6.7 – 11). In the present study, the abundance of most snail species was negatively correlated with pH except Biomphalaria alexandrina. Our findings are in consistence with Hussein et al. (2011) who reported a negative correlation between the water pH and the abundance of Lanistes carinatus, Gabbiella senaariensis, and Biomphalaria alexandrina. Marie et al. (2015) recorded a negative correlation between the abundance of Biomphalaria alexandrina and pH levels. Salawu & Odaibo (2014) reported positive correlation between the water pH and the abundance of the snail Segmentorbis angustus. Opisa et al. (2011) and Salawu & Odaibo (2014) suggested that snail abundance is independent of water pH value fluctuations. Because of the conflicting reports, it seems that the effect of water pH on snail abundance is limited. Our results showed that the distribution of gymnocephalus cercariae is positively correlated with water pH, while the xiphidiocercariae distribution is negatively correlated with water pH. Sunita et al. (2012), Yigezu et al. (2018), and Mereta et al. (2019) reported a direct correlation between the prevalence of both of echinostome cercariae and xiphidiocercariae and the pH. It worthy to report that, the pH ranges in all sites of the current study were very close and the range was very narrow (7.47 – 7.74).

According to the current results, only two types of trematode cercariae; gymnocephalus cercariae and xiphidiocercariae, were harvested from the same snail, Lanistes carinatus and the total prevalence of xiphidiocercariae was higher than that of gymnocephalus cercariae. The relatively low prevalence of gymnocephalus cercariae that emerged from this snail may be due to the antagonism by xiphidiocercariae. Mohammed et al. (2016) suggested that the low prevalence of furcocercous cercariae emerging from Bulinus truncates could be due to antagonism by xiphidiocercariae, which were found with high rates. Antagonism involves complex interactions amongst larval trematode species and it has predictable outcomes that can influence patterns of abundance among these species. Interspecific competition for resources and space represents a potentially strong selection pressure for trematodes infecting snail hosts (Hechinger et al., 2011). Laidemitt et al. (2019) observed an obligatory dependence of some digenetic trematode species on Biomphalaria snails for their larval development and they reported that the larval stages of these species might strongly interact with the larvae of Schistosoma mansoni for access to the resources offered by these snails. There is a possibility that xiphidiocercariae in the current study might be competed with other trematode larvae (gymnocephalus cercariae) for infecting Lanistes carinatus. The definitive hosts for xiphidiocercariae and gymnocephalus cercariae are different (Insectivorous bats and fish-eating birds or mammals, respectively) and, also, the secondary intermediate hosts for these two cercarial types are different (Damson or dragon fly nymphs and fish, respectively). Although it is unlikely, it is possible that the difference in the existence and abundance of these hosts could affect the life cycle and the natural occurrence of xiphidiocercariae and gymnocephalus cercariae.

According to our findings, the apple snails Lanistes carinatus and Lanistes varicus were detected at the 5 studied sites in Damietta governorate. Although, these snails might act as pests for agriculture fields, they may serve as medically and ecologically important factors by consuming aquatic weeds and reducing schistosomiasis. Anto et al. (2005) reported that Lanistes varicus has the ability to control the intermediate host snail of intestinal schistosomiasis. Also, Anto & Bimi (2017) revealed that Lanistes varicus snail feeds on the egg masses and juveniles of Bulius truncatus snails. Our findings, therefore, suggest that the invasion of some Ampularidae freshwater snails (Lanistes carinatus and Lanistes varicus) in Damietta governorate may be the cause of the low abundance of Biomphalaria alexandrina and the absence of Bulinus and Lymnaea genera, which were not detected at all in the current study in spite of the extensive search. The invasion of Lanistes carinatus by xiphidiocercariae in Damietta governorate might be the cause of the low infection of this snail with gymnocephalus cercariae, and the absence of Schistosoma larval stages at all sites in the present investigation.

To conclude, the abundance of snail species varied between the five locations in Damietta governorate and was correlated positively or negatively with some physico-chemical parameters. The invasion of the freshwater snails Lanistes carinatus and Lanistes varicus in Damietta governorate may be the cause of the low abundance of Schistosoma intermediate hosts. The invasion of Lanistes carinatus by xiphidiocercariae may be the cause of the low prevalence of gymnocephalus cercariae and the complete absence of Schistosoma larval stages at all the studied sites. Our study recommends further characterization of the snail distribution and the snail interrelationships and suggests a controlled use of the Ampularidae freshwater snails in the biological control of parasite intermediate hosts.