ABSTRACT
The presence of the freshwater snail Oncomelania hupensis lindoensis in their habitats is influenced by abiotic environmental factors (nutrients, water salinity, and predators) that play a crucial role in maintaining snail survival. The objective of this study is to determine the relationship between environmental factors and the presence of O. hupensis lindoensis snails in the Napu Valley, one of the Schistosomiasis-endemic areas in Indonesia. Eight environmental factors were measured in three different habitats: a seepage, a ditch, and a pond. The study found O. hupensis lindoensis snails in all three habitats, with significant differences in their numbers (p < 0.05). The seepage habitat had the highest snail density (762.22 snails per m2) compared to the other habitats. Phosphorus levels were highest in the seepage habitat compared to the other habitats, while nitrogen levels were highest in the pond habitat. Pearson correlation analysis found a significant positive correlation between O. hupensis lindoensis snails and water salinity in the ditch habitat (p < 0.05). In addition to environmental factors, the presence of snails can also be influenced by other factors, such as the presence of snail predators, the presence of snail nutrients, and the population of snail host niche competitors.
HIGHLIGHTS
The highest densities of O. hupensis lindoensis snails were found in the seepage.
The highest phosphorus levels were found in seepage habitats. O. hupensis lindoensis snails were most abundant in this habitat.
The highest nitrogen levels were in the pond habitats. Ponds also had the lowest number of O. hupensis lindoensis snails.
The presence of snails in ditch habitats correlated significantly with salinity.
IINTRODUCTION
The Napu Valley is one of the schistosomiasis-endemic areas in Indonesia. The prevalence of schistosomiasis in humans in Napu from 2008 to 2011 was 0.3–4.8% (Satrija et al. 2015), and the prevalence decreased in 2017–2019 to 0.84–0.13% (Widjaja et al. 2021). According to the WHO road map for 2021–2030, the target for neglected tropical diseases, especially for schistosomiasis elimination, is <1% prevalence of severe intensity infection (WHO 2020). Based on this target, the prevalence of schistosomiasis in Napu is <1% in 2019. In contrast, Schistosoma japonicum infection in the intermediate snail, Oncomelania hupensis lindoensis, showed an increase. The prevalence of infected snails was 2.6% in 2011 (Sugiarto et al. 2011) and 6.23 and 6.23% in 2017 (Mardin et al. 2018).
The snail O. hupensis lindoensis is an intermediate host of the parasite S. japonicum (Colley et al. 2014). O. hupensis lindoensis is found in mountain valleys above 1,000 m. The Napu Valley is at an elevation of 1,018–1,163 m. The abiotic characteristics of the O. hupensis lindoensis snail habitat in the Napu Valley, based on previous research, are as follows: The average water temperature is 28.08 °C, the soil temperature is 25.08 °C, the humidity ranges from 60 to 78%, the water pH tends to be neutral, namely 6–6.5, the soil organic content is C = 1.67–3.72% and N = 0.27–0.59%, with <5% being low, the salinity is 0.59 ppt, and the dissolved oxygen (DO) levels in water are 3.28 mg/L (Hafsah 2013; Mardin et al. 2018).
There has been no specific study addressing the influence of nitrogen and phosphorus levels in water on the presence of the snail O. hupensis lindoensis in the Napu area. Environmental factors, including rainfall, water temperature, soil surface temperature, and water sources, can influence the presence of snails and their susceptibility to parasitic infection (Seto et al. 2008; Cheng et al. 2016; Wepnje et al. 2023). Previous research has shown that environmental ecological factors, such as temperature, pH, humidity, light intensity, DO, and salinity, significantly influence the increase in cercariae infection in O. hupensis lindoensis snails in Napu Valley and Lindu Valley (Mardin et al. 2018). The interaction between snails and parasites is influenced by environmental factors such as temperature, pH, light intensity, and salinity in the snail habitat (Donnelly et al. 1984; Yang et al. 2007; Sulieman et al. 2013). Organic matter content in snail habitat soils is significantly associated with snail presence (Manalo et al. 2023). Phosphorus found in natural water in the form of phosphate can be in the form of agricultural waste, where the use of fertilizers containing phosphate is also widely used around rice fields, which are the habitat of schistosomiasis. Similarly, nitrogen in water is in the form of ammonia, nitrite, and nitrate, where its concentration increases in water as a result of agricultural and livestock activities. These activities are commonly found in Schistosomiasis habitats.
The objectives of this study were (1) to determine the difference in the number of O. hupensis lindoensis snails found in seepage, ditch, and pond habitats; (2) to determine the relationship between the number of snails in seepage, ditch, and pond habitats with pH, temperature, salinity, DO, total dissolved solid (TDS), and conductivity; and (3) to measure nitrogen and phosphorus concentrations in seeps, ditches, and pond habitats.
METHODS
Number of samples = 3 people × 3 zippered plastic bags = 9 samples; Total number of snails in seepage habitat = 6,860 snails, ditch = 3,630 snails, pond = 2,030 snails.
The total number of snails collected in the seepage habitat was 6,860, in the ditch it was 3,630, and in the pond it was 2,030. Environmental factors were measured in triplicate for each site in each habitat, resulting in a total of three sites per habitat. The water temperature was measured using a digital water thermometer. The water salinity was measured using a portable refractometer. The water pH was measured using a digital pH meter tester. All three instruments were made by Shen Zhen Yieryi Technology Co., Ltd, Shen Zhen City, China. The DO in the water was measured using a portable DOanalyzer made by HACH Company, Colorado, USA. The TDS and conductivity of the water were measured using a TDS and EC meter LPP Co Ltd, China. The other instruments were Kjeldahl distillation (Qingdao Kemei Ltd, China) and UV visible spectrophotometer (PG Instruments Ltd, Lutterworth UK) (American Public Health Association 1992).
RESULTS AND DISCUSSION
Snail counts were conducted in three different habitats, each consisting of three sites. At each site, three collection points were used.
We found that most snails were in the seepage compared to other habitats (Table 1). Based on one-way ANOVA, habitat differences affect the number of snails found (p = 0.015) followed by a post hoc test.
Number of O. hupensis lindoensis snails at 10 sites in three habitats
Site . | O. hupensis lindoensis snail (Mean ± SD) . | ||
---|---|---|---|
Seepagea . | Ditchb . | Pondc . | |
1 | 12.33 ± 2.517 | 7.33 ± 2.517 | 3.00 ± 3.000 |
2 | 8.67 ± 1.528 | 5.67 ± 3.055 | 2.67 ± 1.528 |
3 | 11.67 ± 3.512 | 3.33 ± 0.577 | 4.00 ± 1.732 |
Snail density | |||
(Number of snails/m2) | 762.22 | 381.11 | 225.56 |
Site . | O. hupensis lindoensis snail (Mean ± SD) . | ||
---|---|---|---|
Seepagea . | Ditchb . | Pondc . | |
1 | 12.33 ± 2.517 | 7.33 ± 2.517 | 3.00 ± 3.000 |
2 | 8.67 ± 1.528 | 5.67 ± 3.055 | 2.67 ± 1.528 |
3 | 11.67 ± 3.512 | 3.33 ± 0.577 | 4.00 ± 1.732 |
Snail density | |||
(Number of snails/m2) | 762.22 | 381.11 | 225.56 |
Note: One-way ANOVA p = 0.015; F test = 9.062; post hoc ANOVA site 1, a-b (p > 0.05); a-c (p < 0.05); b-c (p > 0.05); Site 2 a-b (p > 0.05); a-c (p < 0.05); b-c (p > 0.05); Site 3 a-b (p < 0.05); a-c (p < 0.05); b-c (p > 0.05).
The seepage habitat had the highest number of snails compared to other habitats. Specifically, the seepage snail habitat had the highest pH range of 8.26–8.30, while the pond habitat had the highest water temperature of 22.90 °C compared to the other two habitats. The ditch habitat had the highest salinity levels (0.85–0.86 ppt), while the seepage habitat had the highest DOlevels (8.46–8.5 ppm), TDS 99.5 ppm, and conductivity 199.9 compared to the other two habitats. Variations were observed in the pH (7.5–7.6), temperature (20.7–20.8 °C), salinity (range 0.85–0.86 ppt), and DO (4.7–4.8 ppm) parameters of the ditch habitat.
The study found a significant positive correlation between the presence of O. hupensis lindoensis snails and salinity in the ditch habitat (p = 0.025) (Table 2).
Relationship between O. hupensis lindoensis existence and environmental factors
Environmental factors . | O. hupensis lindoensis snail (Means ± SD) (r; p value) . | ||
---|---|---|---|
Seepage (r; p) . | Ditch (r; p) . | Pond (r; p) . | |
pH | 0.176; 0.651 | −0.189; 0.627 | a |
Temperature (°C) | 0.08; 0.822 | 0.377; 0.317 | a |
Salinity (ppt) | 0; 0 | 0.734; 0.025* | a |
DO (ppm) | −0.372; 0.324 | −0.218; 0.573 | a |
TDS (ppm) | 0; 0 | 0.660; 0.053 | a |
Conductivity (vs.) | 0; 0 | 0; 0 | a |
Environmental factors . | O. hupensis lindoensis snail (Means ± SD) (r; p value) . | ||
---|---|---|---|
Seepage (r; p) . | Ditch (r; p) . | Pond (r; p) . | |
pH | 0.176; 0.651 | −0.189; 0.627 | a |
Temperature (°C) | 0.08; 0.822 | 0.377; 0.317 | a |
Salinity (ppt) | 0; 0 | 0.734; 0.025* | a |
DO (ppm) | −0.372; 0.324 | −0.218; 0.573 | a |
TDS (ppm) | 0; 0 | 0.660; 0.053 | a |
Conductivity (vs.) | 0; 0 | 0; 0 | a |
r = pearson correlation coefficient. p = probability (p < 0.05).
*p < 0.05.
The number of snails related significantly to water salinity in the ditch. No significant relationship was found between the number of snails and water quality parameters in the ponds.
Snails were more abundant in seepage which may be related to higher phosphate levels but lower total N levels than those in ditches and ponds (Table 3). In this study, we collected O. hupensis lindoensis snails in three habitats over three days, namely seepage, ditch, and pond habitats, and found that the highest number of snails was found in the seepage habitat and the other two habitats had few snails. The seepage habitat is located in Watumaeta village which is located in the middle of the garden and has many trees around the seepage. The seepage water comes from springs and rainwater. The seepage water empties into a puddle that resembles a small pond. This habitat is still naturally covered by trees and is not utilized as an agricultural field so it still has the potential for snails to breed. Previous research found that Oncomelania quadrasi snail density was significantly associated with habitat conditions covered by trees (Madsen et al. 2008). The DO level of water in the seepage habitat is high (>5 mg/L), which means that high DO levels cause the oxidation process of organic and inorganic materials. This habitat still tends to be natural because there is no human activity such as waste disposal and agriculture. Previous research found the number of freshwater snails Biomphalaria alexandrina, Bulinus truncatus, and Lymnaea natalensis by 65.12% which were found in the DO range of 0.6–8 mg/L (Marie et al. 2015).
Nitrogen and phosphor levels in sediments
Type of habitat of O. hupensis lindoensis snails . | N-total (%) . | P2O5 (mg/100 g) . | Number of snails . | |
---|---|---|---|---|
Seepage (three sites) | Mean | 0.19 | 61.05 | 10.89 |
SD | 0.072 | 1.972 | 2.85 | |
Ditch (three sites) | Mean | 0.30 | 54.27 | 5.44 |
SD | 0.047 | 4.274 | 2.65 | |
Pond (three sites) | Mean | 0.69 | 31.51 | 3.22 |
SD | 0.100 | 5.170 | 1.99 |
Type of habitat of O. hupensis lindoensis snails . | N-total (%) . | P2O5 (mg/100 g) . | Number of snails . | |
---|---|---|---|---|
Seepage (three sites) | Mean | 0.19 | 61.05 | 10.89 |
SD | 0.072 | 1.972 | 2.85 | |
Ditch (three sites) | Mean | 0.30 | 54.27 | 5.44 |
SD | 0.047 | 4.274 | 2.65 | |
Pond (three sites) | Mean | 0.69 | 31.51 | 3.22 |
SD | 0.100 | 5.170 | 1.99 |
Snails were collected using the ‘man-per-minute’ method and then collected into plastic bags, and examined at the Schistosomiasis Laboratory. The O. hupensis lindoensis snails found were 4–5 mm in size and black-brown with conical shells Hadijaja (1985). Seepage habitat also has a high salinity concentration of 0.10 ppt. Research conducted by Hafsah (2013) found that O. hupensis lindoensis snails have a fairly small size with a length of 3–5 mm a conical shell and a slightly blackish brown color (Hafsah 2013).
Based on the results of the salinity parameter research in the ditch habitat there is a significant correlation with the number of O. hupensis lindoensis snails found in the ditch. The salinity concentration of water in the ditch is 0.85–0.86 ppt (8.5–8.6 × 10–11%), and the measurement results show that it exceeds the normal standard of 0.5 ppt for fresh waters (Biscayane Bay Water Watch 2023). The correlation between the two variables is also quite high. The habitat conditions of the ditch where O. hupensis lindoensis snails were found around rice fields. The water in the ditch comes from rice fields and rainwater. Pesticide metabolites produce sulfites or sulfates that are deposited on the surface of sediments and cause the pH of the water to become acidic. The presence of S. japonicum parasites is influenced by salinity conditions, the results of laboratory testing found that the more salinity increases, the more the population of Schistosoma haematobium, Schistosoma mansoni, and Schistosoma mattheei worms decreases progressively (Donnelly et al. 1984). Similar conditions also occur in snails Biomphalaria arabica vector S. mansoni, at a NaCl concentration of 7.2% there was 100% mortality of snails in laboratory testing (Adekiya et al. 2020). Increasing salinity caused a progressive decrease in survival of S. mattheei, S. haematobium, and S. mansoni cercariae (Donnelly et al. 1984).
Another factor that also affects the presence of snails in freshwater is pH. The measurement of pH in the field shows a value that is still within the normal range in pond and ditch habitats, while for seepage habitats the pH is >7. The pH value in the three habitats does not correlate with the number of snails found. Although the pH condition is >7, snails can still live. Previous research found that Biomphalaria glabrata snails can tolerate and survive in a relatively wide pH range (O'Sullivan et al. 2011). Most freshwater snails can survive in the pH range of 7–9, whereas very few snails can live at pH <7 and >9 (Marie et al. 2015).
Freshwater temperature affects the presence of snails. A review of studies shows that temperature increases can alter the distribution, and optimal conditions for breeding, growth, and survival of schistosomiasis snails (Kalinda et al. 2017). Water temperature in the three O. hupensis lindoensis habitats ranged from 22 to 23 °C. Water temperature in the three O. hupensis lindoensis habitats ranged from 22 to 23 °C. The snails are highly adaptive to this temperature and grow normally and even faster. Studies on the effect of temperature on the growth of the snail Bulinus globosus, the intermediate vector of S. haematobium in Zimbabwe found that temperature greatly affects the growth rate of snails, namely temperatures that were >21 °C. There is a faster increase in snail shell length than temperatures below (Highveld et al. 1990). Previous research found that the temperature in the habitat of O. hupensis lindoensis was 22.3–24.1 °C (Hafsah 2013). The optimal temperature for infection in snails is 10–20 °C; the infection rate of snails decreases dramatically below 10 °C and above 20 °C (Yang et al. 2007; Li et al. 2016).
TDS under normal circumstances in fresh waters is <500 ppm (Moran 2018). The results of TDS measurements in the three habitats ranged from 49.8 to 99.5 ppm. Previous research also showed a positive correlation between TDS with the presence, abundance, and diversity of snails Bulinus globosus, Biomphalaria pfeifferi, and Lymnaea natalensis (Alhassan et al. 2020).
DO under normal circumstances in fresh waters is 9.1mg/L (200 °C), 8.3 mg/L (250 °C), and 7.0 mg/L (350 °C). At temperatures of 200 and 300 °C, the DO saturation level reached 7.0–9.0 mg/L (Nwoko et al. 2023). There is a tendency for the DO value to decrease with increasing temperature. DO levels in the three habitats ranged from 2.8 to 8.5 ppm, the pond habitat had the lowest DO levels, while the seepage habitat had highest DO levels. In contrast, the water temperature in the pond habitat was the highest compared to the seepage and ditch habitats and the seepage habitat had a lower water temperature than the other two habitats.
The results showed the highest conductivity value of 199.9 ms in seepage, 129.1 ms in ditches, and 94.9 ms in ponds. Conductivity is a measure of the ability of water to conduct electric current. Because dissolved salts and other inorganic chemicals conduct electricity, conductivity increases as salinity increases. Conductivity is also affected by temperature: the warmer the water, the higher the conductivity (United States Environmental Protection Agency 2023). Previous research found a negative relationship between conductivity and the presence of Biomphalaria snails but a positive relationship with temperature (Rowel et al. 2015). However, a preliminary study found a positive correlation between the abundance of Biomphalaria snails and conductivity (Rumi & Hamann 1990).
Total N levels in the seepage were lower than in the ditch and pond. On the other hand, snails were more abundant in seepage than in ditches and ponds. Freshwater snails are more abundant in areas with lower nitrogen levels because nitrogen is toxic to snails. Experimental results found that freshwater snails are more susceptible to nitrogen-containing fertilizers (Simplício et al. 2017). Consequently, the use of nitrogen-containing fertilizers on land that is a snail habitat may lead to a reduction in snail populations on that land.
Phosphorus is essential for the growth of organisms and can be a nutrient that limits the primary productivity of a water body. Phosphorus can stimulate the growth of photosynthetic aquatic micro- and macro-organisms in disturbing amounts. Phosphorus can be in the form of orthophosphate, which is widely applied to agricultural land as fertilizer (American Public Health Association 1992). The use of phosphorus as a fertilizer does not have a toxic effect on snails compared to nitrogen (Simplício et al. 2017).
The presence of nitrate and phosphate in freshwater ecosystems can increase eutrophication (Daldorph & Thomas 1991). In this study, nitrogen levels in the pond were found to be quite high, and algae growth was observed. Phosphorus was also detected in the pond, although the concentration was smaller than nitrogen. This is possible because the pond is close to a rice field area that has the potential to use pesticide fertilizers, causing high nitrogen and phosphorus in the pond. The accumulation of phosphorus and nitrogen causes eutrophication, which affects the decrease in vector parasite snail density due to reduced oxygen levels and increased pH (pH > 10) (Daldorph & Thomas 1991).
In addition to the physical and chemical environmental factors that can affect snail survival in freshwater, other factors outside the snail play a role. Environmental factors such as temperature, pH, salinity, DO, TDS, and conductivity are not the only factors that can affect the presence of snails but are also influenced by other factors such as the presence of snail predators and niche competitor populations of snail hosts (Cedeno-Leon & Thomas 1982).
CONCLUSIONS
O. hupensis lindoensis snails were found more in seepage habitats than in ditches and ponds. In Napu villages in Central Sulawesi, Indonesia, a significant positive correlation was found between the presence of O. hupensis lindoensis snails and salinity in the ditch habitat. Phosphorus levels, which were highest in seepage habitats, and nitrogen concentrations, which were lowest in seepage habitats, did not correlate well with the presence of the snails. The implication of this research is that it is recommended that biomonitoring of snail O. hupensis lindoensis be prioritized in water bodies with high phosphorus but low nitrogen levels.
ACKNOWLEDGEMENTS
We thank the Faculty of Mathematics and Natural Sciences and the Faculty of Agriculture, Tadulako University for support in data analysis in the laboratory.
DATA AVAILABILITY STATEMENT
All relevant data are included in the paper or its Supplementary Information.
CONFLICT OF INTEREST
The authors declare there is no conflict.