In this study, I used BiomedCentral, Google, ScienceDirect, and the PubMed Database in the National Center for Biotechnology Information (NCBI) Database for searching articles on S. japonicum Sulawesi and the genus Oncomelania. Articles were published between 2011 and 2023. However, other relevant publications published before 2011 were also included.
In this study, I also used the nucleotide NCBI BLAST to assess similar identity and a tree-view rectangle cladogram (NCBI), slanted cladogram (NCBI), and rectangle cladogram from ETE3 and PhyML. I used nucleotide BLAST for two or more alignments to have accession numbers, a similar percentage identity, and a query cover percentage for Oncomelania, for example, O. lorelindoensis and O. robertsoni. For query cover, if the BLAST (megablast) showed that it was not significant, I would do BLAST for somewhat similar sequences.
The generation of a tree-view slanted cladogran was performed from the nucleotide NCBI BLAST results of GenBank. For ETE3 and PhyML sequence alignment, I used FASTA from NCBI BLAST results. Data comprise Oncomelania hupensis GU367391.1, O. minima AB611791.1, O. robertsoni KR002675.1, and O. quadrasi DQ112287.1.
Sulawesi Schistosoma japonicum
The genetic structure of the population of S. japonicum distributed over the Far East is still unclear.9 Schistosoma japonicum radiated eastward and established distinct groups in central and eastern China.10 However, Yin et al. (2015) suggested that S. japonicum originated in the middle and lower reaches of the Yangtze River and spread to Japan, the mountainous areas of China, and to Indonesia and the Philippines.9 My sequence analysis showed that Sulawesi S. japonicum originated on Laozhou Island, Tongling County, Anhui Province, China. Anhui S. japonicum KU196317.1 shares 99.80% identity similarity with Sulawesi S. japonicum KU196348.1 (Table 1). It is the highest percentage among other Chinese S. japonicum worms.
Five species of the Schistosoma japonicum complex can infect animals or humans. These include S. ovuncatum, S. sinensium, S. japonicum, S. malayensis, and S. mekongi.11-13 Schistosoma japonicum, S. malayensis, and S. mekongi cause human schistosomiasis.14 Schistosoma japonicum is the parasite that can infect humans in Sulawesi.7
Adult male Sulawesi S. japonicum worms are approximately five to 12 millimeters long, and the females are approximately 10 to 14 millimeters long. The worms are usually in pairs. Female worms are on the canalis gynacophorus of male worms. The body and tail of cercariae are thorny and thin. End of tail branched. The body is 125 micrometers long, and the tail is 180 to 230 micrometers long. There are intraspecies variations in Sulawesi S. japonicum. Adult male worms from Lindu showed consistent similarities to those from Napu worms. Adult female worms displayed distinct variations. The morphology of worms and cercariae in Lindu and Napu is the same as that in other countries,15 such as China and the Philippines.
The infection rate of S. japonicum in Sulawesi fluctuates every year. For example, the prevalence of the parasite in humans in the Bada Valley was 0.5% in 2008 and 5.9% in 2010. In 2015, the prevalence was 1.75% in the Bada Valley, 1.30% in the Lindu Valley, and 1.90% in the Napu. In 2018, the prevalence was 0.43% in the Bada Valley, 0.19% in the Lindu Valley, and 0.35% in the Napu Valley.16
Budiono et al. (2019) suggested that the prevalence of animals with S. japonicum in the Lindu Valley was cattle (61.5%), buffalo (42.3%), pigs (35.6%), horses (25%), and dogs (12.5%).2 No reports are available for the Bada Valley or the Napu Valley. In 2011, the prevalence of mice with Sulawesi S. japonicum infection was 6.8% in the Napu Valley. No reports are available for the Bada Valley or the Lindu Valley. In 2015, the prevalence of mice with S. japonicum infection was 12.50% in the Bada Valley, 8.16% in the Lindu Valley, and 7.69% in the Napu Valley. In 2017, the prevalence of mice with S. japonicum infection was 50% in the Bada Valley, 14.29% in the Lindu Valley, and 7.69% in the Napu Valley.16 These findings show that the infection rate in animals is high.
Distribution of Sulawesi Schistosoma japonicum
According to nucleotide sequences, people with S. japonicum from China, Japan, and Taiwan brought this parasite to Sulawesi, Indonesia.7 Muller and Tech found S. japonicum parasites in the feces of patients in Palu in 1937. Faust and Bonne reported adult worms in dogs, humans, and other wild-type animals in 1948.15 Carney et al. (1973) found the intermediate host of Sulawesi S. japonicum in 1971,4 and then Davis and Carney named this intermediate host O. hupensis lindoensis in 1973.17 Moreover, Nelwan (2022) named this intermediate host O. lorelindoensis along with O. robertsoni and O. quadrasi based on sequences using NCBI BLAST.7,18
Humans and birds can transmit Sulawesi schistosomiasis japonica from endemic areas. For example, in rare cases, birds may transport ingested snails long distances and secrete them alive in a new area.19 Carney et al. reported that a few cases of the disease occur in the Kulawi Valley and the Palu Valley, with individuals in these cases spending considerable time visiting or working in the Lindu Valley.4 Therefore, it could also have expanded to other new areas. These areas can include the Kulawi Valley, the Lariang River, the Palu Valley, and the Salo Karangan River. The Lariang River also flows in West Sulawesi Province. In addition, the Salo Karangan River also flows in South Sulawesi Province. This means that Sulawesi schistosomiasis japonica may have prevailed in South Sulawesi, and West Sulawesi.
Proto-Oncomelania lorelindoensis
Proto-Oncomelania lorelindoensis plays an important role in developing the genus Oncomelania. The distribution of this precursor form of Oncomelania species should be informed as much as possible. It will explain how this genus occurred.
Pomatiopsinae transmit the parasitic Schistosoma japonicum blood-fluke in China, Indonesia, and the Philippines. Pomatiopsinae are amphibious to terrestrial and have a wide distribution.8 The east-to-west hypothesis suggests that Proto-Pomatiopsinae diverges in Australia. Proto-Oncomelania colonizes northward of Australia. It was in Borneo and eastern Indonesia6 including Sulawesi and Maluku. This means that proto-Oncomelania in Sulawesi is proto-Oncomelania lorelindoensis. It is reasonable to state that all species in the genus Oncomelania originated from proto-Oncomelania lorelindoensis, with subsequent dispersal to the southern Philippines. It occurred during the Mio-Pliocene. Then, it colonizes the Far East.
Proto-Oncomelania lorelindoensis first colonized the Philippines as proto-Oncomelania quadrasi, Japan as proto-Oncomelania minima, and China as proto-Oncomelania hupensis and proto-Oncomelania robertsoni (Table 2 and Figure 1). Each proto-Oncomelania formed each species in the genus Oncomelania. All are five species.
The genus Oncomelania
The colonization of Japan would have occurred in the mid-Miocene, followed by an invasion of the Yangtze Plain of China from its east coast. At that time, the change from proto-Oncomelania gave rise to Japanese Pomatiopsinae and O. hupensis. Oncomelania hupensis colonizes China, and back-tracking recolonizes the Philippines and Sulawesi. Allozyme and DNA-sequence-based phylogenies for Oncomelania showed that the “southern continental” pomatiopsines and Japanese O. minima were similar to all other Oncomelania.6
Oncomelania snails in China may be the same species or subspecies of O. hupensis. In other Far East countries, Oncomelania snails have been considered either subspecies or independent species of O. hupensis.20 Attwood et al. (2015) introduced the idea that Oncomelania snails originated in O. hupensis,5 except for O. lorelindoensis, O. minima, O. robertsoni, and O. quadrasi.7 This supports that the genus Oncomelania has five species: Oncomelania hupensis, O. lorelindoensis, O. minima, O. robertsoni, and O. quadrasi, as suggested by Nelwan7
Both O. quadrasi and O. minima are in different groups than O. hupensis and O. robertsoni. However, O. quadrasi is closer to O. robertsoni and O. hupensis than O. minima to O. robertsoni and O. hupensis (Table 3, Figure 2). Oncomelania lorelindoensis shares 86.21% identity similarity with O. hupensis hupensis KR002674.1.21 Oncomelania quadrasi DQ112287.1 shares 84.40% identity similarity with O. hupensis hupensis KR002674.1.7 In addition, O. lorelindoensis and O. quadrasi have a 6.2 value-pairwise difference in the percentage of the 12S rRNA gene. Both have 6.4 value-pairwise differences from Yunnan O. hupensis hupensis.22 This shows that O. lorelindoensis should be in the same branch as O. quadrasi in a slanted cladogram (Figure 3), for example. However, both of them have distant family relationships.
Oncomelania lorelindoensis
The intermediate hosts of Sulawesi S. japonicum occur in Lindu and its surroundings. These include the Lindu sub-district, North Lore sub-district, and Lore Peore sub-district. These subdistricts are within Lore Lindu National Park or close to the park. Previous literature stated that intermediate hosts of Sulawesi S. japonicum originated in Chinese Oncomelania hupensis. Therefore, those authors named this intermediate host Oncomelania hupensis lindoensis.17 It is still within the Oncomelania hupensis group. My sequences show that Sulawesi Oncomelania snails are beyond the O. hupensis group because they have distant relationships. Based on that, I named the intermediate host of Sulawesi S. japonicum with the name Oncomelania lorelindoensis to replace O. hupensis lindoensis.
Oncomelania lorelindoensis has a conical shell that is yellowish-brown and clear. Snails have a size of approximately 6.5 to 7.5 millimeters of circle and a length of approximately 1 to 5 millimeters for adult snails15 with an open umbilicus. Sulawesi Oncomelania snails have lips that protrude from the base of their shell. The operculums in these snails contain a horny substance and are rather hard. The glands around the eyes of O. lorelindoensis are light yellow to bright yellow.21,23
In 2011, the prevalence of O. lorelindoensis with Sulawesi schistosomiasis japonica was 3.56% in the Lindu Valley and 0.98% in the Napu Valley. No reports are available for the Bada. In 2016, the prevalence was 5.84% in the Bada Valley and 4.96% in the Lindu Valley. No reports were available for the Napu Valley. In 2017, the prevalence was 0.81% in the Bada Valley, 3.43% in the Lindu Valley, and 7.63% in the Napu Valley.16 This shows that the infection rate in snails is high.
Habitats of Oncomelania lorelindoensis
The epidemiology of Sulawesi S. japonicum depends on the existence of its intermediate host. This is due to the development of the larval stages of S. japonicum worms that occur in the body of the O. lorelindoensis snail. The life of snails depends on the existence of suitable habitats that keep them alive.3
Habitats of O. lorelindoensis occur in two habitat areas: natural and disturbed. Natural habitats can include forests and rivers. Disturbed habitats can include rice fields and former agricultural pastures.24 Snails of this species live in muddy water, in moist places, and in watery places.25
The intermediate host of Sulawesi S. japonicum occurs in the highland of Central Sulawesi S. japonicum endemic areas. The natural habitat of the snail is in the forest borders and in the forest or lakeside. Its habitat is shrubs under large trees that are always wet.26 In addition, habitats can comprise rivers, swamps, and water seepage.24 Disturbed habitats can comprise abandoned rice fields, former farm meadows, and the edges of irrigation canals. Overall, O. lorelindoensis’s habitats in Lore Lindu National Park comprise forest (7.64%), grassland (18.06%), plantations (29.86%), and rice fields (44.44%).26 Generally, these habitats include rice fields, irrigation with stagnant water, and grass or leaf fall. This intermediate host lives in moist, watery places, but snails die when submerged in water26 for quite a long time.23
Oncomelania lorelindoensis habitat may also have occurred in the Lariang River, the Palu River, and the Salo Karangan River. The headwaters of these rivers are in Lore Lindu National Park, where Sulawesi schistosomiasis japonica endemic areas occur.7 Floods could carry snails27 from the headwaters to the lower land of the rivers, especially the Lariang River and Palu River. Snails can spread along these rivers. Potential habitats, for example, forests and rice fields along these rivers, can become new habitats for O. lorelindoensis snails. For example, birds can carry accidentally infected snails to these three rivers. Consequently, new endemic areas can occur.
The behavior of using river or ditch water in the Napu Valley has a 2.31 times higher risk of infection with the parasite compared to the behavior that does not use river or ditch water.24 This suggests that other rivers in Sulawesi can be habitats for S. japonicum worms and their intermediate hosts. This means that the Lariang River, the Palu River, and the Salo Karangan River may be potential habitats for O. lorelindoensis and Sulawesi S. japonicum. An intermediate host of Sulawesi S. japonicum may have occurred in South Sulawesi and West Sulawesi provinces. The transmission of schistosomiasis in Corsica, France, supports that schistosomiasis can occur from one river to another. In the case of Corsica, it is from the Cavu River to the Solenzara River. These two rivers do not intermingle.28
Environmental characteristics of Oncomelania lorelindoensis
Environmental factors that affect the breeding of O. lorelindoensis can include air temperature, humidity, pH, and sunlight.29 Humidity, sunlight, and temperature are the limiting factors for a snail’s life. The optimal temperature is between 16 °C and 28 °C, with a pH value between six and eight. The sun is an important factor in the existence of cercariae of the genus Schistosoma. In addition, it is important to release cercariae at water temperatures between 10 °C and 30 °C, even higher30 and between 22 °C and 25.5 °C.25
Three classes of phytoplankton are in the habitats of O. lorelindoensis. These include Chlorophycea, Cyanophycea, and Diatomae. All are feeding of O. lorelindoensis. Chlorophycea is more dominant than those of other classes. However, Hadidjaja and Sudomo (1976) stated that Diatomae are the main feeding of O. lorelindoensis.30
It seems that food, humidity, pH, sunlight, and temperature are important factors for the life of Sulawesi S. japonicum and its intermediate host. Places that are suitable for both can become new areas for these two organisms.
Control of Oncomelania lorelindoensis
Indonesia uses two approaches for controlling O. lorelindoensis: mechanic and chemical. Mechanic control is achieved by clearing focus areas, constructing drainage, backfilling, or draining focus areas. Chemically, it is through spraying niclosamide (bayluscide) molluscicide. This country has used this molluscicide since the 1980s.29 However, chemical molluscicides can damage the environment. Therefore, botanical molluscicides may be more useful for controlling O. lorelindoensis. It will not damage the environment. Botanical molluskicide sources are available for controlling Sulawesi Oncomelania. These can include Allium sativum and Buddleja lindleyana.31,32
Genetic manipulation techniques may also be useful. However, ethical issues must be fully considered before using these approaches in the field. These methods will not kill or damage the snail of O. lorelindoensis7 and will not damage the environment.