Abstract
Foodborne zoonotic trematodiasis is a public health problem in many countries. A study on digenean larvae (cercariae stage) obtained from snails in all ten main small canals and two rice fields was carried out in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh city, Vietnam to identify the snail composition and digenean prevalence in snails. The snails were sampled in the dry season (January 2022) and the wet season (June 2022). In the ten canals, 23 snail species belonging to 16 genera, 10 families from the samplings were found; however, there were no cercariae in these 23 snail species. In the two rice fields, 11 snail species in 11 genera and 7 families were collected. In which, Bithynia siamensis in Ly Nhon rice field and Thiara scabra in Binh Khanh rice field infected xiphidio cercariae. For Bithynia siamensis, the prevalence in the dry season (5.6%) was higher than in the wet season (4.6%) (P > 0.05). In Binh Khanh rice field, only one Thiara scabra infected cercariae in the wet season. Further research on digenean infection in different months and in other water bodies in Can Gio Mangrove Biosphere Reserve should be done to contribute to the control of digeneans and reserve the biodiversity.
Keywords: Digeneans, Snails, Mangrove biosphere reserve, Vietnam
1. Introduction
Can Gio Mangrove Biosphere Reserve is located in Can Gio, the coastal district southeast of Ho Chi Minh City, Vietnam. The Biosphere Reserve was divided into three zones: the core zone (4720 ha) was for conservation, research, monitoring, and human activities were prohibited in this zone; the buffer zone (37,340 ha) was as a protective buffer for the core zone, and tourists could come to visit; the transition zone (29,310 ha) which surrounds the core and buffer zones was for socio-economic development (1). Therefore, Can Gio is a very different area from other places in Vietnam. The research in 2019 in this area finds that the digenean prevalence of wild fish in canal in Ho Chi Minh City is 80% [1], and Sea bass (Lates calcarifer) cultured in ponds in Can Gio Mangrove Biosphere infects digenean (metacercariae stage) with the prevalence at 0.8% [2]. However, no research on snails and cercariae in snails in this area is carried out.
The study on trematode is needed as foodborne zoonotic trematodiasis are a public health problem in many countries in the world [3], especially in Southeast Asia [4]. Humans are often infected by helminth parasites transmitted from fish [5] and crustaceans [6]. Freshwater snails play a role as the first intermediate host in the life cycle of digeneans. The distribution of foodborne trematodes depends on the relationship between the hosts, parasite, environment and eating habits [6]. For example, large liver flukes can cause disease in humans and livestocks [7]; common symptoms when infected with Fasciola hepatica are epigastric pain, upper abdominal pain, and malaise, even having fever and arthralgia [8], and fascioliasis can be associated with long-term complications such as anemia and malnutrition [7]. There is not much information about the clinical importance of infections with minute intestinal flukes, but heavy infections can cause serious gastrointestinal symptoms [9] while small liver flukes cause significant human-health impact and substantial clinical or sub-clinical disease [10]. For lung flukes, adult worms can cause focal haemorrhagic pneumonia when they migrate in the tissue [6].
Snails are the first intermediate hosts everywhere where trematodes are transmitted [11]. Snails belonging to the Lymnaeidae family are the first intermediate host of large liver fluke [7]. Lymnaea viridis and Lymnaea swinhoei are the intermediate hosts for Fasciola gigantica in Vietnam [12]. The natural snail host of Paragonimus siamensis in Thailand is Filoparudina martensi [13]. Two species of snails including Oncomelania sp.1 and sp.2 are the first intermediate hosts of Paragonimus in Vietnam [14]. Ten species of snails belonging to four families is the first intermediate host for Clonorchis sinensis [15]. The first intermediate snail species of C. sinensis in China, Taiwan, Korea and Japan is Parafossarulus manchouricus [16]. Parafossarulus, Bythynia and Alocinma spp. are the first intermediate snail host of C. sinensis, and Bythynia spp. is the host of O. viverrini and Codiella spp. for Opisthorchis feliensis [17]. Two species of Bithynia snails is found to be the first intermediate host of Opisthorchis viverrini in Thailand [18]. Melanoides tuberculata, P. manchouricus and Maningilla sp. are the first intermediate hosts of liver flukes in Vietnam, in which M. tuberculata is the most common species [19]. However, M. tuberculata and Tarebia granifera are not suitable first intermediate hosts of C. sinensis in Northern Vietnam [20]. M. tuberculata, Thiara and Terabia granifera are the first intermediate hosts of heterophyids [21]. M. tuberculata is the host of Haplorchis pumilio [[22], [23], [24]] and the host of Centrocestus formosanus [25]. Thiara granifera is found commonly infected with H. pumilio in Taiwan [23], C. formosanus in Thailand [24] and Stellantchasmus falcatus in Hawai [26]. Pirenella spp. of snails is the first intermediate host for H. heterophyes and Semisulcospira spp. provides the snail hosts for M. yokogawai [17]. Species of the Bithyniidae, the Stenothyridae and the Planorbidae dominated in rice fields and small canals, and M. tuberculata are found to be highest FZT prevalence among eight snail species [27].
In Vietnam, snail composition and distribution has been studied for a long time. There are 47 freshwater snail species in the North of Vietnam [28]; and sixteen snail species distributes in ponds, rivers, streams, canals and rice fields in two communes of Nghia Phu district, Nam Dinh province [27]. In the Central of Vietnam, 11 snail species is collected in An My and An Hoa communes, Tuy An district, Phu Yen province [29]. In the Mekong Delta of Vietnam, 14 freshwater snails is found in Vinh Long and Dong Thap provinces [30]. In 2015, 137 freshwater snail species have been recorded from Vietnam and 94 of them is assessed in IUCN list [31]. In Can Gio Mangrove Biosphere Reserve, 19 snail species belonging to 16 genera and 13 families are collected from 4 research points in the wet season 2010 and the dry season 2011. In which, total snail species in the dry season in Can Gio mangrove forest is higher than in the wet season with the highest number of snail species in the canal [32].
Trematode infections are found in eight snail species in snails in Nam Dinh province in the North of Vietnam [27]. The study in 2013 shows that the presence of cercariae in three snail species of Bithynia fuchsiana, Parafossarulus striatulus (the Bithyniidae) and Melanoides tuberculata (the Thiaridae) and records 12 cercariae species of 8 families [33]. Five groups of cercariae from 11 snail species were found in Phu Yen province in 2014 [29]. In 2015, three cercariae groups are recovered from 7 snail species, in which Melanoides tuberculata has the highest prevalence [34]. Nine snail species infected with cercariae in Ninh Binh province and Ha Noi city [35].
The above information showed that there were a lot of studies on snail composition and cercariae from snails in Vietnam. However, all this research was done in the agriculture and aquaculture areas in Phu Yen, Nam Dinh, Ninh Binh and Ha Noi, and there was no research in the Mangrove Biosphere Reserve in Can Gio, the first Mangrove Biosphere Reserve in Vietnam, where are rich in mangrove fauna comprising 210 species of planktonic and benthic organisms, 19 species of mammals, 133 species of birds, 283 species of fishes [36], 46 species of reptiles and amphibians [37], 204 species of crustaceans, gastropoda, bivalves, and 89 species of insects [38]. Therefore, a study to investigate the digenean infections in snails and snail composition in canals and rice fields in Can Gio Mangrove Biosphere, Ho Chi Minh City is implemented to contribute to the control of digeneans and conserve the biodiversity. The results can use to find the strategy to reduce the trematode prevalence in fish and the harmful snaisl for aquaculture and agriculture in Can Gio area.
2. Materials and methods
2.1. Study sites
The study site of Can Gio Mangrove Biosphere Reserve is in Can Gio district of Ho Chi Minh City, Vietnam (Fig. 1).
Fig. 1.
Map showing location of the study area of Can Gio Mangrove Biosphere Reserve.
Snails were mainly distributed in canals, fishponds and rice fields with the highest trematode prevalence in small canals [39], so rice fields and canals were considering choosing for the study because most of ponds in Can Gio were for shrimp culture. According to Decision No 2580 by Ho Chi Minh city People's Committee dated July 20, 2021 [40], there were 10 sixth-level canals in Can Gio Mangrove Biosphere Reserve. The sixth-level canal was the lowest range in the waterway system in Ho Chi Minh city which was connected directly to the smaller canals linking with rice fields, fish farms, residential areas and wetlands. The water in all 10 sixth-level canals in Can Gio Mangrove Biosphere Reserve was brackish. For the rice fields, using completely rainwater, Decision No 2816 by Ho Chi Minh city People's Committee dated July 01, 2019 [41] showed that three communes and one town cultivated rice including Binh Khanh (69.58 ha), Ly Nhon (62.85 ha), An Thoi Dong (0.15 ha) and Can Thanh town (0.11 ha) in Can Gio. Therefore, ten sixth-level canals and two large rice fields of Binh Khanh and Ly Nhon were chosen for the research in January and June 2022 (Table 1).
Table 1.
Total sampled canals and rice fields in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam.
| No | Name of canals/Rice fields | Zone | Sampling in the dry season (January 2022) | Sampling in the wet season (June 2022) |
|---|---|---|---|---|
| A | The sixth-level canals | |||
| 1 | Tan canal - Bong Gieng Lon canal | Transition zone | 4 | 4 |
| 2 | Duoc canal - Sau Quan canal -Lap Doi canal | Transition zone | 4 | 4 |
| 3 | Goc Tre canal | Transition zone | 4 | 4 |
| 4 | Ca Nham Lon canal | Transition zone | 4 | 4 |
| 5 | Long Thanh canal | Transition zone | 4 | 4 |
| 6 | Mong Ga canal - Tac Moc Mu | Core zone | 4 | 4 |
| 7 | Don canal | Transition zone | 4 | 4 |
| 8 | Duoi Ca canal | Buffer zone | 4 | 4 |
| 9 | Tac An Tet - Tac Cau Kho canal | Buffer zone | 4 | 4 |
| 10 | Tac Cong canal | Core zone | 4 | 4 |
| B | Rice fields | |||
| 11 | Binh Khanh | Transition zone | 15 | 15 |
| 12 | Ly Nhon | Transition zone | 15 | 15 |
2.2. Sampling of snails
Two cross-sectional studies on snails were carried out in January 2022 (the dry season) and in June 2022 (the wet season). Four samples from four different habitats, the natural environment where snails lived, were done in each canal and 15 samples were collected in each rice field. Water environment like temperature and pH at the sampling points in each season were measured.
In canals, quantitative snail sampling was done by using a 25-cm wide dredge to scrape the canal bottom from 1.0 m out from the bank and back to the edge. Each point was sampled once in the dry season and once in the wet season. Each sample was transferred to cloth bags and transported to the laboratory where they were analyzed within 24 h of collection. Four habitats for samling are different from each other [Fig. 2(a-d)]: the first point has no grass, no trees, and no aquatic plants (Fig. 2a); the second point has grass and aquatic plants but no trees (Fig. 2b); the third point has aquatic plants and trees on the canal bank but no grass (Fig. 2c); the fourth point has grass on the side of canal bank but no trees and no aquatic plants (Fig. 2d).
Fig. 2.
Examples of four different habitats for sampling.
In rice fields, snails were collected by hand along the rice field bank in the area of 0.4 m wide × 10 m long, and each sampling point is 500 m far from each other. The first sampling point at the beginning of the main path at the edge of the rice field and the next sampling points were continued along this path.
2.3. Examination of snails for cecariae
Snails were examined for digenean infection (cercariae stage) by shedding method [27,42] in the containers of 250 mL beakers, and left for 24 h for shedding, and then checked in three days for cercariae at 8:00AM and 2:00PM each day. Each snail was kept separated in the different beakers filled with water and kept at the room temperature. All beakers were covered by a tray to prevent snails to escape. Water in each beaker was poured into the Petri dish and checked cercariae under the stereo miroscope and then optical microscope. Morphological methods were used to identify snails following the key by Dang et al. (1980) [28] and cercariae was identified following the keys by Frandsen and Christensen (1984) [42] and Shell (1985) [43]. Specimens of each snail species were preserved separately in the small plastic bottles filled with 70 percent ethanol and all cercariae were kept in the small bottles filled with 4 percent formalin, such that identifications could later be verified. All of these plastic bottles with specimens were kept in the laboratory of Department of Biology.
2.4. Data analysis
Microsoft Excel 2010 was used for data entry and SPSS (Statistical Package for Social Sciences version 20; SPSS Inc., Chicago, Illinois) was applied for data analysis. The Chi-squared test was used to compare the difference of digenean prevalence (cercariae stage) between two sampling times. A value of P < 0.05 was considered significant.
3. Results
Snail composition and distribution in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam.
The result from two samplings of snails in three zones of Can Gio Mangrove Biosphere Reserve showed that 34 snail species belonging to 27 genus and 17 families was collected and identified by morphological methods. In which, 23 snail species in 16 genus and 10 families was collected from 10 canals, and 11 snail species in 11 genus and 7 families was got from the two rice fields (Table 2). Total snail species were found differently in the three research zones with 11, 14 and 30 snail species in Core zone, Buffer zone and Transition zone, respectively.
Table 2.
Snail samples in canals and rice fields in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam (January and June 2022).
| Family | Genus | Species | Total snails in canals |
Total snails in rice fields |
||
|---|---|---|---|---|---|---|
| Jan | Jun | Jan | Jun | |||
| Pisaniidae | Cantharus | Cantharus spiralis (Gray, 1839) | 7 | 0 | ||
| Ellobiidae | Cassidula | Cassidula aurisfelis (Bruguière, 1789) | 2 | 9 | ||
| Ellobium | Ellobium chinense (L. Pfeiffer, 1854) | 0 | 36 | |||
| Laemodonta | Laemodonta punctatostriata (H. Adams & A. Adams, 1854) | 0 | 10 | |||
| Pythia | Pythia plicata (Férussac, 1821) | 0 | 7 | |||
| Potamididae | Cerithidea | Cerithidea djadjariensis (K. Martin, 1899) | 4 | 2 | ||
| Cerithidea cingulata (Gmelin, 1791) | 6 | 9 | ||||
| Cerithidea obtusa (Lamarck, 1822) | 0 | 46 | ||||
| Cymatiidae | Cymatium | Cymatium pileare (Linnaeus, 1758) | 10 | 14 | ||
| Muricidae | Chicoreus | Chicoreus capucinus (Lamarck, 1822) | 1 | 58 | ||
| Thais | Thais gradata (Jonas, 1846) | 3 | 42 | |||
| Littorinidae | Littoraria | Littoraria intermedia (Philippi, 1846) | 16 | 85 | ||
| Littoraria mauritiana (Lamarck, 1822) | 75 | 28 | ||||
| Littoraria melanostoma (Gray, 1839) | 7 | 52 | ||||
| Littoraria scabra (Linnaeus, 1758) | 79 | 77 | ||||
| Assimineidae | Omphalotropis | Omphalotropis rubens (Quoy & Gaimard, 1832) | 18 | 1 | ||
| Neritidae | Neripteron | Neripteron pileolus (Récluz, 1850) | 15 | 14 | ||
| Neripteron violaceum (Gmelin, 1791) | 34 | 2 | ||||
| Neritina | Neritina undata (Lamarck, 1822) | 11 | 10 | |||
| Neritina canalis (G.B. Sowerby I, 1825) | 19 | 71 | ||||
| Clithon | Clithon oualaniense (Lesson, 1831) | 0 | 1 | |||
| Melongenidae | Pugilina | Pugilina cochlidium (Linnaeus, 1758) | 19 | 0 | ||
| Assimineidae | Sphaerassiminea | Sphaerassiminea miniata (Habe, 1942) | 0 | 16 | ||
| Bithyniidae | Bithynia | Bithynia siamensis (I. Lea, 1856) | 162 | 87 | ||
| Viviparidae | Filopaludina | Filopaludina sumatrensis (Dunker, 1852) | 23 | 0 | ||
| Lymnaeidae | Lymnaea | Lymnaea viridis Quoy & Gaimard, 1832 | 10 | 0 | ||
| Planorbidae | Gyraulus | Gyraulus convexiusculus (T. Hutton, 1849) | 4 | 0 | ||
| Thiaridae | Melanoides | Melanoides tuberculata (O.F. Müller, 1774) | 226 | 9 | ||
| Sermyla | Sermyla tornatella (I. Lea & H.C. Lea, 1851) | 109 | 506 | |||
| Thiara | Thiara scabra (O.F. Müller, 1774) | 98 | 27 | |||
| Ampullariidae | Pomacea | Pomacea canaliculata (Lamarck, 1822) | 381 | 477 | ||
| Pila | Pila conica (W. Wood, 1828) | 484 | 19 | |||
| Stenothyridae | Stenothyra | Stenothyra messageri (Bavay & Dautzenberg, 1900) | 28 | 17 | ||
| Stenothyra sp. | 37 | 12 | ||||
A total of 3632 snails were collected in both of the dry season (January 2022) and the wet season (June 2022). The snail species had high numbers of occurrences such as Pomacea canaliculata (23.6%), Sermyla tornatella (16.9%), Pila conica (13.8%), Bithynia siamensis (6.9%) and Melanoides tuberculata (6.5%). The percentage of the other snails was less than 5.0 percent (Table 3).
Table 3.
Percentage contribution of each snail species in canals and rice fields in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam in January and June 2022.
| Snail species | Dry season (January 2022) |
Wet season (June 2022) |
Two seasons |
|||
|---|---|---|---|---|---|---|
| Total | % | Total | % | Total | % | |
| Cantharus spiralis | 7 | 0.37 | 0 | 0.00 | 7 | 0.19 |
| Cassidula aurisfelis | 2 | 0.11 | 9 | 0.52 | 11 | 0.30 |
| Ellobium chinense | 0 | 0.00 | 36 | 2.06 | 36 | 0.99 |
| Laemodonta punctatostriata | 0 | 0.00 | 10 | 0.57 | 10 | 0.28 |
| Pythia plicata | 0 | 0.00 | 7 | 0.40 | 7 | 0.19 |
| Cerithidea djadjariensis | 4 | 0.21 | 2 | 0.11 | 6 | 0.17 |
| Cerithidea cingulata | 6 | 0.32 | 9 | 0.52 | 15 | 0.41 |
| Cerithidea obtusa | 0 | 0.00 | 46 | 2.64 | 46 | 1.27 |
| Cymatium pileare | 10 | 0.53 | 14 | 0.80 | 24 | 0.66 |
| Chicoreus Capucinus | 1 | 0.05 | 58 | 3.33 | 59 | 1.62 |
| Thais gradata | 3 | 0.16 | 42 | 2.41 | 45 | 1.24 |
| Littoraria intermedia | 16 | 0.85 | 85 | 4.87 | 101 | 2.78 |
| Littoraria mauritiana | 75 | 3.97 | 28 | 1.61 | 103 | 2.84 |
| Littoraria melanostoma | 7 | 0.37 | 52 | 2.98 | 59 | 1.62 |
| Littoraria scabra | 79 | 4.18 | 77 | 4.42 | 156 | 4.30 |
| Omphalotropis rubens | 18 | 0.95 | 1 | 0.06 | 19 | 0.52 |
| Neripteron pileolus | 15 | 0.79 | 14 | 0.80 | 29 | 0.80 |
| Neripteron violaceum | 34 | 1.80 | 2 | 0.11 | 36 | 0.99 |
| Neritina undata | 11 | 0.58 | 10 | 0.57 | 21 | 0.58 |
| Neritina canalis | 19 | 1.01 | 71 | 4.07 | 90 | 2.48 |
| Clithon oualaniense | 0 | 0.00 | 1 | 0.06 | 1 | 0.03 |
| Pugilina cochlidium | 19 | 1.01 | 0 | 0.00 | 19 | 0.52 |
| Sphaerassiminea miniate | 0 | 0.00 | 16 | 0.92 | 16 | 0.44 |
| Bithynia siamensis | 162 | 8.58 | 87 | 4.99 | 249 | 6.86 |
| Filopaludina sumatrensis | 23 | 1.22 | 0 | 0.00 | 23 | 0.63 |
| Lymnaea viridis | 10 | 0.53 | 0 | 0.00 | 10 | 0.28 |
| Gyraulus convexiusculus | 4 | 0.21 | 0 | 0.00 | 4 | 0.11 |
| Melanoides tuberculate | 226 | 11.97 | 9 | 0.52 | 235 | 6.47 |
| Sermyla tornatella | 109 | 5.77 | 506 | 29.01 | 615 | 16.93 |
| Thiara scabra | 98 | 5.19 | 27 | 1.55 | 125 | 3.44 |
| Pomacea canaliculate | 381 | 20.18 | 477 | 27.35 | 858 | 23.62 |
| Pila conica | 484 | 25.64 | 19 | 1.09 | 503 | 13.85 |
| Stenothyra messageri | 28 | 1.48 | 17 | 0.97 | 45 | 1.24 |
| Stenothyra sp. | 37 | 1.96 | 12 | 0.69 | 49 | 1.35 |
| Total | 1888 | 100 | 1744 | 100 | 3632 | 100 |
3.1. Cercariae morphotypes infected in snails
Xiphidio cercariae (Fig. 3) was the only cercariae group recovered from both of two snail species of Bithynia siamensis (Fig. 4a) and Thiara scabra (Fig. 4b) in Ly Nhon and Binh Khanh rice fields. For Bithynia siamensis in Ly Nhon rice field, the prevalence in the dry season (5.6%) was higher than the wet season (4.6%); however, there was no significantly different from the prevalence between two seasons (P > 0.05) (Table 5). In Binh Khanh rice field, only one Thiara scabra was infected in the wet season. For the overall prevalence in both two seasons for each snail species, Bithynia siamensis had the prevalence at 5.2 percent and Thiara scabra had the lower prevalence at 0.8 percent (Table 4).
Fig. 3.
Xiphidio cercariae.
Fig. 4.
Infected snails in the research. a. Bithynia siamensis. b. Thiara scabra.
Table 5.
Statistical analysis for the difference of prevalence for Bithynia siamensis between the dry and the wet seasons.
| Chi-Square Tests | |||||
|---|---|---|---|---|---|
| Value | df | Asymp. Sig. (2-sided) | Exact Sig. (2-sided) | Exact Sig. (1-sided) | |
| Pearson Chi-Square | 0.105a | 1 | 0.746 | ||
| Continuity Correctionb | 0.001 | 1 | 0.980 | ||
| Likelihood Ratio | 0.107 | 1 | 0.744 | ||
| Fisher's Exact Test | 1.000 | 0.501 | |||
| Linear-by-Linear Association | 0.105 | 1 | 0.746 | ||
| N of Valid Cases | 249 | ||||
. 1 cells (25.0%) have expected count less than 5. The minimum expected count is 4.54.
. Computed only for a 2 × 2 table.
Table 4.
Number of infected snails in canals and rice fields in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam.
| Species | In the dry season (January 2022) |
In the wet season (June 2022) |
In two seasons |
|||
|---|---|---|---|---|---|---|
| Collected snails | Infected snails/% | Collected snails | Infected snails/% | Collected snails | Infected snails/% | |
| Bithynia siamensis (in Ly Nhon rice field) | 162 | 9/5.6 | 87 | 4/4.6 | 249 | 13/5.2 |
| Thiara scabra (in Binh Khanh rice field) | 98 | 0 | 27 | 1/3.7 | 125 | 1/0.8 |
pH of water at the sampling time in canals in the dry season was slightly higher than in the wet season. For the temperature in the dry season, it was also a little higher than in the wet season (Table 6).
Table 6.
Environmental data measured at the sampling points in canals in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam.
| Species | In the dry season (January 2022) |
In the wet season (June 2022) |
||
|---|---|---|---|---|
| Min | Max | Min | Max | |
| pH | 6.5 | 7.0 | 6.0 | 7.0 |
| Temperature (0C) | 27.5 | 29.0 | 27.0 | 29.0 |
4. Discussion
The research result provides more information about snail diversity in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh city, Vietnam. It is interesting that 23 snail species in the research canals are completely different from 11 snail species in rice fields. It can be explained that the research canals and rice fields do not link directly to each other. Therefore, the linked canals which connect the research canals, and the rice fields should be studied in the future to find if these 34 snail species exist. In addition, water in canals is brackish while rice fields use complete rainwater, so snail species must be different. Total snail species in this research (34 snail species belonging to 28 genus and 17 families) is higher than the study in Can Gio Mangrove Biosphere Reserve in 2012 [32] with 19 snail species (16 snail species from the canal) in 16 genera and 13 families. The main reason for the difference is that the area in this study with 10 canals and two rice fields is larger than 4 research points in 2012 [32]. Moreover, the number of snail species might increase after the period of ten years. However, this can conclude only if the two studies are applied the same research method.
The dominant families of snails in the study are the Ampullariidae, the Thiaridae and the Bithyniidae. This result is similar to the finding by the previous researchers in Vietnam [39] that most snails (5629 snails of total 25,000 snails) are collected from small canals and rice fields belonging to the Thiaridae, and the Bithyniidae had the highest density of distribution in canals, rice fields and marslands [29]. However, snail species of Pomacea canaliculata belonging to the Ampullariidae which was not abundant in the previous study in rice fields [39] has the highest percentage in this research. The reason maybe that the rice fields in Can Gio Mangrove Biosphere Reserve are suitable for this species or the residents in Can Gio, the lowest population density in Ho Chi Minh city, are not interested in them; therefore, they do not get them for eating.
The collected snails from canals in this research have cercariae free whereas Bithynia siamensis and Thiara scabra from rice fields are infected with digeneans. No infected snails are found in the canals because water speed in all canals is high, so there is less chance for snails to eat digenean eggs like Heterophyidae or no opportunity for Sporocyst such as Echinostomatidae to get into snails if there are any. Moreover, snail species in the canals might not be suitable hosts for digeneans. Furthermore, there are less risks of digenean infections in the canal areas of Can Gio Mangrove Biosphere, so snails have no cercariae. In contrast, standing water in rice fields provides good environments for infection in snails if digenean eggs are available.
Pomacea canaliculata, Sermyla tornatella and Pila conica are particularly abundant in rice fields in this study, but all of them do not have any cercariae. Cercariae were not found in Pomacea sp. in Phu Yen province [29], but it was infected in Nam Dinh province [27]. Pila polita had cercariae free [27], but Sermyla tornatella infected Gymnocephalus (1,46%) and pleurolophocercariae (2,92%) [29]. Thiara scabra was infected digenean with the low prevalence at 0.8 percent, this number was much less than the research in Nam Dinh province [27] with the prevalence of 20.7 percent in fishponds, and the prevalence of 6.9 percent in Phu Yen province [29]. Melanoides tuberculata, the most important host for fishborne zoonotic parasites belonging to Heterophyidae, was plenty in small canals and Bithynia siamensis, a potential host for Heterophyidae and Opisthorchiidae, was found a lot in rice fields in the research in 2015 [39], but they occur less than 7.0 percent for each species in this research. Melanoides tuberculata and Bithynia fuchsiana was infected with the high prevalence in ponds and canals [27,29], in natural water bodies [34]; however, Melanoides tuberculata has cercariae free in this research and Bithynia siamensis has the highest overall prevalence at 5.2 percent. Therefore, the result in this research confirms again that Bithynia is easier to infect cercariae than the other sampled snails, and Melanoides tuberculata can infect digenean in most of the water bodies but it can have cercariae free in certain areas.
Only xiphidio cercariae are recovered from snail species of Bithynia siamensis (N = 13) and Thiara scabra (N = 1) in this study with the low numbers of cercariae per snail. Although this finding supports the result in 2005 [44] that xiphidio cercariae was the most prevalent in their research, and xiphidio cercariae was found only in Thiara scabra [29], this makes surprising because more than one morphotype of cercariae were found in the other studies in Vietnam in the previous years [27,30,34]. The explanation can be that Can Gio Mangrove Biosphere Reserve is separated from the other areas as it is like an island surrounded by water; therefore, digeneans from the other areas have not invaded into this Mangrove Biosphere Reserve yet. One more reason is that all water bodies are not examined, so other groups of cercariae in this area have not been recognized.
Some water environment factors were done during the research period. However, the collected data were not very different between the dry and the wet seasons in the research canals. How pH and temperature in this study affect the distribution of snails and the digenean prevalence between the dry and the wet seasons can not be identified yet. Therefore, more research on the effects of water environment should be done more carefully and in more detailed from different months to find the clear answers for this issue.
Regarding the seasonality, snail populations were typically more abundant in the rainy season than in the dry season thanks to the good conditions for the multiplication of snails [45]. This is correct with the collected snails from the canals in this research. However, total numbers of snail samples in rice fields in the dry season in this research (1559 snails) is much higher than in the wet seasons (1145 snails). It seems that the seasonality does not affect the snail breeding in rice fields, especially the snail species of Pila conica, Melanoides tuberculata, Bithynia siamensis and so on in this study. More research should be done to get the answer to support this finding. The season also affects the digenean prevalence in snails in this research. Only one Thiara scabra is found Type 1 of xiphidio cercariae in the wet season; however, 13 snails of Bithynia siamensis is infected Type 2 of xiphidio cercariae in both of the two seasons, and the prevalence in the dry season is higher than in the wet season, but there is no significantly different (P > 0.05). The different digenean prevalence in this study is like the report in 2014 [29] that the occurrence of cercariae in snails was different among the months of the year and the prevalence in the dry season was higher than the wet season due to the high temperature. The seasonality of digenean prevalence observed in this study also agrees with the research results in 2005 [44] that the prevalence of cercariae was high in the dry season and decreased in the wet season. The findings of digenean prevalence in this area have not been very serious yet based on the research result of the low digenean prevalence in snails in this research and in cultured fish [1]. However, how many snails and fishes are infected digeneans in the other water bodies and how season affects the occurrence of digenean in snails and fish are not known clearly yet. Therefore, more research should be done in Can Gio Mangrove Biosphere Reserve to know the prevalence of cercariae in snails and in fish in different months of the year. Afterwards, the control strategy of digenean such as managing the infected snails and dangerous cercariae can be carried out in the area to contribute to food safety and hygiene, and human’ s health in the future.
5. Conclusions
No cercariae were found in 23 collected snail species from ten canals in three research zones of Can Gio Mangrove Biosphere Reserve. In total 11 snail species collected from two rice fields, only Bithynia siamensis in Ly Nhon rice field and Thiara scabra in Binh Khanh rice field infected xiphidio cercariae. For Bithynia siamensis, the prevalence in the dry season (5.6%) was higher than in the wet season (4.6%) (P > 0.05). In Binh Khanh rice field, only one Thiara scabra infected cercariae in the wet season. Further research on digenean infection in different months and in other water bodies in Can Gio Mangrove Biosphere Reserve should be done to find the diversity of snails and their prevalence in the whole year to contribute to the control of digeneans and reserve the biodiversity.
The research identified the digenean prevalence and snail species composition collected in rice fields and small canals in Can Gio Mangrove Biosphere Reserve in January (the dry season) and June (the wet season) of the year 2022. However, this research still has some limitations. The research was conducted in two months of the two seasons, which provides a snapshot, but it can not fully capture the annual variation in snail populations and infection prevalence. Moreover, the study focused on small canals and rice fields may not capture the full diversity of snail species and digenean infections in the entire Mangrove Biosphere Reserve. Other habitats within the reserve may present different ecological dynamics. In addition, the study might not account for all environmental variables that could affect snail diversity and infection rates, such as water quality parameters, presence of predators, or human activities. For the identification, the morphological methods were used for snail and cercariae identification, but there were no applications of molecular techniques, which could be considered a limitation given that morphological identification can sometimes be less precise. Future research should consider all of these above limitations to find better results and carry out deeper statistical analysis when the results show more outputs.
Data availability statement
Data will be made available on request.
CRediT authorship contribution statement
Pham Cu Thien: Writing – review & editing, Writing – original draft, Validation, Resources, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Thi Duong Nguyen: Writing – original draft, Formal analysis, Data curation.
Declaration of competing interest
Hereby the authors of the manuscript entitled “Digenean infections in snails (cercariae stage) in Can Gio Mangrove Biosphere Reserve, Ho Chi Minh City, Vietnam” would like to confirm that the authors declare no conflict of interest regarding the publication of this article.
Acknowledgements
This work is gratefully acknowledged for the financial support by Ministry of Education and Training, Vietnam (grant number: B2022-SPS-07).
Contributor Information
Pham Cu Thien, Email: thienpc@hcmue.edu.vn.
Thi Duong Nguyen, Email: duong7181@gmail.com.
References
- 1.Pham C.T., Pham T.T.D., Nguyen T.H., Huynh H., Pham N.A.T., Tong X.T. Prevalence of trematode in wild fish from fishing in Ho Chi Minh city. Ho Chi Minh City University of Education Journal of Science. 2019;16(3):152–161. https://DOI:10.54607/hcmue.js.16.3.2467 [Google Scholar]
- 2.Pham C.T., Le N.P.A., Tran T.N.G., Pham N.L.P., Do D.Q.P., Tran T.P.D. Research on prevalence of trematode in grow-out finfish cultured in Ho Chi Minh City. Ho Chi Minh City University of Education Journal of Science. 2019;16(6):133–141. [Google Scholar]
- 3.Chai J.Y., Lee S.H. Foodborne intestinal trematode infections in the Republic of Korea. Parasitololy International. 2022;51:129–154. doi: 10.1016/s1383-5769(02)00008-9. https://doi:10.1016/s1383-5769(02)00008-9 [DOI] [PubMed] [Google Scholar]
- 4.Keiser J., Utzinger J. Emerging foodborne trematodiasis. Emerg. Infect. Dis. 2005;11:1507–1514. doi: 10.3201/eid1110.050614. https://doi:10.3201/eid1110.050614 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.[WHO] World Health Organization . Ha Noi; Vietnam: 2004. Workshop on Food-Borne Trematode Infections in Asia. [Google Scholar]
- 6.[WHO] World Health Organizarion . World Health Organization; Geneva, Switzerland: 1995. Control of Foodborne Trematode Infections. WHO Technical Report Series Number 849 (1995) [Google Scholar]
- 7.Caravedo M.A., Cabada M.M. Human fascioliasis: current epidemiological status and strategies for diagnosis, treatment, and control. Res. Rep. Trop. Med. 2020;11:149–158. doi: 10.2147/RRTM.S237461. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Saba R., Korkmaz M., Inan D., Mamikoglu L., Turhan O., Gunseren F., Cevikol C., Kabaalioglu A. Human fascioliasis. Clin. Microbiol. Infection. 2004;10(5):385–387. doi: 10.1111/j.1469-0691.2004.00820.x. https://doi:10.1111/j.1469-0691.2004.00820.x [DOI] [PubMed] [Google Scholar]
- 9.Nawa Y., Hatz C., Blum J. Sushi delights and parasites: the risk of fishborne and foodborne parasitic zoonoses in Asia. Clin. Infect. Dis. 2005;41:1297–1303. doi: 10.1086/496920. https://doi:10.1086/496920 [DOI] [PubMed] [Google Scholar]
- 10.Dorny P., Praet N., Deckers N., Gabriel S. Emerging food-borne parasites. Vet. Parasitol. 2009;163:196–206. doi: 10.1016/j.vetpar.2009.05.026. https://doi:10.1016/j.vetpar.2009.05.026 [DOI] [PubMed] [Google Scholar]
- 11.Thai T.B. Vietnam Education Publishing House; 2016. Invertebrates. [Google Scholar]
- 12.Dang T.T., Nawa Y. In: Food-borne Helminthiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. vol. 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Fasciola and fascioliasis in Vietnam; pp. 57–60. [Google Scholar]
- 13.Waikagul J., Yoonuan T., T . In: Food-borne Helminthiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. ume 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Paragonimus and paragonimiasis in Thailand; pp. 139–148. [Google Scholar]
- 14.Pham N.D., Nguyen T.L., Dang T.T. In: Food-borne Helminyhiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. ume 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Paragonimus and paragonimiasis in Vietnam; pp. 149–153. [Google Scholar]
- 15.Long-Qi X., Sen-Hai Y., Ying-Dan C. In: Food-borne Helminthiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. vol. 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Clonorchiasis sinensis in China; pp. 1–26. [Google Scholar]
- 16.Yoshida Y. In: Food-borne Helminthiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. vol. 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Clonorchis sinensis and clonorchiasis in Japan; pp. 27–33. [Google Scholar]
- 17.Dubey J.P., Murrell K.D., Cross J.H. In: Foodborne Infections and Intoxications. Riemann H.P., Cliver D.O., editors. Academic Press is an imprint of Elsevier; 2006. Foodborne parasites; pp. 449–476. [Google Scholar]
- 18.Tesana S. In: Food-borne Helminthiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. vol. 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Opisthorchiasis in Thailand; pp. 113–124. [Google Scholar]
- 19.Nguyen V.D., Murrell K.D., Le D.C., Phung D.C., Le V.C., Nguyen D.T., Dalsgaard A. The food-borne trematode zoonoses of Vietnam. Southeast Asian J. Trop. Med. Publ. Health. 2003;34:12–34. [PubMed] [Google Scholar]
- 20.Nguyen M.H., Hoang V.H., Ho T.L., Yulia V.T., Madsen H. PLOS Neglected Tropical Diseases. 2021. Are Melanoides tuberculata and Tarebia granifera (Gastropoda, Thiaridae), suitable first intermediate hosts of Clonorchis sinensis in Vietnam? [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Waikagul J., Radomyos P. In: Food-borne Helminthiasis in Asia. Arizono N., Chai J.Y., Nawa Y., Takahashi Y., editors. vol. 1. The Federation of Asian Parasitologists; Chiba, Japan: 2005. Intestinal trematode infections in Thailand. Clonorchiasis sinensis in China; pp. 103–111. [Google Scholar]
- 22.Khalifa R., El-Naffar M.K., Arafa M.S. Studies on heterophyid cercariae from Assiut province, Egypt. I. Notes on the life cycle of Haplorchis pumilio (Looss, 1896) with a discussion on previously described species. Acta Parasitol. Pol. 1977;25:25–38. [Google Scholar]
- 23.Wang J.J., Chung L.Y., Lee J.D., Chang E.E., Chen E.R., Chao D., Yen C.M. Haplorchis infections in intermediate hosts from a clonorchiasis endemic area in Meinung, Taiwan, Republic of China. J. Helminthol. 2002;76(2):185–188. doi: 10.1079/JOH2002114. https://doi:10.1079/JOH2002114 [DOI] [PubMed] [Google Scholar]
- 24.Dechruksa W., Krailas D., Ukong S., Inkapatanakul W., Koonchornboon T. Trematode infections of the freshwater snail family Thiaridae in the Khek river, Thailand. Southeast Asian J. Trop. Med. Publ. Health. 2007;38(6):1016–1028. [PubMed] [Google Scholar]
- 25.Scholz T., Salgado-Maldonado G. The introduction and dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: a review. Am. Midl. Nat. 1999;143:185–200. [Google Scholar]
- 26.Lee F.O., Cheng T.C. The histochemistry of Stellantchasmus falcatus Onji and Nishio, 1915 (Trematode: Heterophyidae) metacercarial cyst in the mullet Mugil cephalus L. and histopathological alterations in the host. J. Fish. Biol. 1970;2:235–243. doi: 10.1111/j.1095-8649.1970.tb03280.x. [DOI] [Google Scholar]
- 27.Bui T.D., Madsen H., Dang T.T. Distribution of freshwater snails in family-based VAC ponds and associated waterbodies with special reference to intermediate hosts of fish-borne zoonotic trematodes in Nam Dinh Province, Vietnam. Acta Trop. 2010;116:15–23. doi: 10.1016/j.actatropica.2010.04.016. [DOI] [PubMed] [Google Scholar]
- 28.Dang N.T., Thai T.B., Pham V.M. Ha Noi: Technology and Science Publisher; Vietnam: 1980. Key of Identification Invertebrate in the North of Vietnam; pp. 440–490. [Google Scholar]
- 29.Nguyen P.B.N., Nguyen C.L., Vo T.D., Ngo A.T. Infection of trematode larvae (cercariae) in freshwater snails in two communes, an My and an Hoa, Tuy an district, Phu Yen province. Journal of Science-Fisheries Technology. 2014;1 [Google Scholar]
- 30.Ha H.H.V., Nguyen H.H., Nguyen H.B.T. Identification freshwater snail intermediate host of trematoda causing animal disease in Vinh Long and Dong Thap Province. Can Tho University Journal of Science. No. Agriculture. 2014;2:8–12. [Google Scholar]
- 31.Do V.T. Proceedings of the sixth National conference of ecology and biological resources; Hanoi, Vietnam: 2015. Freshwater Snails of Vietnam: Diversity and Conversation Status; pp. 977–986. [Google Scholar]
- 32.Ngo T.L. Ho Chi Minh City University of Education; Unpublished work: 2012. Investigating the Component and the Location of Mollusca and Nematoda in Can Gio Mangrove Forest, Ho Chi Minh City, Technical Report. [Google Scholar]
- 33.Besprozvannykh H.D., Ngo V.H., Nguyen M.H., Nguyen K.V., Rozhkovan A.V., Ermolenko Descriptions of digenean parasites from three snail species, Bithynia fuchsiana (Morelet), Parafossarulus striatulus Benson and Melanoides tuberculata Müller. North Vietnam, Helminthologia. 2013;50(3):190–204. doi: 10.2478/s11687-013-0131-5. [DOI] [Google Scholar]
- 34.Nguyen M.H., Do T.D., Nguyen T.L.A., Phan T.V., Bui N.T., Nguyen V.H., Hoang V.H., Le X.C. 2015. Current Status of Fish-Borne Zoonotic Trematode Infections in Gia Vien District, Ninh Binh Province, Vietnam, Parasites & Vectors.https://doi:10.1186/s13071-015-0643-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Pham N.D., Hoang V.H., Bui T.D., Ho T.L. Infection status and molecular identification of digenean cercariae in snails in kim son district, Ninh Binh province and Ba vi district, ha Noi. Academia Journal of Biology. 2019;41(3) https://doi:10.15625/0866-7160/v41n3.13893 [Google Scholar]
- 36.Tuan L.D. Agricultural Publishing House; 2014. Environmental Resources of Human Ecology System in Can Gio Mangrove Biosphere Reserve. [Google Scholar]
- 37.Sang N.N. Reassessment of the area of amphibians and reptiles in can Gio mangrove Biosphere reserve. Journal of Science-Tecnology Development. 2009;12(3):95–102. [Google Scholar]
- 38.Dung N.X. Scientific Report; 2012. Research, Survey, Assessment of the Biodiversity in Can Gio Mangrove Biosphere Reserve; pp. 1–276. [Google Scholar]
- 39.Madsen H., Bui T.D., Dang T.T., Nguyen K.V., Dalsgaard A., Phan T.V. The role of rice fields, fishponds and water canals for transmission of fish-borne zoonotic trematodes in aquaculture ponds in Nam Dinh province, Vietnam. Parasites Vectors. 2015;8:625. doi: 10.1186/s13071-015-1237-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Ho Chi Minh City People’s Committee . 2023. Decision No 2580 Dated on 20 July 2021 about the Announcement of the Inland Waterway Systems in the Ho Chi Minh City Area in the Period of 2021-2023. [Google Scholar]
- 41.Ho Chi Minh City People’s Committee . 2019. Decision No 2816 Dated on 01 July 2019 about the Approvement of the Plan of Land Use in 2019 in Can Gio District, Ho Chi Minh City. [Google Scholar]
- 42.Frandsen F., Christensen N.Ø. An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Trop. 1984;41:181–202. [PubMed] [Google Scholar]
- 43.Schell S.C. University Press of Idaho; 1985. Handbook of Trematodes of North America North of Mexico; pp. 1–17. [Google Scholar]
- 44.Nkwengulila G., Kigadye E.S.P. Occurrence of digenean larvae in freshwater snails in the ruvu basin, Tanzania. Tanzan. J. Sci. 2005;31(2) https://DOI:10.4314/tjs.v31i2.18417 [Google Scholar]
- 45.Brockelman W.Y., Upatham E.S., Viyanant V., Ardsungnoen S., Chantanawat R. Field studies on the transmission of the human liver fluke, Opisthorchis viverrini, in northeast Thailand: population changes of the snail intermediate host. Int. J. Parasitol. 1986;16:452–545. doi: 10.1016/0020-7519(86)90091-3. [DOI] [PubMed] [Google Scholar]
Associated Data
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Data Availability Statement
Data will be made available on request.