This study aimed to investigate the pulmonate snail species in the vicinity of the cercarial dermatitis outbreak area in southern Thailand. In 2020, an outbreak of cercarial dermatitis was reported in Chana district, Songkhla Province, caused by the ruminant schistosome Schistosoma indicum and its snail intermediate host Indoplanorbis exustus. In the present study, 1,175 pulmonate snails were collected between October 2021 and October 2022 from five provinces covering 34 locations in southern Thailand. Seven pulmonate snail species were identified based on shell morphology, including Amerianna carinata, Gyraulus bakeri, G. convexiusculus, G. hubendicki, Physella acuta, Indoplanorbis exustus, and Radix rubiginosa. Among these snails, eight species, and five types of cercariae were identified, viz. type (i) Echinostome cercariae consisted of Echinoparyphium recurvatum, Echinostoma spiniferum, and E. revolutum, type (ii) Brevifurcate-apharyngeate cercariae consisted of Schistosoma indicum and S. spindale, type (iii) Brevifurcate-pharyngeate-clinostomatoid-cercariae was represented by Clinostomum giganticum, type (iv) Longifurcate–pharyngeate cercariae (strigea cercaria) was Diplostomum baeri eucaliae, and type (v) Ophthalmoxiphidiocercaria. Among the seven pulmonated snail species, three were found to be infected, viz. G. convexiusculus, I. exustus, and R. rubiginosa, with infection rates of 1.14% (2/176), 0.25% (2/802), and 4.02% (7/174), respectively.

Trematode infection, Cercariae, Snail intermediate host

Pulmonate snails are a large and diverse group of snails in Class Gastropoda. They are widely distributed throughout the world in a variety of habitats, including freshwater, terrestrial, and marine environments. Freshwater pulmonates have been reported for their medical and veterinary significance, as they serve as intermediate hosts to various blood, liver and intestinal flukes that affect humans directly or accidentally as parasitic zoonoses (Monzon et al. 1993). The snail hosts recorded for 279 species of flukes indicate that pulmonates play a very important role parasitizing mammals and birds. For example, some species of Schistosoma trematodes, also known as blood flukes, use pulmonate snails as intermediate hosts in their life cycle. These parasites cause schistosomiasis, a neglected tropical disease that affects millions of people worldwide. When snail families are considered and ranked according to the frequency in which they are involved in the transmission of these flukes, species of the pulmonate Planorbidae and Lymnaeidae are the first two among the top ten (Ewers 1964).

Research on pulmonate snails and their role as intermediate hosts for parasites has focused on understanding the transmission dynamics of these diseases and developing strategies for their control. For example, the factors that influence the transmission of parasites from snails to humans have been investigated, such as the behavior of snails and the environmental conditions that promote parasitic development. Other research on pulmonate snails and snail-borne diseases has focused on identifying and characterizing the genetic and molecular mechanisms that underlie the interactions between snails and parasites. This research has the potential to lead to the development of new treatments or control measures for these diseases. Overall, research on pulmonate snails and their role as intermediate hosts in snail-borne diseases is important for understanding the epidemiology of these diseases and to develop effective strategies for prevention and control.

Many studies in Southeast Asia have reported on medically important snails. The snail-borne parasitic diseases are considered diseases of public health importance in this region. The fauna, ecology, and dynamics of transmission have been reported for the snails in seven families that exist in the region viz. Ampulariidae, Bithyniidae, Viviparidae, Thiaridae, and Pomatiopsidae among the Caenogastropoda as well as Lymnaeidae and Planorbidae among the Pulmonata (Tropmed Technical Group 1986).

Here, we focus on Pulmonate freshwater snails from the families Planorbidae and Lymnaeidae. These snails were observed in the vicinity of the cercarial dermatitis outbreak area in southern Thailand, where they are of significant medical importance as intermediate hosts for trematodes. The aim of this study is to investigate the possibility of the occurrence of cercarial dermatitis and trematodiasis, as well as to gain further knowledge about the potential of freshwater pulmonate snails as intermediate hosts for trematodes. Additionally, we aim to examine the distribution of important parasites affecting both humans and animals in communities near the outbreak area of cercarial dermatitis in Chana district, Songkhla province, Thailand, which occurred in 2020 (Krailas et al. 2022).

Two methods, such as cercarial shedding, and crushing, were employed to investigate the presence of cercariae in the snails. The cercarial shedding method involved placing a snail in a small plastic cup containing dechlorinated water and observing the snails twice a day for 7–10 days to detect the emergence of cercariae. The emergent cercariae were examined under a binocular dissecting microscope and a light microscope, both unstained, and live stained with 0.5% neutral red. Snails that did not shed cercariae during the observed time were crushed to examine for parthenitae (sporocysts/rediae) and cercariae. The morphology of the trematodes was described based on living cercariae that had emerged from the snails. The characteristics of the cercariae were photographed using a differential interference contrast (DIC) microscope (Olympus BX53, Japan) and were drawn and identified based on descriptions from previous studies (see e.g. Krailas et al. 2011, 2014, 2022). Free-swimming cercariae were observed under the dissecting microscope, and measurements of 10 specimens fixed in 10% formalin were taken using an ocular micrometer to determine the average size in micrometers.

Snail-borne parasitic diseases have been reported in the Southeast Asian region for more than 50 years. In particular, liver fluke opisthorchiasis, blood fluke schistosomiasis, intestinal fluke echinostomiasis, and fasciolopsiasis are public health issues that affect socioeconomic development in this region.

Freshwater snails that serve as intermediate hosts, are commonly found in various water resources, and Thailand is home to one of the world’s richest freshwater and brackish water snail faunas, with over 170 freshwater species and 96 brackish water species recorded across 75 genera and 23 families. Among these non-marine aquatic Mollusca of Thailand, according to Brandt (1974), there are three superfamilies of snails within the Pulmonata, such as Ancyloidea Rafinesque 1815, Planorboidae Rafinesque 1815, and Lymnaeoidea Rafinesque 1815, all of which belong to Basommatophora Keferstein 1864 (Bouchet and Rocroi 2005).

The SEAMEO-TROPMED organization held a technical meeting on “Snails of Medical Importance in Southeast Asia” in 1985 to update and review the species distribution of medically important snails in the region. The aim was to provide guidance for controlling these snails. The pulmonate snails of Thailand were listed according to their geographical location, viz. Lymnaeidae consisting of Austropeplea ollula, Radix viridis (reported to Radix (Austropeplea) ollula), R. auricularia rubiginosa and R. a. swinhoei and Planorbidae consisting of Hippeutis umbilicalis, Indoplanorbis exustus, Gyraulus convexiusculus, Segmentina hemisphaerula, and S. trochoideus (Brandt 1974; Tropmed Technical Group 1986). These snails are widely distributed throughout Thailand and are commonly found in freshwater environments, serving as intermediate hosts for human and animal trematodes. Besides the medically important snails, there have been numerous regional surveys, species lists, and reviews of pulmonate snail species significant for public health and veterinary purposes, particularly in the vicinity of the cercarial dermatitis outbreak area in southern Thailand (Krailas et al. 2022).

Radix rubiginosa (Lymnaeidae) serves as an intermediate host for the liver fluke Fasciola gigantica and the intestinal flukes Echinostoma malayanum, E. revolutum, and Hypoderaeum conoideum. This snail has been reported throughout the water resources of Thailand, except for the northernmost provinces. Radix swinhoei is an intermediate host for F. gigantica and many species of intestinal flukes in Echinostomatidae, and has been reported in the northernmost provinces. Austropeplea ollula serves as an intermediate host for F. gigantica and echinostomes and is distributed in central and northern Thailand.

The planorbid snails serve as intermediate hosts for human schistosomes, but in Thailand, they mediate echinostomes, Fasciolopsis buski, and non-human schistosomes. Gyraulus convexiusculus is an intermediate host for E. malayanum and E. ilocanum, while Indoplanorbis exustus is an intermediate host for the intestinal flukes E. malayanum, E. revolutum, H. conoideum, Schistosoma spindale, and S. indicum. Segmentina spp. is intermediate hosts for the largest intestinal fluke F. buski, which is found throughout Thailand, particularly in the central region. (Kruatrachue and Harinasuta 1963, 1964; Harinasuta et al. 1965; Manning 1969; Manning et al. 1969; Sornmani 1969a, b; Brandt 1974; Schneider et al. 1974; Ratanaponglakha et al. 1988, 1989; Burch and Upatham 1989; Kullavanijaya and Wongwaisayawan 1993; Krailas et al. 2022).

As reported here, we collected pulmonate snails from five provinces in southern Thailand, categorized into three families based on the morphological characters of their shells, including Lymnaeidae, Physidae, and Planorbidae. Originally, Physidae was native to Holarctic, but extending its distribution now into Central and South America, and has invaded freshwater lentic habitats nearly worldwide, except those in Antarctica (Burch 1988; Wethington and Lydeard 2007; Bousset et al. 2014). Among these Physella acuta (syn. Physa acuta) is an invasive species in Thailand, having previously been collected from tanks within a research facility in Bangkok and subsequently spread throughout the country (Rico et al. 2014; Ng et al. 2018).

In this study, seven pulmonate species were collected, including Amerianna carinata, Gyraulus bakeri, G. convexiusculus, G. hubendicki, Physella acuta, Indoplanorbis exustus, and Radix rubiginosa. Naturally infected snails were found in six of 27 locations that were in the vicinity of the cercarial dermatitis outbreak (Krailas et al. 2022). We related the occurrence and distribution of these pulmonate snails to the cercarial dermatitis outbreak of 2020 in this region, as we found that the snail act as intermediate hosts to several trematode species of medical importance. In summary of our study, trematode infections were found in eight species of five cercarial types from three snail species, including G. convexiusculus, I. exustus, and R. rubiginosa. The infection rates were 1.14% (2/176), 0.25% (2/802), and 4.02% (7/174), respectively. Although the infection rate of parasites is low, we have found something interesting in the ability of snails to serve as intermediate hosts for the trematode parasites encountered in this study, which has not been reported extensively before. This is a report that should be further investigated in the future. Next, we would like to discuss the importance of pulmonate snails and their significance in serving as intermediate hosts for parasitic diseases that are of public health and veterinary importance.

Gyraulus convexiusculus is a widespread snail species that has been collected from ponds, lakes, canals, and rice fields in tropical Asia and surrounding regions (Van Damme 2014). It is an intermediate host for many trematode parasites, including Artyfechinostomum malayanum (Leiper, 1911) Mendheim 1943 (syn. Echinostoma malayanum Leiper, 1911; Euparyphium malayanum Odhner, 1913), which was first described in a human in Malaysia and has since been found in other countries, such as Singapore, Thailand, Indonesia, India, and the Philippines (Premvati and Pande 1974; Maji et al. 1993; Radomyos et al. 1998; Belizario et al. 2007; Chai et al. 2009). G. convexiusculus is the first intermediate host of the intestinal fluke Fasciolopsis buski in South Kalimantan Indonesia and amphistomataous parasites of domestic animals in India. These parasites cause significant losses due to poor health and heavy mortality of humans and commercially important animals (Djajasasmita 1989; Kishore and Shoeb 2017). During our survey, we collected G. convexiusculus snails from 11 locations across five provinces. However, infected snails were only found in two locations located in Chian Yai District of Nakhon Si Thammarat Province and Mueang District of Chumphon Province. We identified two trematode species in these snails, such as Echinoparyphium recurvatum, and Ophthalmoxiphidiocercaria. The genus Echinoparyphium is an important taxon in the family Echinostomatidae, as species in this genus are involved in intestinal foodborne trematodiases in Southeast Asia. E. recurvatum is an intestinal fluke of wild fowl and mammals and is a cosmopolitan species. Many species of snails in the families Lymnaeidae and Planorbidae are susceptible intermediate hosts for E. recurvatum, including Lymnaea pervia, L. limosa, L. palustris, L. auricularia rufescens, Planorbis, Planorbarius dufouri, and Indoplanorbis exustus. Although E. recurvatum infections have mostly been reported in birds, human infections have been reported in Taiwan, Indonesia, Korea, and Egypt (Sohn 1998; Chai et al. 2009; Huffman and Fried 2012), but have never been reported in Thailand to date. In particular, a natural infection was detected in G. convexiusculus. We also report a natural infection of G. convexiusculus with an Ophthalmoxiphidiocercaria trematode in the family Allocreadiidae. The cercariae of this parasite develop in freshwater bivalves of the family Sphaeriidae, but not in the subfamily Crepidostominae, and have also been reported in L. peregra, a freshwater gastropod in the Lymnaeidae (Henderson 1938; Schell 1970). Interestingly, researchers have suggested that trematode cercariae, such as those from Echinoparyphium recurvatum can be distinguished into lymnaeidarum and planorbidarum types. The planorbidarum type, which refers to Echinoparyphium cercariae shed from planorbid snails (Odening 1964; Grabda-Kazubska and Kiseliene 1989; McCarthy 1990).

The planorbid snail, Indoplanorbis exustus was the most abundant of the snails collected in this study. Moreover, I. exustus was collected from 25 locations and are widely distributed in Thailand, India, Sri Lanka, Indonesia, the Philippines, Japan, and Hawaii. The freshwater bulinine planorbid snail I. exustus is the sole intermediate host of the Schistosoma indicum species group, which causes severe outbreaks of cattle schistosomiasis and human cercarial dermatitis in India and Southeast Asia (Burch and Upatham 1989; Agrawal et al. 2000; Gauffre-Autelin et al. 2017). The medically important digenetic trematode Schistosoma includes four prominent species groups, including the S. japonicum species group in Asia, which are S. japonicum, S. mekongi, S. sinensium, S. malayensis, and S. ovuncatum; the S. mansonia species group in Africa, Southwest Asia, and South America, which are S. mansoni, S. rodhaini, S. hippopotami, and S. edwardiense; the S. haematobium species group in Africa, which are S. haematobium, S. intercalatum, S. bovis, S. mattheei, S. curassoni, S. margrehowiei, and S. leiperi, and the S. indicum species group in Asia, which consists of S. indicum, S. nasale, S. spindale, and S. incognitum (Attwood et al. 2007; Webster et al. 2013; Devkota et al. 2015; Jones et al. 2020). In our previous study, we reported that I. exustus is an intermediate host of S. indicum, a ruminant parasite that caused the outbreak of cercarial dermatitis in Chana district, Songkhla Province, South Thailand (Krailas et al. 2022), In this study, S. indicum was detected in one snail of the same species. We also found another type of trematode infection, Furcocercous cercariae/Brevifurcate-pharyngeate-clinostomatoid-cercariae, specifically Clinostomum giganticum Agarwal, 1959, in one I. exustus specimen from a different location. The genus Clinostomum Leidy, 1856 is a cosmopolitan parasite found in the oral cavity, pharynx, and esophagus of fish-eating birds. Its life cycle requires two intermediate hosts (snails and fish or frogs) and one avian definitive host (Osborn 1911, 1912; Kanev et al. 2002; McAllister et al. 2010; Calhoun et al. 2019). The pulmonate gastropods in the families Planorbidae and Lymnaeidae are commonly reported as first intermediate hosts. In this study, both snail families were infected by C. giganticum. Including a previous study, the Clinostomum distribution tended to coincide with the distributions of Planorbidae and Lymnaeidae snails in the same area. Clinostomum is associated with “yellow-spot disease/yellow grubs” in freshwater fish as a secondary intermediate host. The metacercaria larval stage encysts below the integumentary tissue, causing visible swelling of the nodules. The parasites remain encysted and alive within the host for several years until eaten by a bird host. Humans can also become infected by eating raw or undercooked fish meat carrying the metacercarial stage. Therefore, this trematode must be considered not only for its losses in production and fish farming waste but also for its potential zoonotic impact on humans (Hunter and Hunter 1934, 1935; Esch et al. 2001; Wang et al. 2017; Rosser et al. 2018; Sohn et al. 2019; de Souza et al. 2020; Won et al. 2020; Krailas et al. 2022).

Only one species, Radix rubiginosa, was collected from the family Lymnaeidae at 16 of 27 locations. We found trematode infections in seven snails, with four types, and six species of cercariae being identified, viz. (i) Echinostome cercariae consisted of Echinoparyphium recurvatum, Echinostoma spiniferum, and Echinostoma revolutum, type (ii) Brevifurcate-apharyngeate cercariae which was Schistosoma spindale, type (iii) Brevifurcate-pharyngeate-clinostomatoid-cercariae which was Clinostomum giganticum, and type (iv) Longifurcate–pharyngeate cercariae (Strigea cercaria) which was Diplostomum baeri eucaliae. R. rubiginosa is a common freshwater snail that is widely distributed throughout Thailand. It is an abundant species in Lymnaeidae and serves as an intermediate host of the intestinal flukes of the Echinostomatidae. It has also been recorded in Laos, Cambodia, Vietnam, Malaysia, and Indonesia. In the present study, three species of Echinostomatidae were collected, including E. recurvatum, E. spiniferum, and E. revolutum. This is a new record for R. rubiginosa infected with E. recurvatum and E. spiniferum in Thailand. In our previous study of parasites that caused an outbreak of cercarial dermatitis, a double infection of S. indicum and E. spiniferum was found in I. exustus (Krailas et al. 2022). Now, in the present study, E. spiniferum was found in R. rubiginosa. Furthermore, we here report the discovery of three more cercarial types from R. rubiginosa viz. Brevifurcate-apharyngeate cercariae, such as S. spindale, Brevifurcate-pharyngeate-clinostomatoid-cercariae: C. giganticum, and Longifurcate–pharyngeate cercariae (Strigea cercaria): Diplostomum baeri eucaliae. Trematodes in the Family Diplostomatidae are commonly observed in freshwater environments. They have a complex life cycle that involves multiple hosts, including snails, fish, and birds. Many studies on the life histories of members of the genus Diplostomum have been reported, which was initially discovered in Europe, Africa, and the Americas (Palmieri et al. 1976). It was only decades later that the metacercarial characters were resolved causing a disease in fish known as diplostomatosis or eye fluke disease.

The schistosome species, S. spindale causes cercarial dermatitis in the same areas where I. exustus is distributed. The different distribution areas that we reported in this study indicate the prevalence of S. spindale in Nakhon Si Thammarat Province, while S. indicum was detected in Chaiya District, Surat Thani Province. Although R. rubiginosa was common in the Nakhon Si Thammarat in Southern Thailand, they are the intermediate host of S. japonicum, the human blood fluke, and Orientobilharzia harinasutai, the cattle blood fluke, in this area. The freshwater snail I. exustus is susceptible to infection by S. spindale, but here we found S. spindale from R. rubiginosa (Harinasuta and Kruatrachue 1962; Kruatrachue and Harinasuta 1963, 1964; Kruatrachue et al. 1964, 1965, 1968; Bunnag et al. 1986; Inder Singh et al. 1997; Lakshmanan et al. 2016).

Accordingly, the results we present here provide additional information on the potential of pulmonate snails as intermediate hosts for trematodes in Thailand. We emphasize that the distribution of these snail intermediate hosts plays a significant role in the transmission of parasites, which holds great medical, and veterinary significance.

Snail-borne diseases pose significant health risks to animals and humans, and trematodiasis remains a serious problem in Southeast Asia. In particular, cercarial dermatitis affects paddy workers, agricultural laborers, and fishermen. While surveys on larval trematodes in freshwater snails have been conducted, comprehensive data on gastropod infections are lacking. Therefore, this study aimed to determine the prevalence and types of cercarial infections in snails. A review of previous studies on pulmonate snails provided valuable insight into the diversity of parasites within their intermediate host populations. Both Lymnaeidae and Planorbidae snails play important roles as intermediate hosts for various digenean parasites, including schistosomes, echinostomes, clinostomes, and siplostomes. Effective control of trematode infections requires a holistic approach that focuses on managing the overall ecosystem and reducing exposure to the infective stages. This may involve maintaining good water quality, controlling the snail populations, and limiting bird access to fish habitats (as Clinostomum and Diplostomum infections primarily affect fish populations, with no direct transmission to humans). The presence of trematodes in snails presents a significant health concern in southern Thailand. Therefore, further studies are warranted to characterize these infections in other regions and expand our understanding of the extent and impact of snail-borne diseases.

This research was supported by the Department of Biology, Faculty of Science, and Silpakorn University, Thailand. The financial support came from the Faculty of Science grant no. SRIF-JRG-2564-07 and SRIF-JRG-2565-12. We thank our students in Parasitology and Medical Malacology Research Unit of SUT for their dedicated field and laboratory work. Thank also for the graduate research assistant scholarships SCSU-STA-2564-10, SCSU-STA-2565-03, SCSU-STA-2565-05, and SCSU-STA-2565-06. We are indebted to the reviewers and the editor for their instructive comments and suggestions to the manuscript.