Corresponding author: Matthias Glaubrecht (
Academic editor: Andreas Schmidt-Rhaesa
Minute intestinal flukes from several distinct families of endoparasitic platyhelminths are a medically important group of foodborne trematodes prevalent throughout Southeast Asia and Australasia. Their lifecycle is complex, with freshwater snails as primary intermediate hosts, with infecting multiple species of arthropods and fish as second intermediate hosts, and with birds and mammals including humans as definitive hosts. In Southeast Asian countries, the diversity of snail species of the
Trematodes (or flatworms) are endoparasitic platyhelminths that not only infect fishes, birds and other wildlife worldwide but also mammals as well as humans. As foodborne parasites they are of medical importance resulting in significant morbidities and mortalities worldwide. For example, the disability adjusted life years (also known as DALYs) for the foodborne trematodiases including
Especially as liver flukes and intestinal flukes human infecting parasites are highly prevalent in Southeast Asian countries (
Trematodes often have very complex life cycles involving at least one, sometimes two or four, but usually three different hosts, of which the first is almost always a mollusc (
The occurrence of trematodes depends on the presence of first and second intermediate host species, as well as the eating habit of local people (
In the present study, the cercarial fauna of
Here we apply, aside from traditional morphological methods, molecular genetic techniques in order to delimit species of cercariae; i.e. sequencing parts of the nuclear ribosomal RNA gene cluster that have been shown to be efficient for the identification of species of trematodes from their distinct life stages (
Specimens of
Snail collections were done during two periods. In the first period, from 2004 to 2009, the snails were collected every two months for one year from each of all the locations. During the second period, from 2014 to 2016, the same localities were visited again, but additional samples were also taken at several new localities, this time collected once only from each location. The snails were collected using the counts per unit of time sampling method (
Collected snails were investigated for trematode infections by using shedding and crushing methods. Descriptions of their morphology were based on living cercariae that had escaped from the snails. The emerged cercariae were studied unstained or vitally stained with 0.5% neutral red. Details of the cercariae were drawn using a camera lucida and identified according to
The preserved cercariae were processed for molecular identification at the Department of Animal Diversity, Zoological Museum of the Center for Natural History (CeNak), Universität Hamburg, Germany. Genomic DNA from the cercariae was extracted using the DNeasy blood and animal tissue kit (QIAGEN, Venlo, The Netherlands). Amplification by polymerase chain reaction (PCR) of the nuclear internal transcribed spacer 2 (ITS2) region were performed with the following primers ITS2-F (5'-CTT GAACGC ACA TTG CGG CCA TGG G-3') and ITS2-R: (5'-GCG GGT AAT CACGTC TGA GCC GAG G-3') (
List of ITS2 sequences used for the phylogenetic analysis. For SUT numbers, see the material lists in the main part of the text.
Species of cercariae | Type of cercariae | Locality | GenBank accession number | Reference |
---|---|---|---|---|
|
– | – |
|
C. Y. Liu (unpubl.) |
|
Xiphidiocercariae | – |
|
|
|
Xiphidiocercariae | – |
|
|
|
Xiphidiocercariae | SUT 0515066 B |
|
This study |
SUT 0515067 B |
|
This study | ||
SUT 0515077 B |
|
This study | ||
SUT 0515079 C |
|
This study | ||
SUT 0515087 B |
|
This study | ||
SUT 0515090 B |
|
This study | ||
SUT 0516106 A |
|
This study | ||
SUT 0516109 B |
|
This study | ||
SUT 0516118 B |
|
This study | ||
SUT 0516121 A |
|
This study | ||
SUT 0516125 A |
|
This study | ||
SUT 0516128 B |
|
This study | ||
SUT 0516129 B |
|
This study | ||
SUT 0516130 B |
|
This study | ||
SUT 0516139 B |
|
This study | ||
SUT 0516145 B |
|
This study | ||
|
Xiphidiocercariae | SUT 0516109 B |
|
This study |
SUT 0516143 B |
|
This study | ||
|
Xiphidiocercariae | SUT 0516124 A |
|
This study |
SUT 0516138 B |
|
This study | ||
|
Parapleurophocercous cercariae | – |
|
|
– |
|
|
||
|
Parapleurophocercous cercariae | SUT 0515090 B |
|
This study |
SUT 0516125 A |
|
This study | ||
– |
|
|
||
|
Parapleurophocercous cercariae | SUT 0515058 A |
|
This study |
SUT 0515059 B |
|
This study | ||
SUT 0515071 A |
|
This study | ||
SUT 0515072 B |
|
This study | ||
SUT 0515074 B |
|
This study | ||
SUT 0515075 B |
|
This study | ||
SUT 0515078 B |
|
This study | ||
SUT 0515086 A |
|
This study | ||
SUT 0516138 B |
|
This study | ||
SUT 0516139 B |
|
This study | ||
SUT 0516142 B |
|
This study | ||
|
Pleurophocercous cercariae | SUT 0516102 B |
|
This study |
SUT 0516109 B |
|
This study | ||
SUT 0516125 A |
|
This study | ||
SUT 0516142 B |
|
This study | ||
Pleurophocercous cercariae | – |
|
M. Karamian, S. M. Sadjjadi and B. Farhangmehr (unpubl.) | |
Pleurophocercous cercariae | – |
|
|
|
|
Pleurophocercous cercariae | – |
|
|
|
Pleurophocercous cercariae | – |
|
|
|
Megarulous cercariae | SUT 0515058 A |
|
This study |
– |
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|
||
Echinostome cercariae | Echinostome cercariae | SUT 0515086 A |
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This study |
Gymnocephalous cercariae | Gymnocephalous cercariae | SUT 0515059 B |
|
This study |
|
Gymnocephalous cercariae | – |
|
|
|
Gymnocephalous cercariae | – |
|
M. D. Bargues and S. Mas-Coma (unpubl.) |
– |
|
|
Specimens of
Shells of
Localities, number of collected snails, number of infected snails and trematodes obtained from collected snails; sampling periods: 2004–2009 and 2014–2016.
No. | Voucher Number | Location |
|
2004–2009 | 2014–2016 | ||||
---|---|---|---|---|---|---|---|---|---|
No. of collected snails | No. of infected snails | Infection rates (%) | No. of collected snails | No. of infected snails | Infection rates (%) | ||||
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SUT 0515083 | Huai Pa Hung (Pai drainage, Salween river system), Pang Mapha District, Mae Hong Son Province | * | * | * | 179 | 1: |
0.56 | |
|
SUT 0515081 | Huay Nam Kong (Salween river system), Muang District, Mae Hong Son Province | * | * | * | 24 | 0 | 0 | |
|
SUT 0515077 | Tham Pla (Pai drainage, Salween river system), Muang District, Mae Hong Son Province | 185 | 144: |
77.84 | 179 | 8: |
4.47 | |
|
SUT 0515078 | Pai river (Pai drainage, Salween river system), Muang District, Mae Hong Son Province | * | * | * | 64 | 1: |
1.56 | |
|
SUT 0515079 | Huay Sua Tao (Pai drainage, Salween river system), Muang District, Mae Hong Son Province | 574 | 98: |
17.07 | 153 | 2: |
1.31 | |
|
SUT 0514052 | Ban Mai Saraphi (Ping drainage, Chao Phraya river system), Chom Thong District, Chiang Mai Province | * | * | * | 162 | 11: |
6.79 | |
|
SUT 0514051 | Ban Mae Suai Luang (Ping drainage, Chao Phraya river system), Chom Thong District, Chiang Mai Province | * | * | * | 23 | 2: |
8.70 | |
|
SUT 0514054 | Mae Soy bridge (Ping drainage, Chao Phraya river system), Chom Thong District, Chiang Mai Province | * | * | * | 70 | 5: |
7.14 | |
|
SUT 0514050 | Ban Huay Phang (Ping drainage, Chao Phraya river system), Chom Thong District, Chiang Mai Province, | * | * | * | 103 | 0 | 0 | |
|
SUT 0516119 | Thansawan waterfall (Yom drainage, Chao Phraya river system), Chiang Muan District, Phayao Province | 219 | 2: |
0.91 | 17 | 1: |
5.88 | |
|
SUT 0516117 | Yom river (Yom drainage, Chao Phraya river system), Chiang Muan District, Phayao Province | * | * | * | 30 | 0 | 0 | |
|
SUT 0516108 | Mae Nam Saai kg 9 +457 bridge (Yom drainage, Chao Phraya river system), Muang District, Phrae Province | * | * | * | 143 | 0 | 0 | |
|
SUT 0516113 | Mae Marn reservoir (Yom drainage, Chao Phraya river system), Sung Men District, Phrae Province | * | * | * | 52 | 0 | 0 | |
|
SUT 0514045 | Wang river (Wang drainage, Chao Phraya river system), Chae Hom District, Lampang Province | * | * | * | 49 | 12: |
24.49 | |
|
SUT 0514044 | Ban Thung Hang stream (Wang drainage, Chao Phraya river system), Chae Hom District, Lampang Province | * | * | * | 165 | 11: |
6.67 | |
|
SUT 0514046 | Huay MaeYuak (Wang drainage, Chao Phraya river system), Chae Hom District, Lampang Province | * | * | * | 44 | 1: |
2.27 | |
|
SUT 0516124 | km. 40+075 bridge (Wang drainage, Chao Phraya river system), Chae Hom District, Lampang Province | * | * | * | 59 | 4: |
6.78 | |
|
SUT 0515090 | Wa river (Nan drainage, Chao, Phraya river system), Bo Kluea District, Nan Province | * | * | * | 159 | 16: |
10.06 | |
|
SUT 0516114 | Huay Si Pun reservoir (Nan drainage, Chao Phraya river system), Ban Luang District, Nan Province | * | * | * | 108 | 0 | 0 | |
|
SUT 0516109 | Mae pool waterfall (Nan drainage, Chao Phraya river system), Laplae District, Uttaradit Province | 137 | 43: |
31.39 | 91 | 10: |
10.99 | |
|
SUT 0516112 | Kaeng Sai Ngam (Nan drainage, Chao Phraya river system), Tha Pla District, Uttaradit Province | * | * | * | 32 | 0 | 0 | |
|
SUT 0513019 | Kaeng Wangwua (Nan drainage, Chao Phraya river system), Tha Pla District, Uttaradit Province | * | * | * | 292 | 4: |
1.37 | |
|
SUT 0513023 | Huai Nam Re Noi (Nan drainage, Chao Phraya river system), Tha Pla District, Uttaradit Province | * | * | * | 155 | 0 | 0 | |
|
SUT 0516103 | Tat Duen waterfall (Yom drainage, Chao Phraya river system), Si Satchanalai District, Sukhothai Province | 300 | 141: |
47 | 137 | 0 | 0 | |
|
SUT 0516102 | Si Satchanalai national park (Yom drainage, Chao Phraya river system), Si Satchanalai District, Sukhothai Province | 749 | 262: |
34.98 | 147 | 1: |
0.68 | |
|
SUT 0515075 | Cheek point near moei river (Moei drainage, Salween river system), Tha Song Yang District, Tak Province | * | * | * | 55 | 9: |
16.36 | |
|
SUT 0515076 | Mae Salit Luang harbour (Moei drainage, Salween river system), Tha Song Yang District, Tak Province | * | * | * | 25 | 0 | 0 | |
|
SUT 0515073 | Ban Wang Takhian (Moei drainage, Salween river system), Mae Sot District, Tak Province | * | * | * | 17 | 0 | 0 | |
|
SUT 0515072 | Thong Dee harbour (Moei drainage, Salween river system), Mae Sot District, Tak Province | * | * | * | 304 | 21: |
6.91 | |
|
SUT 0515074 | Ban Huay Muang (Moei drainage, Salween river system), Mae Sot District, Tak Province | * | * | * | 300 | 21: |
7.00 | |
|
SUT 0516126 | Ban Pak Huay Mae Tho (Ping drainage, Chao Phraya river system), Muang District, Tak Province | * | * | * | 150 | 3: |
2.00 | |
|
SUT 0516121 | Kaeng Wang Nam Yen (Khek drainage, Chao Phraya river system), Khao Kho District, Phetchabun Province | * | * | * | 9 | 8: |
88.89 | |
|
SUT 0516120 | Rajapruek resort (Khek drainage, Chao Phraya river system), Khao Kho District, Phetchabun Province | * | * | * | 52 | 28: |
53.85 | |
|
SUT 0516123 | Huai Sa Dao Pong (Khek drainage, Chao Phraya river system), Khao Kho District, Phetchabun Province | * | * | * | 31 | 0 | 0 | |
|
SUT 0515088 | Kaeng Bang Ra Chan (Khek drainage, Chao Phraya river system), Khao Kho District, Phetchabun Province | * | * | * | 71 | 6: |
8.45 | |
|
SUT 0516129 | Sam Sip Khot waterfall (Pa Sak drainage, Chao Phraya river system), Khao Kho District, Phetchabun Province | * | * | * | 47 | 18: |
38.30 | |
|
SUT 0514041 | Ban Wang Ta Pak Moo 13 (Pa Sak drainage, Chao Phraya river system), Wichian Buri District, Phetchabun Province | * | * | * | 312 | 0 | 0 | |
|
SUT 0514042 | Huai Leng (Pa Sak drainage, Chao Phraya river system), Wichian Buri District, Phetchabun Province | * | * | * | 84 | 0 | 0 | |
|
SUT 0514040 | Ban Wang Tian (Pa Sak drainage, Chao Phraya river system), Wichian Buri District, Phetchabun Province | * | * | * | 212 | 0 | 0 | |
|
SUT 0514043 | Huay Range reservoir, Ban Wang Ta Pak (Pa Sak drainage, Chao Phraya river system), Wichian Buri District, Phetchabun Province | * | * | * | 128 | 0 | 0 | |
|
SUT 0516130 | Than Thip waterfall (Pa Sak drainage, Chao Phraya river system), Lom Sak District, Phetchabun Province | * | * | * | 41 | 16: |
39.02 | |
|
SUT 0515087 | Ban Kaeng Lat (Khek drainage, Chao Phraya river system), Nakhon Thai District, Phitsanulok Province | * | * | * | 14 | 5: |
35.71 | |
|
SUT 0516118 | Kaeng Sopha (Khek drainage, Chao Phraya river system), Wang Thong District, Phitsanulok Province | 282 | 72: |
25.53 | 30 | 2: |
6.67 | |
|
SUT 0515067 | Poi waterfall (Khek drainage, Chao Phraya river system), Wang Thong District, Phitsanulok Province | * | * | * | 83 | 9: |
10.84 | |
|
SUT 0516105 | Phunamkej Resort (Khek drainage, Chao Phraya river system), Wang Thong District, Phitsanulok Province | * | * | * | 73 | 0 | 0 | |
|
SUT 0516111 | Kaeng Nangkoi (Khek drainage, Chao Phraya river system), Wang Thong District, Phitsanulok Province | * | * | * | 15 | 0 | 0 | |
|
SUT 0516106 | Kaeng Hom (Khek drainage, Chao Phraya river system), Nakhon Thai District, Phitsanulok Province | * | * | * | 95 | 0 | 0 | |
|
SUT 0515086 | Huai Nam Sai (Khek drainage, Chao Phraya river system), Nakhon Thai District, Phitsanulok Province | * | * | * | 93 | 38: |
40.86 | |
|
|||||||||
|
SUT 0516128 | Tat Kok Tup waterfall (Loei drainage, Mekong river system), Phu Luang District, Loei Province | * | * | * | 45 | 12: |
26.67 | |
|
SUT 0515068 | Pla Ba waterfall (Mekong river system), Phu Ruea District, Loei Province | 53 | 1: |
1.89 | 178 | 3: |
1.69 | |
|
SUT 0516125 | km. 50+350 Loei river (Loei drainage, Mekong river system), Phu Luang District, Loei Province | * | * | * | 55 | 13: |
23.64 | |
|
SUT 0515064 | Bueng Thung Sang (Chi drainage, Mekong river system), Muang District, Khon Kaen Province | * | * | * | 20 | 0 | 0 | |
|
SUT 0516131 | Lamphraphloeng reservoir (Mun drainage, Mekong river system), Pak Thong Chai District, Nakhon Ratchasima Province | * | * | * | 36 | 0 | 0 | |
|
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|
SUT 0516135 | Mae Rumphueng Beach (Mae Rumphueng canal, Gulf of Thailand), Muang Rayong District, Rayong Province | * | * | * | 150 | 0 | 0 | |
|
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|
SUT 0516127 | Bung Boraphet (Chao Phraya river system), Muang District, Nakhon Sawan Province | * | * | * | 42 | 1: |
2.38 | |
|
SUT 0516133 | Dong Phaya Yen waterfall (Pa Sak drainage, Chao Phraya river system), Muak Lek District, Sara Buri Province | 371 | 1: |
0.27 | 27 | 1: |
3.70 | |
|
SUT 0516132 | Suanmaduea waterfall (Pa Sak drainage, Chao Phraya river system), Phatthana Nikhom District, Lop Buri Province | 358 | 5: |
1.40 | 48 | 0 | 0 | |
|
SUT 0515055 | Pond of Silpakorn University (Tha Chin river system), Muang District, Nakhon Pathom Province | 381 | 2: |
0.52 | 30 | 0 | 0 | |
|
SUT 0515091 | Hin dad hot spring (Khwae Noi drainage, Mae Klong river system), Thong Pha Phum District, Kanchanaburi Province | 39 | 5: |
12.82 | 2 | 0 | 0 | |
|
SUT 0515092 | Sai Yok Yai waterfall (Khwae drainage, Mae Klong river system), Sai Yok District, Kanchanaburi Province | * | * | * | 49 | 0 | 0 | |
|
SUT 0515093 | Sai Yok Noi waterfall (Khwae drainage, Mae Klong river system), Sai Yok District, Kanchanaburi Province | * | * | * | 29 | 0 | 0 | |
|
SUT 0515061 | Ban Thung Makham Tia (Phachi drainage, Mae Klong river system), Dan Makham Tia District, Kanchanaburi Province | * | * | * | 42 | 1: |
2.38 | |
|
SUT 0515060 | Ban Ta Pu (Phachi drainage, Mae Klong river system), Dan Makham Tia District, Kanchanaburi Province | * | * | * | 99 | 0 | 0 | |
|
SUT 0515059 | Ban Nong Phai (Phachi drainage, Mae Klong river system), Dan Makham Tia District, Kanchanaburi Province | * | * | * | 118 | 5: |
4.24 | |
|
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|
SUT 0515066 | Ban Purakom (Phachi drainage, Mae Klong river system), Suan Phueng District, Ratchaburi Province | * | * | * | 280 | 30: |
10.71 | |
|
SUT 0515069 | Huay Nueng (Phachi drainage, Mae Klong river system), Suan Phueng District, Ratchaburi Province | 832 | 94: |
11.30 | 272 | 23: |
8.46 | |
|
SUT 0515070 | Lum Nam Phachi (Phachi drainage, Mae Klong river system), Suan Phueng District, Ratchaburi Province | * | * | * | 242 | 5: |
2.07 | |
|
SUT 0515057 | Ban Dan Thap Tako (Phachi drainage, Mae Klong river system), Chom Bueng District, Ratchaburi Province | * | * | * | 240 | 11: |
4.58 | |
|
SUT 0515058 | Phachi river Bridge (Phachi drainage, Mae Klong river system), Chom Bueng District, Ratchaburi Province | * | * | * | 292 | 16: |
5.48 | |
|
SUT 0515056 | Ban Pa Wai (Phachi drainage, Mae Klong river system), Chom Bueng District, Ratchaburi Province | * | * | * | 111 | 11: |
9.91 | |
|
SUT 0515071 | Huai Ban Bor (Phachi drainage, Mae Klong river system), Suan Phueng District, Ratchaburi Province | * | * | * | 196 | 21: |
10.71 | |
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SUT 0513032 | Khlong Cha-am (Cha-am canal, Gulf of Thailand), Cha-am District, Phetchaburi Province | * | * | * | 72 | 0 | 0 | |
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SUT 0516146 | Khlong Bueng reservoir (Bueng canal, Gulf of Thailand), Muang District, Prachuap Khiri Khan Province | * | * | * | 92 | 0 | 0 | |
|
SUT 0514037 | Khlong Huai Yang (Yang canal), Thap Sakae District, Prachuap Khiri Khan Province | 961 | 1: |
0.10 | 22 | 0 | 0 | |
|
SUT 0514038 | Kar on waterfall (Nongyaplong canal), Bang Saphan District, Prachuap Khiri Khan Province | 685 | 5: |
0.73 | 39 | 0 | 0 | |
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SUT 0516149 | Krapo waterfall (Tha Sae canal), Tha Sae District, Chumphon Province | 223 | 181: |
81.17 | 30 | 0 | 0 | |
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SUT 0516137 | Khlong Klai (Nong Noi canal, Ta Pi river system), Ban Na San District, Surat Thani Province | * | * | * | 104 | 4: |
3.85 | |
|
SUT 0514048 | Dat Fa waterfall (Lumpool canal, Ta Pi river system), Ban Na San District, Surat Thani Province | * | * | * | 144 | 2: |
1.39 | |
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SUT 0516142 | Vibhavadi waterfall (Tha Thong canal), Don Sak District, Surat Thani Province | * | * | * | 107 | 24: |
22.43 | |
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SUT 0516147 | Khlong Tha Sai (Takhoei canal, Gulf of Thailand), Tha Chang District, Surat Thani Province | * | * | * | 20 | 0 | 0 | |
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SUT 0516148 | Ban Tung Ao (Ta Khoei canal, Gulf of Thailand), Phunphin District, Surat Thani Province | * | * | * | 35 | 0 | 0 | |
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SUT 0516145 | Krung Ching waterfall (Klai canal), Nopphitam District, Nakhon Si Thammarat Province | 157 | 12: |
7.64 | 22 | 4: |
18.18 | |
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SUT 0516139 | Khlong Prong (Klai canal), Nopphitam District, Nakhon Si Thammarat Province | * | * | * | 50 | 11: |
22.00 | |
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SUT 0515097 | Khlong Sai (Khlong Sai canal, Andaman sea), Muang District, Krabi Province | * | * | * | 5 | 0 | 0 | |
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SUT 0515098 | Wang Than Thip (Wang Than Thip canal, Andaman sea), Muang District, Krabi Province | * | * | * | 42 | 0 | 0 | |
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SUT 0515095 | Khlong Palian (Palian canal), Yan Ta Khao District, Trang Province | 77 | 15: |
19.48 | 1">15 | 4: |
26.67 | |
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SUT 0516138 | Khlong Tha Leung (Tha Nae canal), Si Banphot District, Phatthalung Province | * | * | * | 36 | 14: |
38.89 | |
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SUT 0516141 | Khlong La reservoir (Utaphao canal, Gulf of Thailand), Khlong Hoi Khong District, Songkhla Province | * | * | * | 35 | 0 | 0 | |
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SUT 0516144 | Khlong Sathing Mo (Songkhla lake, Gulf of Thailand), Singhanakhon District, Songkhla Province | * | * | * | 3 | 0 | 0 | |
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SUT 0516143 | Khlong Cham Rai reservoir (Utaphao canal), Khlong Hoi Khong District, Songkhla Province | * | * | * | 139 | 3: |
2.16 | |
|
6,583 | 1,084 | 16.47 | 8,493 | 493 | 5.80 |
N = North, NE = Northeast, E = East, C = Central, S = South * = no record.
The various trematode cercariae (distinguished and described in more detail below) exhibit a certain geographical pattern within the various water bodies in Thailand. Only two among the fifteen trematode species found in the thiarid
Distribution of
In contrast, several species exhibit a more restricted distribution. For example,
Cercariae of
A total of 15,076 snails of
In this study, neither double trematode infections nor triple trematode infections of collected
Distribution of trematodes obtained from
Type and species of trematodes | 2004–2009 | 2014–2016 | Total | Infection rate (%) |
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---|---|---|---|---|---|---|---|---|---|---|---|---|
No. infected snails | No. infected snails | |||||||||||
N | NE | E | C | S | N | NE | E | C | S | |||
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304 | 0 | 0 | 9 | 75 | 122 | 22 | 0 | 1 | 46 | 579 | 3.84 |
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0 | 0 | 0 | 0 | 0 | 9 | 0 | 0 | 1 | 13 | 23 | 0.15 |
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164 | 1 | 0 | 0 | 2 | 0 | 0 | 0 | 0 | 0 | 167 | 1.11 |
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0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 14 | 15 | 0.10 |
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0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 6 | 7 | 0.05 |
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98 | 0 | 0 | 3 | 0 | 7 | 0 | 0 | 0 | 0 | 108 | 0.72 |
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0 | 0 | 0 | 0 | 0 | 10 | 4 | 0 | 0 | 0 | 14 | 0.09 |
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0 | 0 | 0 | 1 | 229 | 111 | 0 | 0 | 4 | 95 | 440 | 2.92 |
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160 | 0 | 0 | 0 | 0 | 3 | 2 | 0 | 0 | 7 | 172 | 1.14 |
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0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 2 | 3 | 0.02 |
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5 | 0 | 0 | 0 | 2 | 0 | 0 | 0 | 0 | 0 | 7 | 0.05 |
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23 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 23 | 0.15 |
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8 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 8 | 0.05 |
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0 | 0 | 0 | 0 | 0 |
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0 | 0 | 0 | 0 | 0 | 10 | 0 | 0 | 0 | 0 | 10 | 0.07 |
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The cercariae were categorized by their morphology and organ characters, using as reference previous morphological descriptions (e.g.
(Fig.
Body oval; throughout with granules. Oral sucker bigger than ventral sucker; globular in shape and with stylet. Virgulate organ in the anterior part of the body. Pharynx small; an esophagus was not observed. Three pairs of penetration glands present located at about two thirds of the body, two anterior pairs with fine granules and a posterior pair with rather coarse, dark granules. Genital primordial C-shaped; excretory bladder U-shaped. Tail shorter than body; spinose at its tip.
The cercariae develop within sporocysts.
The infection rate was 3.84% (579/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 53–88 μm (mean: 72 μm) × 105–138 μm (mean: 117 μm)
Stylet 5–8 μm (mean: 6 μm) × 20–40 μm (mean: 30 μm)
Oral sucker 23–40 μm (mean: 33 μm) × 23–33 μm (mean: 29 μm)
Pharynx 8–12 μm (mean: 10 μm) × 5–8 μm (mean: 8 μm)
Ventral sucker 13–25 μm (mean: 18 μm) × 8–20 μm (mean: 16 μm)
Excretory bladder 18–55μm (mean: 33 μm) × 10–35 μm (mean: 20 μm)
Tail 10–28 μm (mean: 21 μm) × 25–88 μm (mean: 44 μm)
Images of
(Fig.
Body oval. Oral sucker at the anterior end of body, with stylet. Virgulate organ present. Ventral sucker roundish, smaller than oral sucker. Pharynx very small, a prepharynx, an esophagus and ceca were not observed. Four pairs of penetration glands present, located near the middle of the body; the two anterior pairs with fine granules and the two posterior pairs with coarse granules. Excretory bladder V-shaped. Tail shorter than body, rather slender and spinose at its tip.
The cercariae develop within sporocysts.
The infection rate was 0.15% (23/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 65–93 μm (mean: 81 μm) × 95–120 μm (mean: 108 μm)
Stylet 3–3 μm (mean: 3 μm) × 10–23 μm (mean: 16 μm)
Oral sucker 13–30 μm (mean: 24 μm) × 10–28 μm (mean: 20 μm)
Pharynx 5–15 μm (mean: 10 μm) × 8–10 μm (mean: 8 μm)
Ventral sucker 8–33 μm (mean: 18 μm) × 13–28 μm (mean: 19 μm)
Excretory bladder 13–35 μm (mean: 27 μm) × 13–48 μm (mean: 37 μm)
Tail 15–25 μm (mean: 20 μm) × 40–90 μm (mean: 72 μm)
(Fig.
Body oval. Oral sucker with stylet, virgulate organ near oral sucker. Pharynx round and short, esophagus absent. Ventral sucker smaller than oral sucker. Two pairs of penetration glands present, one anterior pair with fine granules and one posterior pair with coarse granules. Excretory bladder near posterior end of body. Tail short, spinose at its end.
The cercariae develop within sporocysts.
The infection rate was 1.11% (167/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 54–93 μm (mean: 78 μm) × 80–110 μm (mean: 100 μm)
Stylet 9–14 μm (mean: 11 μm) × 12–14 μm (mean: 12 μm)
Oral sucker 26–33 μm (mean: 31 μm) × 35–41 μm (mean: 38 μm)
Pharynx 11–16 μm (mean: 14 μm) × 13–25 μm (mean: 21 μm)
Ventral sucker 15–17 μm (mean: 17 μm) × 16–19 μm (mean: 18 μm)
Excretory bladder 9–13 μm (mean: 10 μm) × 21–47 μm (mean: 39 μm)
Tail 18–26 μm (mean: 24 μm) × 27–76 μm (mean: 69 μm)
(Fig.
Body oval, rather small. Stylet present, but virgulate organ absent. Pharynx small, esophagus Y-shaped. Ventral sucker poorly developed. Two pairs penetration glands present, located near the middle of the body. Excretory bladder thin-walled, located in the posterior part of the body. Tail long and round.
The cercariae develop within sporocysts.
The infection rate was 0.10% (15/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 78–98 μm (mean: 89 μm) × 105–133 μm (mean: 113 μm)
Stylet 3–3 μm (mean: 3 μm) × 10–18 μm (mean: 15 μm)
Oral sucker 18–30 μm (mean: 25 μm) × 20–30 μm (mean: 23 μm)
Pharynx 5–10 μm (mean: 8 μm) × 5–10 μm (mean: 9 μm)
Ventral sucker 15–20 μm (mean: 19 μm) × 15–20 μm (mean: 18 μm)
Excretory bladder 30–40 μm (mean: 34 μm) × 15–18 μm (mean: 16 μm)
Tail 13–20 μm (mean: 16 μm) × 85–125 μm (mean: 106 μm)
(Fig.
Body oval, rather small. Oral and ventral sucker of approximately equal in size. Oral sucker with long stylet, virgulate organ absent. Pharynx rather large, esophagus short and slender, bifurcating, located between oral and ventral sucker. Genital primordium located just posterior of ventral sucker. Four pairs of penetration glands grouped together near anterior margin of ventral sucker. Excretory bladder thin-walled. Tail shorter than body and round, not spinose at its tip.
The cercariae develop within sporocysts.
The infection rate was 0.05% (7/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 73–103 μm (mean: 89 μm) × 85–128 μm (mean: 106 μm)
Stylet 3–3 μm (mean: 3 μm) × 13–18 μm (mean: 16 μm)
Oral sucker 20–30 μm (mean: 25 μm) × 13–30 μm (mean: 24 μm)
Pharynx 8–13 μm (mean: 9 μm) × 5–13 μm (mean: 9 μm)
Ventral sucker 13–20 μm (mean: 16 μm) × 10–20 μm (mean: 15 μm)
Excretory bladder 18–35 μm (mean: 28 μm) × 13–23 μm (mean: 16 μm)
Tail 15–28 μm (mean: 20 μm) × 65–113 μm (mean: 82 μm)
(Fig.
The cercarial body is pear-shaped. It has a circular oral sucker that is located near the proximal end of the body. The mouth is equipped with transverse rows of spines. The small ventral sucker is located approximately at two-thirds of the body length measured from the front. The small pharynx is situated in the anterior part of the body just distal of the oral sucker between the two distinct eyespots; an esophagus is absent. There are seven pairs of penetration glands, which are arranged laterally in two longitudinal rows in the posterior two thirds of the body. The excretory bladder has an oval shape and is dark pigmented. A genital primordium is present, located between the ventral sucker and the excretory bladder. The tail is longer than the body and rather slender, and is equipped with lateral finfolds proximally and a dorsoventral finfold along the longer distal portion.
The cercariae develop within rediae.
The infection rate was 0.72% (108/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 91–141 μm (mean: 125 μm) × 169–296 μm (mean: 258 μm)
Oral sucker 28–49 μm (mean: 37 μm) × 28–49 μm (mean: 36 μm)
Pharynx 9–11 μm (mean: 10 μm) × 13–20 μm (mean: 16 μm)
Ventral sucker 15–25 μm (mean: 19 μm) × 15–24 μm (mean: 18 μm)
Excretory bladder 29–41 μm (mean: 35 μm) × 29–41 μm (mean: 35 μm)
Tail 11–37 μm (mean: 31 μm) × 466–529 μm (mean: 491 μm)
Lateral finfolds 9–18 µm (mean: 14.75 µm) × 70–129 µm (mean: 111 µm)
(Fig.
Body is oval in shape. The oral sucker is located at the anterior of body. The mouth aperture is equipped with transverse rows of spines. A pair of pigmented eyespots and pharynx are present. Seven pairs of penetration glands extend from the pharynx to the posterior end of the body. Cystogenous cells are arranged in lateral fields from the level of the pharynx to the posterior end of the body. The excretory bladder is saccular and thick-walled. The tail is longer than the body. There are lateral finfolds at one-third of tail tunk and a dorso-ventral finfold at the distal portion.
The cercariae develop within rediae.
The infection rate was 0.09% (14/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 43–83 µm (mean: 61 µm) × 105–140 µm (mean: 120 µm)
Oral sucker 20–30 µm (mean: 25 µm) × 23–35 µm (mean: 28 µm)
Ventral sucker 15–33 µm (mean: 23 µm) × 18–30 µm (mean: 25 µm)
Pharynx 8–20 µm (mean: 14 µm) × 8–25 µm (mean: 12 µm)
Excretory bladder 10–50 µm (mean: 26 µm) × 20–35 µm (mean: 26 µm)
Tail 20–30 µm (mean: 26 µm) × 263–355 µm (mean: 311 µm)
Lateral finfolds 8–15 µm (mean: 13 µm) × 75–125 µm (mean: 103 µm)
Dorsal finfolds 5–23 µm (mean: 13 µm) × 183–253 µm (mean: 218 µm)
(Fig.
The body is oval in shape. The oral sucker is located at the anterior end of the body. There are three transverse rows of oral spines present. Seven pairs of penetration glands in four groups of 3:4:4:3 are present that are situated between the pharynx and the excretory bladder. A pair of pigmented eyespots and a pharynx are present. The ventral sucker is poorly developed. The excretory bladder is V-shaped and thick-walled. The tail is longer than the body. There is a bilateral finfold and a dorso-ventral finfold on the tail.
The cercariae develop within rediae.
The infection rate was 2.92% (440/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 80–118 μm (mean: 99 μm) × 168–207 μm (mean: 202 μm)
Oral sucker 28–38 μm (mean: 34 μm) × 30–50 μm (mean: 41 μm)
Eye spots 5–15 μm (mean: 9 μm) × 5–15 μm (mean: 9 μm)
Pharynx 10–22 μm (mean: 17 μm) × 10–28 μm (mean: 19 μm)
Ventral sucker 13–35 μm (mean: 23 μm) × 15–45 μm (mean: 27 μm)
Excretory bladder 43–90 μm (mean: 64 μm) × 20–55 μm (mean: 39 μm)
Tail 20–33 μm (mean: 26 μm) × 405–495 μm (mean: 458 μm)
Lateral finfold 10–25 μm (mean: 18 μm) × 74–148 μm (mean: 108)
(Fig.
The body is oval in shape. The oral sucker has oral spines or rostellar hooks like a tapeworm on the dorsal wall of the mouth aperture. A pair of eyespots is located above the prenetration glands at the same level as the pharynx. There are seven pairs of penetration glands. The genital primordial is elongated-triangular and located between the ventral sucker and the excretory bladder. The excretory bladder has dark granules and is thin-walled. The tail is slender and longer than the body. It is equipped with very narrow finfolds.
The cercariae develop within rediae.
The infection rate was 1.14% (172/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 45–73 μm (mean: 65 μm) × 83–121 μm (mean: 118 μm)
Oral sucker 17–27 μm (mean: 25 μm) × 18–30 μm (mean: 26 μm)
Pharynx 8–10 μm (mean: 9 μm) × 9–11 μm (mean: 10 μm)
Ventral sucker 13–17 μm (mean: 15 μm) × 14–18 μm (mean: 16 μm)
Excretory bladder 25–31 μm (mean: 29 μm) × 39–53 μm (mean: 46 μm)
Tail 15–18 μm (mean: 15 μm) × 70–93 μm (mean: 83 μm)
(Fig.
The body is elongate pear-shaped and distinctly granulose. Eyespots are absent. The pharynx is large and extends into an esophagus that is bifurcating (Y-shape) into two blind ending intestinal caeca that almost reach the posterior end of the body. The ventral sucker is bigger than the oral sucker. The excretory bladder is rather small. The tail is about as long as the body and relatively slender. There is an adhesive gland present at its tip.
The cercariae encyst rapidly after developing within rediae.
The infection rate was 0.02% (3/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 143–175 μm (mean: 153 μm) × 438–470 μm (mean: 453 μm)
Oral sucker 50–68 μm (mean: 60 μm) × 63–73 μm (mean: 68 μm)
Pharynx 15–23 μm (mean: 20 μm) × 28–38 μm (mean: 34 μm)
Ventral sucker 60–78 μm (mean: 67 μm) × 48–80 μm (mean: 6 μm)
Excretory bladder 43–48 μm (mean: 45 μm) × 33–40 μm (mean: 36 μm)
Tail 40–50 μm (mean: 45 μm) × 463–475 μm (mean: 469 μm)
(Fig.
The body is elongate-oval, slightly bent. Eyespots, a pharynx, an esophagus, intestinal caeca and a ventral sucker are absent. There is a narrow dorsal finfold in the middle part of the body. The penetration gland is located in the anterior part of the body. The excretory bladder is small and thin-walled, located at the posterior end of the body. The tail is forked. The stem of the tail is rather thick and longer than the furcae. Finfolds are present along the margins of the furcae.
The cercariae develop within sporocysts.
The infection rate was 0.05% (7/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 19–40 μm (mean: 30 μm) × 73–112 μm (mean: 96 μm)
Anterior organ 12–16 μm (mean: 14 μm) × 15–22 μm (mean: 19 μm)
Excretory bladder 4–8 μm (mean: 6 μm) × 12–37 μm (mean: 23 μm)
Tail stem 16–32 μm (mean: 28 μm) × 155–199 μm (mean: 187 μm)
Tail furcal 8–12 μm (mean: 10 μm) × 29–56 μm (mean: 52 μm)
Dorso-median finfold 6–15 μm (mean: 11 μm)
(Fig.
The body is elongate-oval in shape. A pair of unpigmented eyespots is present. A prepharynx is present but rather short. The pharynx is small and roundish in shape. The esophagus is long, bifurcating into two intestinal caeca that are shorter than half the length of the esophagus. The oral sucker is larger than the ventral sucker. There are two pairs of penetration glands, filled with dark granules that are located around the ventral sucker. There is a Y-shaped excretory bladder located medially close to the posterior end of the body. The tail is longer than the body and divided into two furcae. The tail stem is slender and about as long as the furcae.
The cercariae develop within sporocysts.
The infection rate was 0.15% (23/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 106–155 μm (mean: 139 μm) × 186–282 μm (mean: 257 μm)
Oral sucker 29–41 μm (mean: 37 μm) × 29–42 μm (mean: 38 μm)
Pharynx 12–16 μm (mean: 14 μm) × 15–20 μm (mean: 17 μm)
Ventral sucker 16–38 μm (mean: 26 μm) × 16–32 μm (mean: 23 μm)
Tail 49–62 μm (mean: 57 μm) × 221–311 μm (mean: 275 μm)
Fork-tail 40–65 μm (mean: 61 μm) × 241–321 μm (mean: 286 μm)
(Fig.
The body is of a bowl-like shape. The surface of the body is covered with spines that have the appearance of fish scales. The genital pore of the seminal vesicle is located in the anterior part of the body. Eyespots are present. The mouth is located near the ventral sucker. The esophagus is narrow and the intestinal caeca form a ring. There is one pair of testes present, and an ovary is located anterolateral to the left of the testes. The excretory bladder is small and short, and is situated close to the posterior end of the body. The tail is longer than the body and possesses spatulate furcae. At the base of the tail a pair of bilaterally symmetrical appendages is present, each equipped with an adhesive pad at its distal end.
The cercariae develop within rediae.
The infection rate was 0.05% (8/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 460–600 µm (mean: 533 µm) × 280–430 µm (mean: 362 µm)
Genital pore 20–40 µm (mean: 31 µm) × 20–50 µm (mean: 34 µm)
Ventral sucker 50–110 µm (mean: 76 µm) × 50–120 µm (mean: 77 µm)
Testis 30–120 µm (mean: 88 µm) × 40–120 µm (mean: 85 µm)
Excretory bladder 20–70 µm (mean: 40 µm) × 40–90 µm (mean: 57 µm)
Tail 120–180 µm (mean: 146 µm) × 620–800 µm (mean: 686 µm)
Tail stem 120–180 µm (mean: 146 µm) × 390–530 µm (mean: 467 µm)
Tail furcal 80–150 µm (mean: 111 µm) × 180–290 µm (mean: 219 µm)
Appendages 40–70 µm (mean: 58 µm) × 120–150 µm (mean: 138 µm)
(Fig.
The body is elongate pear-shaped. Eyespots are absent. The oral sucker is circular in shape and is equipped with collar spines. The prepharynx is long. The esophagus is shorter than the prepharynx, bifurcating into two intestinal caeca that almost reach to the posterior end of the body. The relatively large ventral sucker is located approximately at two-thirds of the body length measured from the front. Penetration glands are absent. The excretory bladder is small and triangular in shape, its two main collecting tubes beginning at the level of the esophagus. The tail is slender and almost of the same length as the body.
The cercariae develop within rediae.
The infection rate was 0.07% (10/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 150–163 µm (mean: 151 µm) × 243–325 µm (mean: 270 µm)
Oral sucker 38–48 µm (mean: 44 µm) × 38–48 µm (mean: 44 µm)
Ventral sucker 40–73 µm (mean: 62 µm) × 55–63 µm (mean: 60 µm)
Pharynx 13–18 µm (mean: 14 µm) × 20–30 µm (mean: 24 µm)
Excretory bladder 18–55 µm (mean: 38 µm) × 18–55 µm (mean: 33 µm)
Tail 28–40 µm (mean: 34 µm) × 195–313 µm (mean: 240 µm)
Echinostome cercaria.
(Fig.
The body is oval and covered with spines. The terminal oral sucker is equipped with minute spines. Eyespots are absent. The prepharynx is long and thin. The pharynx is rather large and of a round shape. The esophagus is short but rather wide, bifurcating into two intestinal caeca that extend towards the posterior part of the body. There are 4–5 penetration glands present that are located laterally of the caeca between the level of the pharynx and the ventral sucker. The ventral sucker is of about the same size as the oral sucker. The excretory bladder is roundish, with a thin wall and located medially near the posterior end of the body. Two thin, undulating excretory tubules that begin just anterior of the pharynx insert into the excretory bladder. The tail is longer than the body, with the opening duct of the excretory bladder located at its end. There are groups of of 3–5 distinct pigment granules present in the tail but flame cells could not observed.
The cercariae develop within rediae.
The infection rate was 0.01% (1/15,076) (Table
Size range and average size (in micrometers, calculated from 10 cercariae):
Body 115–160 μm (mean: 134 μm) × 150–195 μm (mean: 176 μm)
Oral sucker 30–40 μm (mean: 33 μm) × 28–40 μm (mean: 36 μm)
Pharynx 8–20 μm (mean: 13 μm) × 13–28 μm (mean: 22 μm)
Ventral sucker 35–48 μm (mean: 41 μm) × 33–45 μm (mean: 41 μm)
Excretory bladder 28–45 μm (mean: 39 μm) × 25–43 μm (mean: 31 μm)
Tail 23–35 μm (mean: 27 μm) × 183–223 μm (mean: 199 μm)
Gymnocephalous cercaria.
In the present study, ITS2 sequences from nine distinct cercarial types (collected during the second period of this study) of a total of fifteen trematode species found in Thai populations of
The phylogenetic tree obtained from the neighbor-joining analysis (Fig.
Neighbor-joining tree on the basis of ITS2 sequences of cercarial species obtained from Thai populations of
– Specimens of
– The sequences of the echinostome cercaria and the gymnocephalous cercaria obtained from
– This latter clade in turn formed a well-supported clade together with
– A group of species with arthropods as second intermediate hosts, i.e.
Thiarid gastropods, that transmit parasites of native birds, fishes or mammals, have frequently been reported as first intermediate hosts of trematodes affecting the respiratory, intestinal and hepatic systems not only in some domestic animals but also in humans. As outlined in the Introduction, this represents a serious threat to public health. For example, thiarid snails such as
The present study aimed at bringing together the classical parasitological approach of the morphological characterization of the cercariae stages of trematodes obtained from their snail host, with a molecular parasitology approach, presenting a phylogenetic analyses of the minute intestinal flukes identified from their thiarids host, exemplified here for the first time with
We here focussed on the larval trematode infections found in this snail collected in various regions in Thailand during two periods of field work. When we started the research in the first period (2004–2009),
As we mentioned above, only three species of trematodes, viz.
In the following we discuss in more details various aspects for the distinct trematode species found in their Thai thiarid snail host
Parapleurophocercous cercariae and pleurophocercous cercariae were reported to be commonly found also in other freshwater snails in Thailand, such as e.g.
Various reports have indicated the presence of parapleurophocercous cercariae and some species of pleurophocercous cercariae of the intestinal trematodes
In this study, we found human trematodes, viz.
Therefore, it is from this perspective that for the epidemiology of zoonosis in general we recommend the study of snail intermediate hosts of human and animal trematode infections. It would be interesting to study whether there are geographically related higher or lower incidences of human infections, perhaps also correlated to infected fishes in these areas.
In contrast, known as parasites to animals only, xiphidiocercariae can be distinguished by their stylet organ in the mouth part of the cercariae. They can be divided into two morphological types, the first type being the virgulate xiphidiocercariae, and the second type the armatae xiphidiocercariae (see e.g.
Megarulous cercariae have been morphologically characterized as belonging to
Furcocercous cercariae are generally from trematodes of the
Echinostome cercariae are distributed throughout Southeast Asia (
Gymnocephalous cercariae are small larval stages of trematodes, in general attributed to the
In a previous report, the gymnocephalous cercariae were produced by trematodes of the
In general, morphological as well as molecular studies of cercariae were able to confirm the specific identity and prevalence of various infectious trematodes in Thai freshwater snails of
We also used the ITS2 marker for a phylogenetic reconstruction (Fig.
The first group with parapleurophocercous and pleurophocercous cercariae, respectively (marked f and g in Fig.
In a second group cluster trematode species with virgulate xiphidiocercariae and armatae xiphidiocercariae, respectively (marked a and b in Fig.
In addition, also the sequences of trematode species with echinostome cercaria and the gymnocephalous cercaria obtained from
We anticipate that more detailed studies, based on molecular phylogenetic analyses, looking into these and other correlations of intermediate hosts, their regional occurrences and ecological specifics will shed more light on the evolutionary potential of trematode parasites from thiarid snails.
To date, studies on freshwater snails and their interactions with parasitic trematodes are under-represented worldwide (Adema et al. 2012). There is an urgent need for collaboration bringing together deeper understanding on the basic biology, biodiversity, and evolutionary associations of parasitic trematodes on the one hand and their snail hosts on the other, i.e. those studying parasitology and malacology, taking advantage of their respective expertise in host-parasite interactions and evolutionary systematics.
Accordingly, the aims of this approach presented here were to establish reliable and reproducible data for the morphological identification as well as the methodology for the extraction of high quality DNA from preserved trematode cercariae in specifically known populations of their thiarid snails hosts (including museum samples collected several years ago). It was also the aim to conduct a phylogenetic analysis of the minute intestinal flukes. In addition, the present paper adds to a more in-depth evolutionary systematic analysis with data on reproductive biology, geographical distribution, morphology and molecular phylogenies of
Using this combinational approach, it will eventually be possible to identify in more details the host-parasite relationships of thiarid snails as first intermediate host populations not only in Thailand, and also to determine the role of parasitic infections in these gastropods and as human pathogens.
This research was supported by the Research and Development Institute, Silpakorn University, Thailand. We also thank the Department of Biology, Faculty of Science, Silpakorn University. We are grateful for financial support from the Thailand Research Fund through the Royal Golden Jubilee Ph. D. Program (Grant No. PHD/0093/2556) and the Deutsche Akademische Austauschdienst (DAAD) to Nuanpan Veeravechsukij, Duangduen Krailas and Matthias Glaubrecht. The study was also supported through a collaboration grant from the Deutsche Forschungsgemeinschaft (DFG) to MG, which is thankfully acknowledged here. Comments from reviewers and the subject editor helped in improving the manuscript of the paper.