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Prevalence of Zoonotic Trematode Metacercariae in Freshwater Fish from Gangwon-do, Korea
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Korean J Parasito > Volume 52(4):2014 > Article
Cho, Lee, Kim, Seok, Lee, Jeong, Na, and Sohn: Prevalence of Zoonotic Trematode Metacercariae in Freshwater Fish from Gangwon-do, Korea

Abstract

The infection status of zoonotic trematode metacercariae was investigated in a total of 2,293 freshwater fish collected from 11 rivers or streams in 9 administrative regions of Gangwon-do, Korea for 5 years (2009-2013). All fish were collected by netting methods and examined using the artificial digestion methods. Clonorchis sinensis metacercariae were detected in 4 fish species, i.e., Pungtungia herzi, Squalidus japonicus coreanus, Acheilognathus rhombeus, and Ladislabia taczanowskii, from only Hantangang in Cheorwon-gun. Metagonimus spp. metacercariae were found in 1,154 (50.3%) fish and their average number per infected fish was 55.8. Among the positive fish species, especially Tribolodon hakonensis from Namdaecheon in Yangyang-gun and Plecoglossus altivelis from Osipcheon in Samcheok-si were most heavily infected. Centrocestus armatus metacercariae were detected in 611 (26.7%) fish and the average metacercarial burden per infected fish was 1,032. Two chub species, Zacco platypus and Zacco temminckii were highly and heavily infected with C. armatus metacercariae in almost all regions surveyed. Echinostoma spp. metacercariae were also found in 24 fish from a few localities, but their numbers per fish infected were very low. From the above results, it is confirmed that the metacercariae of intestinal flukes, especially Metagonimus spp. and C. armatus, were heavily infected, while C. sinensis metacercariae were rarely found in fish from Gangwon-do, Korea.

INTRODUCTION

Soil-transmitted nematodiases were one of the national health problems in the Republic of Korea (=Korea) in old days, before 1980. However, they are no longer a public health problem these days. On the other hand, the prevalence of zoonotic trematode (mainly fishborne trematodes: FBTs) infections, including clonorchiasis, is maintained high, and they became the most important parasitic diseases in some endemic areas, especially in riverside areas of 7 major rivers, i.e., Hangang (River), Gumgang, Mangyeonggang, Yeongsangang, Tamjingang, Seomjingang, and Nakdonggang, in Korea [1,2,3,4]. Human infections with FBTs are usually caused by habitual consumption of raw fish containing infective larvae, metacercariae. The endemic areas of FBT infections are highly localized depending on the food habits of residents and on the presence of susceptible intermediate hosts [5]. Moreover, FBTs show low host-specificity, and then many kinds of reservoir hosts can contribute to the maintenance of their life cycles. Thus, the infection status of FBT metacercariae in intermediate hosts is one of the important epidemiological indices together with the status of adult worm infections in the definitive and reservoir hosts [6,7,8,9,10].
Gangwon-do (Province) is located at the northeast (between 37°02' and 38°37' N; 127°05' and 129°22' E) of Korea, and comprised of 7 si (City) and 11 gun (County). The landscape of this province is dominated by Taebaek Mountains, of which mountainous areas occupy the most areas of the province and retained the head streams of Hangang and Nakdonggang [11].
Epidemiological studies have been performed to investigate the infection status of FBTs, including Metagonimus spp. in Gangwon-do. Most of these studies were performed before an early 1990's and focused on the infection status with M. yokogawai metacercariae in sweetfish, Plecoglossus altivelis, from rivers and streams in the east coast of Gangwon-do [12,13,14,15,16,17,18]. In addition, metacercarial infections of Metagonimus spp. and Echinostoma hortense were investigated in some species of freshwater fish from several regions in Gangwon-do [19,20,21,22,23]. However, large-scale surveys on the infection status of FBT metacercariae in a variety of fish species have not been conducted in Gangwon-do. Therefore, in the present study, we investigated the infection status of zoonotic trematode metacercariae in freshwater fish from various regions of Gangwon-do for a period of 5 years.

MATERIALS AND METHODS

Surveyed areas

The survey was conducted in 13 localities of 9 administrative regions in Gangwon-do, from 2009 to 2013. The surveyed areas (year examined) were as follows: ① Sooipcheon in Yanggu-gun (2009); ② Namdaecheon in Yangyang-gun (2009); ③ Donggang in Yeongwol-gun (2009); ④ Osipcheon in Samcheok-si (2009); ⑤ Gagokcheon in Samcheok-si (2009); ⑥ Hwagang in Cheorwon-gun (2010); ⑦ Hantangang in Cheorwon-gun (2010); ⑧ Hongcheongang in Hongcheon-gun (2010); ⑨ Seomgang in Hoengseong-gun (2011); ⑩ Hantangang in Cheorwon-gun (2012); ⑪ Joyanggang in Jeongseon-gun: (2012); ⑫ Hantangang in Cheorwon-gun (2013); ⑬ Pyeongchanggang in Pyeongchang-gun (2013) (Fig. 1).

Freshwater fish examined

We collected a total of 865 freshwater fish (32 species) in 5 localities, i.e., Sooipcheon (in Yanggu-gun), Namdaecheon (in Yangyang-gun), Donggang (in Yeongwol-gun), Osipcheon (in Samcheok-si), and Gagokcheon (in Samcheok-si), 2 times in a year, June and October 2009. We also collected 547 freshwater fish (29 species) in Hwagang (in Cheorwon-gun), Hantangang (in Cheorwon-gun), and Hongcheongang (in Hongcheon-gun) 2 times in a year, June and October 2010, and in Seomgang (in Hoengseong-gun) in September 2011. A total of 881 freshwater fish (30 species) were collected in Hantangang (in Cheorwon-gun) and Joyanggang (in Jeongseon-gun) 2 times a year in July and October 2012, and in Hantangang (in Cheorwon-gun) and Pyeongchanggang (in Pyeongchang-gun) 2 times a year in June and September 2013. The numbers and species of fish examined were shown in Tables 1, 2, and 3. As for fish collection methods, nettings with a gill net, casting net, and stake net were used in all surveyed areas.

Examination methods

All collected fish were transferred on ice to the laboratory of the Department of Parasitology and Tropical Medicine, Gyeongsang National University School of Medicine, Jinju, Korea. After identification of fish species, fish were individually ground with a mortar with pestle or in a grinder. Each ground fish meat was mixed with artificial gastric juice and the mixture was incubated at 36℃ for 2-3 hr. The digested material was filtered with 1×1 mm of mesh, and washed with 0.85% saline until the supernatant became clear. The sediment was carefully examined under a stereomicroscope. Each species of FBT metacercariae was separately collected by the general feature [5], and they were counted to obtain the infection rates and densities by fish species.

RESULTS

Infection status of Clonorchis sinensis metacercariae

The metacercariae of C. sinensis were detected only in 4 fish species, i.e., Pungtungia herzi, Squalidus japonicus coreanus, Acheilognathus rhombeus, and Ladislabia taczanowskii, collected from Hantangang in Cheorwon-gun. The infection rate of fish was 29.8% (28 out of 94 fish), and a total of 56 metacercariae were harvested (2.0 metacercariae per fish). The infection status of each fish species and each year is revealed in Table 4.

Infection status of Metagonimus spp. metacercariae

The metacercariae of Metagonimus spp. were found in 1,154 (50.3%) fish, and their average number per infected fish was 55.8. Among the positive fish species, Tribolodon hakonensis from Namdaecheon in Yangyang-gun and P. altivelis from Osipcheon in Samcheok-si were most heavily infected. The infection status of each fish species, collection site, and examination year is designated in Tables 5, 6, and 7.

Infection status of Centrocestus armatus metacercariae

The metacercariae of C. armatus were detected in 611 (26.7%) fish, and the average metacercarial burden per infected fish was 1,032. Two species of chubs, Zacco platypus and Zacco temminckii were most highly and most heavily infected in almost all regions surveyed. The infection status by each fish species, collection site, and examination year is shown in Tables 8, 9, and 10.

Infection status of Echinostoma spp. metacercariae

A total of 102 metacercariae of Echinostoma spp. were detected in 24 (15.5%) out of 155 freshwater fish (9 species) collected from 5 localities of Gangwon-do. The infection status by fish species, collection site, and examination year is designated in Table 11.

DISCUSSION

In the present study, C. sinensis metacercariae were detected in 28 fish (4 species, i.e., P. herzi, S. japonicus coreanus, A. rhombeus, and L. taczanowskii) from Hantangang in Cheorwon-gun. In our previous study [10], C. sinensis metacercariae were also found in 2 fish species, P. herzi and S. japonicus coreanus, from Hantangang in Cheorwon-gun, Gangwon-do [10]. According to Kim et al. [9], all fish collected from upper regions of Cheongju-si, Chungcheongbuk-do were negative for C. sinensis metacercariae [9]. It is interesting to note that C. sinensis metacercariae were detected only in fish from limited areas of Hantangang among various regions surveyed in Gangwon-do. First of all, the presence of snail intermediate host, Parafossarulus manchouricus, in this river should be investigated.
Several studies have been performed to investigate on metacercariae of intestinal flukes in fish from Gangwon-do before the early 1990's [12,13,14,15,16,17,19,20,21,22,23]. Especially, the prevalence of M. yokogawai metacercariae was investigated in sweetfish from rivers and streams in the east coast of Gangwon-do [12,13,14,15,16,17,18]. Metacercarial infections of Metagonimus spp. (M. miyatai and M. takahashii) were also examined in freshwater fish from Seomgang, Jucheongang, Pyeongchanggang, Hongcheongang, Donggang, and Osipcheon, in Gangwon-do, and also from the upper reaches of Namhangang [21,22,23]. In addition, epidemiological studies on E. hortense infection were performed in some areas of Gangwon-do [19, 20].
Ahn and Ryang [21] detected 3-87 Metagonimus spp. metacercariae (37.6 in average) in 30 (68.2%) out of 44 Z. platypus from Hongcheongang [21]. In the present study, Metagonimus spp. metacercariae were found in 71 (39.9%) out of 178 fish (12 species), including Z. platypus from Hongcheongang, and their burden per infected fish was 14.3. In case of Z. platypus, all of 20 fish examined were infected with them, and the mean burden was 33.4. Therefore, when we compared the infection status of Metagonimus spp. metacercariae in Z. platypus with that in Ahn and Ryang [21], the prevalence is higher in the present study, although the metacercarial burden is almost similar.
Ahn [22] also detected Metagonimus spp. metacercariae in Z. platypus from Seomgang, Jucheongang, Pyeongchanggang, Hongcheongang, and Donggang in Gangwon-do [22]. The prevalence by the surveyed area was 75.7% (112/148 fish), 77.1% (37/48), 87.5% (28/32), 63.2% (12/19), and 81.5% (22/27), respectively. The metacercarial burden in total 69 Z. platypus ranged 3-1,218 (93.8 in average). In the present study, they were found in all Z. platypus from Seomgang (23 fish), Pyeongchanggang (20), Hongcheongang (20), and Donggang (30), and their burdens were 28.8, 13.1, 33.4, and 31.6 metacercariae per fish, respectively. From the above findings, it is indicated that the prevalence is higher in the present study, and the metacercarial burden is higher in Ahn's study [22]. Like in Ahn's study [22], Metagonimus spp. (M. yokogawai) metacercariae were also found in 2 fish species, P. altivelis (sweetfish) and T. hakonensis (sea rundace), from Osipcheon in Samcheok-si in the present study. All fish (2 species) examined were infected with them in both studies. In the present study, the metacercarial burden was 615 in 29 sweetfish and 82 in 21 sea rundace, whereas the burden was 729 in 5 sweetfish and 68 in 10 sea rundace in Ahn [22]. In Namdaecheon, Yangyang-gun, Metagonimus spp. (M. yokogawai) metacercariae were detected in 27 (90.0%) T. hakonensis in the present study, with their burden being 449 metacercariae per infected fish. By the aforementioned findings, it is confirmed again that 2 fish species, P. altivelis and T. hakonensis, are highly suitable second intermediate hosts of Metagonimus spp. (M. yokogawai) in Gangwon-do.
The infection status of M. yokogawai metacercariae was frequently investigated in sweetfish from Namdaecheon in Yangyang-gun. Song et al. [15] found 116 metacercariae per fish from 9 out of 10 sweetfish examined. Recently, Cho et al. [18] detected 170 metacercariae per fish from all of 20 (100%) fish. In the present study, 1-397 (49 per infected fish) metacercariae were found from 20 (80.0%) out of 25 fish examined. However, no metacercariae were detected in 25 and 22 sweetfish eaxamined by Seo et al. [13] and Ahn et al. [16], respectively. In sweetfish from Osipcheon in Samcheok-si, the infection status of M. yokogawai metacercariae was also surveyed by several workers. Seo et al. [13] reported 100% prevalence and 1,643 metacercariae per fish in 15 sweetfish examined. Ahn [14] and Song et al. [15] detected 382 and 185 metacercariae per fish in 9 and 10 fish examined, respectively. In the present study, 29 sweetfish from Osipcheon in Samcheok-si were infected with 615 metacercariae per fish. Accordingly, the endemicity of M. yokogawai metacercariae was much higher in sweetfish from Osipcheon in Samcheok-si than those from Namdaecheon in Yangyang-gun.
As the second intermediate hosts of Metagonimus spp. (M. miyatai and M. takahashii), approximately 48 species of freshwater fish (37 genera) have been listed in Korea [5]. In the present study, Metagonimus spp. metacercariae were detected in a variety of fish species in Gangwon-do, from 2009 to 2013. Among the positive fish, 16 species, i.e., Acanthorhodeus macropterus (from ⑩, ⑫), Acheilognathus majusculus (⑦, ⑫), Acheilognathus signifier (⑥, ⑩), Chaenogobius urotaenia (④), Hemibarbus mylodon (③, ⑦, ⑩, ⑪, ⑫, ⑬), Ladislabia taczanowskii (④, ⑩, ⑬), Liobagrus andersoni (③, ⑪, ⑫), Microphysogobio longidorsalis (③, ⑥, ⑧, ⑩, ⑪, ⑫, ⑬), Rhynchocypris steidachneri (⑦), Odontobutis platycephala (⑧), Onchorhynchus masou masou (②, ④, ⑤), Opsariichthys uncirostris (⑧, ⑨), Pseudobagrus koreanus (⑩), Pseudopungtungia tenuicorpa (⑪, ⑫), Squalidus japonicus coreanus (⑦), and Tridentiger brevispinis (④), have never been listed as the second intermediate hosts of Metagonimus spp. in Korea [5]. Therefore, 64 fish species (42 genera) in total are included among the second intermediate hosts of Metagonimus spp. in Korea.
To date, 3 Metagonimus species, i.e., M. yokogawai, M. takahashii, and M. miyatai, are known to distribute in Korea [24]. As the second intermediate hosts for M. yokogawai, 3 fish species, i.e., P. altivelis, Tribolodon taczanowskii (=T. hakonensis), and Lateolabrax japonicus, were reported [25,26,27]. As for M. takahashii, 4 fish species, i.e., Carassius auratus, P. altivelis, T. taczanowskii (=T. hakonensis) and L. japonicas, have been known to be the second intermediate hosts [28,29,30,31]. Two species of chubs, Z. platypus and Z. temminckii, were recorded as the second intermediate hosts for M. miyatai [24]. Possible presence of another species of Metagonimus in Korea should be investigated in the near future through recovery of adult worms via experimental infection of animals with these metacercariae.
In the present study, the metacercariae of C. armatus were detected in various fish species from Gangwon-do. Especially in 2 species of chubs, Z. platypus and Z. temminckii, they were highly and heavily infected in almost all regions surveyed. Hong et al. [32] investigated the infection status of C. armatus metacercariae in Z. platypus and Z. temminckii collected from 19 sites in 5 major rivers, Hangang, Geumgang, Yeongsangang, Seomjingang, and Nakdonggang [32]. They could catch Z. temminckii only in 3 regions, Hongcheongang (in Hongcheon-gun), Soyanggang (Inje-gun), and Seocheon (Yanggu-gun), of Gangwon-do. According to them [32], C. armatus metacercariae were detected in 100% (20/20 fish), 35.0% (7/20), and 68.4% (13/19) of Z. temminckii, and their burdens were 65, 2, and 3 metacercariae, respectively. Therefore, it appears that the endemicity of C. armatus is currently much higher than in the past.
Ten species of freshwater fish (8 genera), i.e., Aphyocypris chinensis, C. auratus, C. splendidus, Microphysogobio yaluensis, P. parva, Pseudobagrus fulvidraco, Rhodeus ocellatus ocellatus, R. uyekii, Z. platypus, Z. temminckii, have been listed as the second intermediate hosts for C. armatus in Korea [5]. In the present study, 15 fish species, i.e., Acheilognathus rhombeus (from ⑩), Acheilognathus signifier (⑥), Coreoperca herzi (⑧, ⑪), Gobiobotia brevibarba (⑫), Hemibarbus longirostris (⑧, ⑩, ⑫), Hemibarbus mylodon (⑬), Koreocobitis rotundicaudata (⑪), Liobagrus andersoni (⑪), Microphysogobio longidorsalis (⑩, ⑫, ⑬) , Opsariichthys uncirostris (①, ⑧, ⑨), Orthrias toni (④), Pseudogobio esocinus (⑩, ⑪, ⑬), Pungtungia herzi (⑧), Rhynchocypris oxycephalus (④), and Tribolodon hakonensis (②, ④), are newly recorded as the second intermediate hosts. Accordingly, 24 fish species (20 genera) in total are listed as the second intermediate hosts of C. armatus in Korea.
In the present study, Echinostoma spp. metacercariae (species undetermined) were detected in 9 fish species, i.e., A. signifer (from ⑥), C. herzi (⑩), O. platycephala (⑧), P. esocinus (⑧), P. tenuicorpa (⑬), P. herzi (⑥, ⑧, ⑨, ⑩), R. oxycephalus (⑬), Siniperca scherzeri (⑧), and Z. platypus (⑨). To date, 3 zoonotic Echinostoma species, i.e., E. cinetorchis, E. hortense, and E. revolutum, are distributed in Korea [33]. Among them, E. hortense is the dominant species and has 8 fish intermediate hosts, i.e., Misgurnus anguillicaudatus, Misgurnus mizolepis, R. oxycephalus, Odontobutis interrupta, S. japonicus coreanus, Rhinogobius brunneus, A. macropterus, and Acanthogobius flavimanus, whereas the remaining 2 species take snails as the second intermediate hosts [5]. Moreover, some inland areas, i.e., Eumseong-gun (Chungcheongbuk-do), Yeongwol-gun (Gangwon-do), Cheongsong-gun (Gyeongsangbuk-do), and Geochang-gun (Gyeongsangnam-do), have been reported as the endemic foci of E. hortense infection [20,34,35,36]. Therefore, the metacercariae of Echinostoma spp. detected in the present study are presumed to be E. hortense.
Conclusively, it is reconfirmed that Gangwon-do is a highly endemic area of intestinal flukes, i.e., Metagonimus spp., C. armatus, and Echinostoma spp., infections rather than clonorchiasis. The inhabitants residing in endemic areas should pay attention to infections with these intestinal flukes, and consumption of raw freshwater fish naturally produced should be avoided. In addition, species differentiation in 2 genera, Metagonimus and Echinostoma, should be done in the near future through experimental infection of these metacercariae to animal hosts.
Korea National Institute of Health2011E54007002013E5400200

ACKNOWLEDGMENTS

This study was supported by an anti-communicable diseases control program, 2011E5400700 (Epidemiological survey on the infection status of Clonorchis sinensis in reservoir and intermediate hosts for its management) and 2013E5400200 (Studies on the biological resources of human infecting trematodes and their larval infections in intermediate hosts) of National Institute of Health (NIH), Korea Centers for Disease Control and Prevention (KCDCP). We thank Jung-A Kim and Hee-Joo Kim, Department of Parasitology and Tropical Medicine, Gyeongsang National University School of Medicine, Jinju, Korea, for their help in the examination of fish.

Conflict of interest

The authors have no conflict of interest concerning the work reported in this paper.

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31. Kim DG, Kim TS, Cho SH, Song HJ, Sohn WM. Heterophyid metacercarial infections in brackish water fishes from Jinju-man (Bay), Kyongsangnam-do, Korea. Korean J Parasitol 2006;44:7-13. PMID: 16514276.
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32. Hong SJ, Woo HC, Kim IT. Study on Centrocestus armatus in Korea. I. Infection status of Zacco platypus and Z. temminckii with the metacercariae of C. armatus. Korean J Parasitol 1989;27:41-46.
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33. Chai JY. Echinostomes in humans. In Fried B, Toledo R eds, The biology of echinostomes: From the molecule to the community. New York, USA. Springer. 2009, pp 147-183.

34. Ryang YS. Studies on Echinostoma spp. in the Chungju Reservoir and upper stream of the Namhan River. Korean J Parasitol 1990;28:221-233.
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35. Son WY, Huh S, Lee SU, Woo HC, Hong SJ. Intestinal trematode infections in the villagers in Koje-myon, Kochang-gun, Kyongsangnam-do, Korea. Korean J Parasitol 1994;32:149-155. PMID: 7953239.
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36. Lee SK, Chung NS, Ko IH, Sohn WM, Hong ST, Chai JY, Lee SH. An epidemiological survey of Echinostoma hortense infection in Chongsong-gun, Kyongbuk Province. Korean J Parasitol 1988;26:199-206.
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Fig. 1
The surveyed areas in Gangwon-do, Korea: ① Sooipcheon in Yanggu-gun (2009); ② Namdaecheon in Yangyang-gun (2009); ③ Donggang in Yeongwol-gun (2009); ④ Osipcheon in Samcheok-si (2009); ⑤ Gagokcheon in Samcheok-si (2009); ⑥ Hwagang in Cheorwon-gun (2010); ⑦ Hantangang in Cheorwon-gun (2010); ⑧ Hongcheongang in Hongcheon-gun (2010); ⑨ Seomgang in Hoengseong-gun (2011); ⑩ Hantangang in Cheorwon-gun (2012); ⑪ Joyanggang in Jeongseon-gun: (2012); ⑫ Hantangang in Cheorwon-gun (2013); ⑬ Pyeongchanggang in Pyeongchang-gun (2013).
kjp-52-399-g001.jpg
Table 1.
Freshwater fisha collected from streams and rivers in Gangwon-do, Korea (2009)
Species of fish No. of fish collected from 5 localitiesb
Total
Cypriniforms
Zacco platypus 26 30 30 23 19 128
Zacco temminckii 23 30 30 - 20 103
Coreoleuciscus splendidus 27 - 30 30 8 95
Pungtungia herzi 11 15 16 - 17 59
Tribolodon hakonensis - 30 - 21 - 51
Microphysogobio longidorsalis 25 - 25 - - 50
Rhynchocypris oxycephalus 10 3 - 1 25 39
Hemibarbus longirostris 14 - 16 - - 30
Pseudogobio esocinus 11 - 10 - - 21
Gobiobotia brevibarba - - 18 - - 18
Carassius auratus 14 2 - - - 16
Hemibarbus labeo - - 13 - - 13
Koreocobitis rotundicaudata - - 13 - - 13
Hemibarbus mylodon 2 - 10 - - 12
Acanthorhodeus macropterus - - 10 - - 10
Orthrias toni - - - 8 - 8
Opsariichthys uncirostris 5 - - - - 5
Misgurnus mizolepis - - 5 - - 5
Ladislabia taczanowskii - - - 3 - 3
Gobiobotia macrocephala - - 3 - - 3
Iksookimia koreensis - - 2 - - 2
Cyprinus capio 1 - - - - 1
Pseudobagrus fulvidraco - - 1 - - 1
Osmeriformes
Plecoglossus altivelis - 25 - 29 - 54
Salmoniformes
Onchorhynchus masou masou - 5 - 2 3 10
Siluriformes
Liobagrus andersoni 10 - 3 - - 13
Silurus asotus - - 1 - - 1
Perciformes
Coreoperca herzi 17 10 15 - - 42
Chaenogobius urotaenia - - - 19 8 27
Tridentiger brevispinis - - - 15 9 24
Rhinogobius giurinus - - - 4 - 4
Acanthogobius pflaumi - 4 - - - 4
Total 196 154 251 155 109 865

a Total 865 freshwater fish of 32 species were examined.

b ① Sooipcheon in Yanggu-gun, ② Namdaecheon in Yangyang-gun, ③ Donggang in Yeongwol-gun, ④ Osipcheon in Samcheok-si, ⑤ Gagokcheon in Samcheok-si.

Table 2.
Freshwater fisha collected from rivers in Gangwon-do, Korea (2010-2011)
Species of fish No. of fish collected from 4 localitiesb
Total
Cypriniforms
Zacco platypus 3 30 20 23 76
Zacco temminckii 10 30 16 5 61
Pungtungia herzi 13 7 25 14 59
Hemibarbus longirostris 12 3 20 20 55
Pseudogobio esocinus 3 8 23 13 47
Microphysogobio longidorsalis 8 - 20 2 30
Coreoleuciscus splendidus 2 - 18 6 26
Carassius auratus 5 3 2 15 25
Rhynchocypris oxycephalus - - - 15 15
Acheilognathus majusculus - 6 6 - 12
Gobiobotia brevibarba - - - 10 10
Rhynchocypris steidachneri - 3 - 6 9
Opsariichthys uncirostris - - 2 5 7
Acheilognathus lanceolatus 2 1 - 3 6
Pseudobagrus koreanus - - - 6 6
Koreocobitis rotundicaudata - - - 6 6
Acheilognathus rhombeus - 5 - - 5
Acheilognathus signifer 4 - - - 4
Hemibarbus mylodon - 3 - - 3
Squalidus japonicus coreanus - 2 - - 2
Hemibarbus labeo - - 1 - 1
Iksookimia koreensis - - - 1 1
Sarcocheilichthys nigripinnis - 1 - - 1
Microphysogobio jeoi - 1 - - 1
Siluriformes
Liobagrus andersoni - - - 3 3
Perciformes
Coreoperca herzi 7 5 20 15 47
Siniperca scherzeri - - 11 - 11
Odontobutis platycephala - - 2 1 3
Scorpaeniformes
Cottus koreanus - - - 15 15
Total 69 108 186 184 547

a Total 547 freshwater fishes in 29 species examined.

b ⑥ Hwagang in Cheorwon-gun (2010), ⑦ Hantangang in Cheorwon-gun (2010), ⑧ Hongcheongang in Hongcheon-gun (2010), ⑨ Seomgang in Hoengseong-gun (2011).

Table 3.
Freshwater fisha collected from rivers in Gangwon-do, Korea (2012-2013)
Species of fish No. of fish collected from 4 localitiesb
Total
Cypriniforms
Zacco temminckii 30 39 22 34 125
Pungtungia herzi 44 24 20 35 123
Microphysogobio longidorsalis 30 24 22 22 98
Zacco platypus 29 20 16 20 85
Pseudogobio esocinus 17 1 40 21 79
Coreoleuciscus splendidus 11 25 14 17 67
Hemibarbus longirostris 2 - 12 17 31
Pseudobagrus koreanus 6 15 7 - 28
Koreocobitis rotundicaudata 2 7 - 15 24
Hemibarbus mylodon 12 1 4 5 22
Acheilognathus rhombeus 20 - - - 20
Gobiobotia brevibarba - 1 4 8 13
Acheilognathus signifer 11 - 1 - 12
Rhynchocypris oxycephalus - - - 10 10
Hemibarbus labeo 8 1 1 - 10
Acanthorhodeus macropterus 5 - 2 - 7
Pseudopungtungia tenuicorpa - 2 - 5 7
Carassius auratus - - 6 - 6
Ladislabia taczanowskii 1 - - 4 5
Iksookimia koreensis - 1 4 - 5
Acheilognathus majusculus - - 4 - 4
Misgurunus anguillicaudatus - - 4 - 4
Pseudobagrus fulvidraco - - 2 - 2
Rhodeus ocellatus - - 2 - 2
Sarcocheilichthys variegatus - - 1 - 1
Siluriformes
Liobagrus andersoni - 18 4 15 37
Liobagrus mediadoposalis 9 - - - 9
Liobagrus obesus 3 - - - 3
Perciformes
Coreoperca herzi 15 17 5 2 39
Siniperca scherzeri - - 3 - 3
Total 255 196 200 230 881

a Total 881 freshwater fishes in 30 species examined.

b ⑩ Hantangang in Cheorwon-gun (2012), ⑪ Joyanggang in Jeongseon-gun (2012), ⑫ Hantangang in Cheorwon-gun (2013), ⑬ Pyeongchanggang in Pyeongchang-gun (2013).

Table 4.
Infection status of Clonorchis sinensis metacercariae in fish from rivers in Gangwon-do, Korea (2010-2013)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
⑦ Hantangang in Cheorwon-gun (2010)a
  Pungtungia herzi 7 6 (85.7) 19 1-6 3.2
  Squaiidus japonicus coreanus 2 2 (100) 4 - 2.0
  Subtotal 9 8 (88.9) 23 1-6 2.9
⑩ Hantangang in Cheorwon-gun (2012)
  Pungtungia herzi 44 16 (36.4) 27 1-3 1.7
  Acheiiognathus rhombeus 20 2 (10.0) 2 - 1.0
  Ladisiabia taczanowskii 1 1 (100.0) 2 - 2.0
  Subtotal 65 19 (29.2) 31 1-3 1.6
⑫ Hantangang in Cheorwon-gun (2013)
  Pungtungia herzi 20 1 (5.0) 2 - 2.0
Total 94 28 (29.8) 56 1-6 2.0

a Previously reported by Cho et al., 2011.

Table 5.
Infection status of Metagonimus spp. metacercariae in fish from streams and rivers in Gangwon-do, Korea (2009)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
① Sooipcheon in Yanggu-gun
  Zacco platypus 26 17 (65.4) 53 1-16 3.1
  Zacco temminckii 23 18 (78.3) 85 1-27 4.7
  Pseudogobio esocinus 11 2 (18.2) 24 11-13 12.0
  Liobagrus mediadiposalis 10 2 (20) 2 - 1.0
  Hemibarbus longirostris 8 1 (12.5) 1 - 1.0
  Subtotal 78 40 (51.3) 165 1-27 4.1
② Namdaecheon in Yangyang-gun
  Tribolodon hakonensis 30 27 (90.0) 12,134 2-2,250 449.4
  Zacco platypus 30 25 (83.3) 223 1-58 8.9
  Zacco temminckii 30 9 (30.0) 66 1-47 7.3
  Plecoglossus altivelis 25 20 (80.0) 979 1-397 49.0
  Pungtungia herzi 15 10 (66.7) 33 1-9 3.3
  Coreoperca herzi 10 1 (10) 1 - 1.0
  Onchorhynchus masou masou 5 4 (80) 95 11-37 23.8
  Subtotal 145 96 (66.2) 13,531 1-2,250 140.9
③ Donggang in Yeongwol-gun
  Zacco platypus 30 30 (100) 949 2-148 31.6
  Zacco temminckii 30 30 (100) 477 2-51 15.9
  Coreoleuciscus splendidus 30 27 (90.0) 238 1-28 8.8
  Microphysogobio longidorsalis 25 11 (44.0) 93 1-27 8.5
  Hemibarbus longirostris 16 15 (93.8) 727 1-260 48.5
  Pungtungia herzi 16 9 (56.3) 19 1-10 2.1
  Hemibarbus labeo 13 12 (92.3) 201 1-70 16.8
  Gobiobotia brevibarba 11 11 (100) 682 6-112 62.0
  Pseudogobio esocinus 10 10 (100) 1,224 10-387 122.4
  Hemibarbus mylodon 10 5 (50) 15 1-7 3.0
  Coreoperca herzi 5 1 (20) 1 - 1.0
  Liobagrus andersoni 3 2 (66.7) 5 1-4 2.5
  Subtotal 199 163 (81.9) 4,631 1-387 28.4
④ Osipcheon in Samcheok-si
  Plecoglossus altivelis 29 29 (100) 17,820 6-3,380 614.5
  Zacco platypus 23 23 (100) 303 1-75 13.2
  Tribolodon hakonensis 21 21 (100) 1,730 1-275 82.4
  Chaenogobius urotaenia 10 1 (10.0) 1 - 1.0
  Ladislabia taczanowskii 3 3 (100) 16 1-12 5.3
  Onchorhynchus masou masou 2 2 (100) 28 3-25 14.0
  Rhynchocypris oxycephalus 1 1 (100) 17 - 17.0
  Subtotal 89 80 (89.9) 19,915 1-3,380 248.9
⑤ Gagokcheon in Samcheok-si
  Zacco platypus 19 6 (31.6) 22 1-7 3.7
  Pungtungia herzi 15 7 (46.7) 10 1-2 1.4
  Zacco temminckii 15 2 (13.3) 5 1-4 2.5
  Rhynchocypris oxycephalus 15 2 (13.3) 4 1-3 2.0
  Tridentiger brevispinis 9 1 (11.1) 8 - 8.0
  Onchorhynchus masou masou 2 2 (100) 68 20-48 34.0
  Subtotal 75 20 (26.7) 117 1-48 5.9
Total 586 399 (68.1) 38,359 1-3,380 96.1
Table 6.
Infection status of Metagonimus spp. metacercariae in fish from rivers in Gangwon-do, Korea (2010-2011)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
⑥ Hwagang in Cheorwon-gun (2010)
  Zacco temminckii 10 7 (70.0) 103 1-47 14.7
  Pungtungia herzi 13 3 (23.1) 5 1-3 1.7
  Hemibarbus longirostris 12 12 (100) 1,267 3-596 105.6
  Microphysogobio longidorsalis 8 1 (12.5) 1 - 1.0
  Acheilognathus signifier 4 4 (100) 106 18-50 26.5
  Zacco platypus 3 3 (100) 82 8-46 27.3
  Pseudogobio esocinus 3 3 (100) 2,078 78-1,680 692.7
  Acheilognathus lanceolatus 2 2 (100) 2 - 1.0
  Coreoleuciscus splendidus 2 2 (100) 11 1-10 5.5
  Subtotal 57 37 (64.9) 3,655 1-1,680 98.8
⑦ Hantangang in Cheorwon-gun (2010)
  Zacco temminckii 30 29 (96.7) 342 1-56 11.8
  Zacco platypus 30 30 (100) 1,013 2-184 33.8
  Pseudogobio esocinus 8 8 (100) 383 4-125 47.9
  Acheilognathus majusculus 6 6 (100) 46 3-10 7.7
  Acheilognathus rhombeus 5 5 (100) 33 1-9 6.6
  Hemibarbus mylodon 3 2 (66.7) 13 5-8 6.5
  Hemibarbus longirostris 3 3 (100) 160 5-85 53.3
  Rhynchocypris steidachneri 3 2 (66.7) 68 32-36 34.0
  Squalidus japonicus coreanus 2 1 (50.0) 3 - 3.0
  Subtotal 90 86 (95.6) 2,061 1-184 24.0
⑧ Hongcheongang in Hongcheon-gun (2010)
  Pungtungia herzi 25 1 (4.0) 1 - 1.0
  Hemibarbus longirostris 20 7 (35.0) 16 1-4 2.3
  Pseudogobio esocinus 23 16 (69.6) 92 1-19 5.8
  Coreoperca herzi 20 1 (5.0) 1 - 1.0
  Coreoleuciscus splendidus 18 4 (22.2) 6 1-2 1.5
  Zacco platypus 20 20 (100) 667 7-123 33.4
  Zacco temminckii 16 13 (81.3) 95 1-22 7.3
  Microphysogobio longidorsalis 20 1 (5.0) 4 - 1.0
  Siniperca scherzeri 11 4 (36.4) 5 - 1.0
  Odontobutis platycephala 2 1 (50.0) 4 - 1.0
  Opsariichthys uncirostris 2 2 (100) 22 8-14 11.0
  Hemibarbus labeo 1 1 (100) 107 - 107.0
  Subtotal 178 71 (39.9) 1,013 -1-123 14.3
⑨ Seomgang in Hoengseong-gun (2011)
  Zacco platypus 23 23 (100) 662 3-122 28.8
  Hemibarbus longirostris 20 19 (95.0) 1,316 1-214 69.3
  Pungtungia herzi 14 2 (14.3) 2 - 1.0
  Pseudogobio esocinus 13 12 (92.3) 102 1-19 8.5
  Gobiobotia brevibarba 10 6 (60.0) 23 1-12 3.8
  Zacco temminckii 5 1 (20.0) 4 - 4.0
  Opsariichthys uncirostris 5 5 (100) 116 5-75 23.2
  Acheilognathus lanceolatus 3 1 (33.3) 3 - 3.0
  Subtotal 93 69 (74.2) 2,228 1-214 32.3
Total 418 263 (62.9) 8,957 1-1,680 34.1
Table 7.
Infection status of Metagonimus spp. metacercariae in fish from rivers in Gangwon-do, Korea (2012-2013)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
⑩ Hantangang in Cheorwon-gun (2012)
  Pungtungia herzi 44 6 (13.6) 7 1-2 1.2
  Zacco temminckii 30 28 (93.3) 834 1-135 29.8
  Zacco platypus 29 29 (100.0) 907 3-115 31.3
  Acheiiognathus rhombeus 20 17 (85.0) 474 1-95 27.9
  Pseudogobio esocinus 17 17 (100.0) 2,389 10-462 140.5
  Hemibarbus mylodon 12 12 (100.0) 601 4-242 50.1
  Acheilognathus signifer 11 8 (72.7) 30 1-7 3.8
  Coreoperca herzi 11 1 (9.1) 2 - 2.0
  Microphysogobio longidorsalis 10 1 (10.0) 1 - 1.0
  Hemibarbus labeo 8 6 (75.0) 53 1-22 8.8
  Pseudobagrus koreanus 6 2 P3.3) 12 2-10 6.0
  Acanthorhodeus macropterus 5 3 (60.0) 8 1-4 2.7
  Hemibarbus longirostris 2 2 (100.0) 151 36-115 75.5
  Ladislabia taczanowskii 1 1 (100.0) 1 - 1.0
  Subtotal 206 133 (64.6) 5,470 1-462 41.1
⑪ Joyanggang in Jeongseon-gun (2012)
  Zacco temminckii 39 38 (97.4) 4,939 10-403 130.0
  Coreoleuciscus splendidus 25 25 (100.0) 424 1-71 17.0
  Microphysogobio longidorsalis 24 20 (83.3) 185 1-42 9.3
  Pungtungia herzi 24 10 (41.7) 23 1-9 2.3
  Zacco platypus 20 20 (100.0) 1,333 5-169 66.7
  Liobagrus andersoni 8 3 (37.5) 5 1-3 1.7
  Pseudopungtungia tenuicorpa 2 2 (100.0) 2 - 1.0
  Coreoperca herzi 2 1 (50.0) 1 - 1.0
  Hemibarbus mylodon 1 1 (100.0) 1 - 2.0
  Hemibarbus labeo 1 1 (100.0) 320 - 320.0
  Gobiobotia brevibarba 1 1 (100.0) 95 - 95.5
  Subtotal 147 122 (83.0) 7,329 1-403 60.1
⑫ Hantangang in Cheorwon-gun (2013)
  Pseudogobio esocinus 40 38 (95.0) 1,473 1-486 38.8
  Zacco temminckii 22 18 (81.8) 199 2-32 11.1
  Microphysogobio longidorsalis 22 1 (4.5) 1 - 1.0
  Zacco platypus 16 16 (100) 559 1-67 34.9
  Hemibarbus longirostris 10.1
  Carassius auratus 10.8
  Gobiobotia brevibarba 4 4 (100) 97 15-29 24.3
  Hemibarbus mylodon 4 3 (75.0) 224 43-134 74.7
  Liobagrus andersoni 4 2 (50.0) 3 1-2 1.5
  Acheilognathus majuscules 4 2 (50.0) 2 - 1.0
  Rhodeus ocellatus 2 2 (100) 17 7-10 8.5
  Acanthorhodeus macropterus 2 2 (100) 102 38-64 51.0
  Sarcocheilichthys variegatus 1 1 (100) 1 - 1.0
  Hemibarbus labeo 1 1 (100) 153 - 153.0
  Subtotal 140 105 (75.0) 2,985 1-486 28.4
⑬ Pyeongchanggang in Pyeongchang-gun (2013)
  Pungtungia herzi 35 2 (5.7) 5 1-4 2.5
  Zacco temminckii 34 32 (94.1) 325 1-29 10.2
  Pseudogobio esocinus 21 19 (90.5) 148 1-30 7.8
  Zacco platypus 20 20 (100) 261 1-53 13.1
  Coreoieuciscus splendidus 17 15 (88.2) 213 1-63 14.2
  Hemibarbus longirostris 17 16 (94.1) 269 1-145 16.8
  Rhynchocypris oxycephalus 10 6 (60.0) 9 1-3 1.5
  Gobiobotia brevibarba 8 7 (87.5) 32 1-9 4.6
  Pseudopungtungia tenuicorpa 5 1 (20.0) 1 - 1.0
  Hemibarbus mylodon 5 1 (20.0) 1 - 1.0
  Ladislabia taczanowskii 4 2 (50.0) 5 2-3 2.5
  Subtotal 198 132 (66.7) 1,325 1-145 10.0
Total 691 492 (71.2) 17,109 1-486 34.8
Table 8.
Infection status of Centrocestus armatus metacercariae in fish from streams and rivers in Gangwon-do, Korea (2009)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
① Sooipcheon in Yanggu-gun
  Zacco temminckii 23 22 (95.7) 7,231 77-1,035 329
  Zacco platypus 26 25 (96.2) 3,937 1-887 158
  Opsariichthys uncirostris 5 1 (20.0) 3 - 3.0
  Subtotal 54 48 (88.9) 11,171 1-1,035 233
② Namdaecheon in Yangyang-gun
  Zacco temminckii 30 21 (70.0) 4,772 1-3,687 227
  Zacco platypus 30 25 (83.3) 3,533 2-809 141
  Tribolodon hakonensis 30 2 (6.7) 2 - 1.0
  Subtotal 90 48 (53.3) 8,307 1-3,687 173
③ Donggang in Yeongwol-gun
  Zacco temminckii 30 30 (100) 6,178 31-663 206
  Zacco platypus 30 30 (100) 10,699 54-1,006 357
  Subtotal 60 60 (100) 16,877 31-1,006 281
④ Osipcheon in Samcheok-si
  Zacco platypus 23 22 (95.7) 2,973 10-576 135
  Tribolodon hakonensis 21 5 (23.8) 16 1-10 3.2
  Rhynchocypris oxycephalus 1 1 (100) 13 - 13.0
  Orthrias toni 8 1 (12.5) 1 - 1.0
  Subtotal 53 29 (54.7) 3,003 1-576 104
⑤ Gagokcheon in Samcheok-si
  Zacco temminckii 15 12 (80.0) 2,421 1-1,518 202
  Zacco platypus 19 18 (94.7) 8,449 1-1,880 469
  Subtotal 34 30 (88.2) 10,870 1-1,880 362
Total 291 215 (73.9) 50,228 1-3,687 234
Table 9.
Infection status of Centrocestus armatus metacercariae in fish from rivers in Gangwon-do, Korea (2010-2011)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
⑥ Hwagang in Cheorwon-gun (2010)
  Zacco temminckii 10 10 (100) 2,208 108-406 221
  Zacco platypus 3 3 (100) 1,149 154-774 383
  Acheilognathus signifer 4 1 (25) 1 - 1.0
  Subtotal 17 14 (82.4) 3,358 1-774 240
⑦ Hantangang in Cheorwon-gun (2010)
  Zacco temminckii 30 30 (100) 15,637 24-2,630 521
  Zacco platypus 30 30 (100) 14,650 8-4,355 488
  Carassius auratus 3 1 (33.3) 1 - 1.0
  Subtotal 63 61 (96.8) 30,288 1-2,630 497
⑧ Hongcheongang in Hongcheon-gun (2010)
  Zacco temminckii 16 16(100) 53,486 42-8,041 3,343
  Zacco platypus 20 20 (100) 123,150 780-13,650 6,158
  Opsariichthys uncirostris 2 2(100) 3,750 1,460-2,290 1,875
  Pungtungia herzi 25 10 (40) 56 1-24 5.6
  Hemibarbus longirostris 20 3 (15) 4 1-2 1.3
  Coreoperca herzi 20 2 (10) 7 1-6 3.5
  Coreoleuciscus splendidus 18 3 (16.7) 3 - 1.0
  Subtotal 121 56 (46.3) 180,456 1-13,650 3,222
⑨ Seomgang in Hoengseong-gun (2011)
  Zacco temminckii 5 3 (60.0) 1,755 2-1,385 585
  Zacco platypus 23 23 (100) 41,599 21-8,720 1,809
  Opsariichthys uncirostris 5 2 (40.0) 158 60-98 79
  Subtotal 33 28 (84.8) 43,512 2-8,720 1,554
Total 234 159 (68.0) 257,614 1-13,650 1,620
Table 10.
Infection status of Centrocestus armatus metacercariae in fish from rivers in Gangwon-do, Korea (2010-2012)
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
⑩ Hantangang in Cheorwon-gun (2012)
  Zacco temminckii 30 30 (100) 17,982 28-2,340 599
  Zacco platypus 29 29 (100) 28,640 23-6,620 988
  Pseudogobio esocinus 17 2 (11.8) 3 1-2 1.5
  Microphysogobio longidorsalis 20 1 (5.0) 1 - 1.0
  Acheilognathus rhombeus 10 6 (60.0) 45 3-12 7.5
  Hemibarbus longirostris 2 1 (50.0) 4 - 4.0
  Subtotal 108 69 (63.9) 46,675 1-6,620 676
⑪ Joyanggang in Jeongseon-gun (2012)
  Zacco temminckii 39 39 (100) 40,537 163-3,205 1,039
  Zacco platypus 20 20 (100) 6,361 53-978 318
  Liobagrus andersoni 8 2 (25.0) 2 - 1.0
  Coreoperca herzi 2 1 (50.0) 2 - 2.0
  Pseudogobio esocinus 1 1 (100) 10 - 10.0
  Koreocobitis rotundicaudata 1 1 (100) 5 - 5.0
  Subtotal 71 64 (90.1) 46,917 2-3,205 733
⑫ Hantangang in Cheorwon-gun (2013)
  Zacco temminckii 22 22 (100) 14,315 112-2,760 651
  Zacco platypus 16 16 (100) 29,603 370-3,735 1,850
  Microphysogobio longidorsalis 22 1 (4.5) 2 - 2.0
  Hemibarbus longirostris 12 1 (8.3) 2 - 2.0
  Gobiobotia brevibarba 4 2 (50.0) 5 1-4 2.5
  Rhodeus ocellatus 2 2 (100) 15 3-12 7.5
  Subtotal 78 44 (56.4) 43,942 1-3,735 999
⑬ Pyeongchanggang in Pyeongchang-gun (2013)
  Zacco temminckii 34 34 (100) 148,770 96-11,470 4,376
  Zacco platypus 20 20 (100) 36,420 240-8,080 1,821
  Pseudogobio esocinus 21 1 (4.8) 2 - 2.0
  Microphysogobio longidorsalis 22 3 (13.6) 3 - 1.0
  Coreoleuciscus splendidus 17 1 (5.9) 2 - 2.0
  Hemibarbus mylodon 5 1 (20.0) 1 - 1.0
  Subtotal 119 60 (50.4) 185,198 1-11,470 3,087
Total 376 237 (63.0) 322,732 1-11,470 1,362
Table 11.
Infection status of Echinostoma spp. metacercariae in fish from streams and rivers in Gangwon-do, Korea
Locality (year) and fish sp. examined No. of fish examined No. (%) of fish infected No. of metacercariae detected
Total Range Average
⑥ Hwagang in Cheorwon-gun (2010)
  Pungtungia herzi 13 2 (15.4) 5 1-4 2.5
  Acheiiognathus signifer 4 1 (25.0) 1 - 1.0
  Subtotal 17 3 (17.7) 6 1-4 2.0
⑧ Hongcheongang in Hongcheon-gun (2010)
  Pungtungia herzi 25 4 (16.0) 4 - 1.0
  Pseudogobio esocinus 23 1 (4.3) 1 - 1.0
  Siniperca scherzeri 11 1 (9.1) 1 - 1.0
  Odontobutis platycephala 2 1 (50.0) 4 - 4.0
  Subtotal 61 7 (11.5) 10 1-4 1.4
⑨ Seomgang in Hoengseong-gun (2011)
  Zacco platypus 23 8 (34.8) 75 3-18 9.4
  Pungtungia herzi 14 2 (14.3) 5 2-3 2.5
  Subtotal 37 10 (27.0) 80 2-18 8.0
⑩ Hantangang in Cheorwon-gun (2012)
  Pungtungia herzi 14 1 (7.1) 1 - 1.0
  Coreoperca herzi 11 1 (9.1) 1 - 1.0
  Subtotal 25 2 (8.0) 2 - 1.0
⑬ Pyeongchanggang in Pyeongchang-gun (2013)
  Rhynchocypris oxycephalus 10 1 (10.0) 3 - 3.0
  Pseudopungtungia tenuicorpa 5 1 (20.0) 1 - 1.0
  Subtotal 15 2 (13.3) 4 1-3 2.0
Total 155 24 (15.5) 102 1-18 4.3
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