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Ozobranchus jantseanus (Clitellata: Ozobranchidae) from Reeve’s Turtle, Mauremys reevesii: New Annelid Fauna in Korea

Kyo Soung Koo1orcid, Kayoung Yun2, Yikweon Jang2,*orcid
The Korean Journal of Parasitology 2022;60(3):213-215.
Published online: June 30, 2022

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*Corresponding author (jangy@ewha.ac.kr)
• Received: February 5, 2022   • Revised: May 29, 2022   • Accepted: June 2, 2022

© 2022, Korean Society for Parasitology and Tropical Medicine

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  • Turtle leeches have not been recorded in Korea, although they occur in geographically adjacent countries including China and Japan. This study describes a turtle leech, Ozobranchus jantseanus (Clitellata: Ozobranchidae), found from Reeve’s turtle (Mauremys reevesii) in Korea. Of the 143 Reeve’s turtles collected from the freshwater reservoir in Jinju City, Gyeongsangnam-do, Korea, 95 unidentified leeches were found in 8 (5.6%) individuals. The leeches had 22 somites with 11 pairs of externally exposed branchiae, body-sized posterior suckers, and spines on the dorsal surface. We identified these leeches as Ozobranchus jantseanus Oka, 1912 (Clitellata: Ozobranchidae). This species of turtle leeches found in Korea may fill the gap in the biodiversity of East Asian annulus.
  • Key words: Ozobranchus jantseanus, leech, freshwater turtle, Korea
A total of 7 species of turtle leeches in the genus Ozobranchus are distributed globally [1]. The first recorded O. branchiatus (Menzies 1791) and O. margoi (Apáthy, 1890) are representative turtle leeches that parasitize sea turtles. In addition, 4 species of leeches in freshwater turtles (O. jantseanus Oka, 1912; O. shipleyi Harding, 1909; O. papillatus Kaburaki, 1921; and O. polybranchus Sanjeeva Raj, 1951) and 1 species in crocodiles (Ozobranchus quatrefagesi) are recorded [2,3]. There are 4 species of turtle leeches found in Asia, which include O. jantseanus (hosts on freshwater turtles in East Asia), O. shipleyi (hosts on Nicoria trijuga, found in Sri Lanka, India, and Pakistan), O. papillatus (hosts on Kachua tetum in India), and O. polybranchus (hosts on Pelochelys bibroni in South and Southeast Asia) [3,4]. O. jantseanus parasitizes Mauremys reevesii (Gray, 1831), a freshwater turtle that thrives mainly in East Asia, including China, Korea, and Japan. Although no eggs of O. jantseanus were found, adult leeches have been recorded in 2 species of turtles, M. japonica (Temminck & Schlegel, 1838) and Trachemys scripta elegans (Wied, 1839) in Japan [5,6]. Since M. reevesii is a freshwater turtle native to Korea, geographically located between China and Japan, the discovery of O. jantseanus in Korea has been expected for a long time. In this study, we first report a species of turtle leech, O. jantseanus Oka, 1912 (Clitellata; Ozobranchidae) in Korea and describe their morphological characteristics.
From May 1 to June 31, 2021, a total of 143 M. reevesii were collected from Geumho Reservoir (35°12′35.14″N, 128°09′08. 76″E, a.s.l, 37m) located in Jinju City, Gyeongsangnam-do, Korea. Unidentified leeches and eggs were found in 8 turtles (5.6%). We found 95 leeches with an average of 11.9±3.7 (mean±SD; 2–34 in range) per turtle (Fig. 1). Leeches were parasitic on the soft tissues between the carapace and the plastron of the turtle’s armpits and groin (Fig. 1). We investigated the morphological characteristics of leeches, with the possibility of identifying species of the genus Ozobranchus [7]. The leeches were stored in 70% ethanol and then gradually relaxed with distilled water to observe external traits. A large sucker was exposed on the opposite side of the leech’s head, which was hidden in a small sucker (Fig. 2). We examined the external traits of leeches larger than 1 mm with a dissecting microscope (Model 41, American Optical Corp., Buffalo, New York, USA). We found that the average number of somites was 21.9±0.6 (n=60; range, 18–22). The number of branched-branchiae exposed on both sides of the body was 11 pairs in 58 individuals, but 10 pairs in one individual (Fig. 3A). There were spines along the somites on the back of the leeches (Fig. 3B). Leech eggs were found in a 5 turtles, which were anchored on the host’s carapace in the form of a colony (Fig. 1). No leech eggs were found in the plastron. The samples are deposited in the laboratory of Ewha Animal Behavior in Ewha Womans University in Seoul, Korea.
The leeches were determined to be O. jantseanus in the genus Ozobranchus based on the following characters: 1) distribution in East Asia, 2) parasitism in freshwater turtles, 3) 11 pairs of external branched-branchiae, and 4) 22 somites on the body [1,3,8,9].
Leeches in the genus Ozobranchus mainly parasitize turtles, and O. jantseanus is specific to M. reevesii [1,10]. Since these species-specific parasites coexist interdependently over a long period of time, these issues may be an important topic for studying host-parasite coevolution [11,12].
O. jantseanus was found with M. reevesii in 1916 in Kyoto, Japan [10]. Since M. reevesii turtle is a species introduced to Japan, O. jantseanus might be introduced along with the turtle [13,14]. O. jantseanus has only been found in turtles living in China, but not in those in Korea, therefore, it is not known how it was introduced into Japan [8]. This study confirmed that O. jantseanus thrives in Korea. In the future, it will be possible to study the migration and spread of M. reevesii between continents and islands through genetic phylogenetic studies.
Although M. reevesii is an exotic species in Japan, it is quite widespread. Interestingly, the parasite O. jantseanus shows the same distribution pattern as that of the turtle host [6]. Since M. reevesii is distributed throughout Korea, O. jantseanus is expected to be found nationwide along with the host [15]. There are several interesting issues about the relationships between turtles and turtle leeches. The phylogeographic relationship should be first studied separately in the host and the parasite species, after which the evolutionary relationship between the host and parasite species should be examined. These studies will shed light on the coevolution of the turtles and turtle leeches.
In conclusion, our discovery is important for filling the turtle leech biodiversity gap in East Asia beyond documenting new species in Korea. It will further enable the subsequent investigations of the genus Ozobranchus, which is rarely studied despite its global distribution.

The authors declare no conflict of interest related to this study.

We thank the members of the Animal Behavior Lab at Ewha Womans University for their assistance in this study, especially Yoon-Ju Kim. This work was supported by Korea Environmental Industry & Technology Institute, grant number (KEITI 2021002270001).
Fig. 1
A leech and eggs attached on the carapace of Mauremys reevesii.
kjp-60-3-213f1.jpg
Fig. 2
Dorsal (A) and ventral (B) view of a leech under a dissecting microscope.
kjp-60-3-213f2.jpg
Fig. 3
(A) The body separated as somites and many branched-branchiae on the body side. (B) The spines are arranged horizontally on the dorsal surface.
kjp-60-3-213f3.jpg
  • 1. Sawyer RT. Leech biology and behaviour. Clarendon Press; Oxford England. 1986.
  • 2. Poirier J, de Rochebrune AT. Sur un type nouveau de la classe des Hirudinées. C R Hebd Séances Acad Sci 1884;98:1597-1600.
  • 3. Sanjeeva Raj PJ. A synopsis of the species of the genus Ozobranchus (de Quatrefages) 1852 (Hirudinea—Annelida). J Bombay Nat Hist Soc 1954;52:473-480.
  • 4. Richardson LR. The family Ozobranchidae redefined, and a novel ozobranchiform leech from Murray River turtles (class Hirudinoidea: order Rhynchobdelliformes). Proc Linn Soc NSW USA 1969;94:61-80.
  • 5. Yamauchi T, Nishibori T, Suzuki D. First report of Ozobranchus jantseanus (Hirudinida: Ozobranchidae) parasitizing the exotic red-eared slider Trachemys scripta elegans in Japan. Comp parasitol 2012;79:348-349. https://doi.org/10.1654/4553.1
  • 6. Nakano T, Nakamura R, Ohtsuka S, Suzuki T, Suzuki D. Low genetic diversity in Ozobranchus jantseanus (Hirudinida: Ozobranchidae) in Japan: Possibility of introduction with their host turtles. Parasitol int 2017;66:798-801. https://doi.org/10.1016/j.parint.2017.08.006
  • 7. Fauna Sinica Yang T. Annelida Hirudinea. Science Press; Beijing, China. 1996.
  • 8. Oka A. Key to Japanese leeches. Dobutsugaku Zasshi 1910;22:56-64.
  • 9. Inakuma M. An experiment on Ozobranchus jantseanus Oka. Dobutsugaku Zasshi 1922;34:13-18.
  • 10. Yamauchi T, Suzuki D. Geographical distribution of Ozobranchus jantseanus (Annelida: Hirudinida: Ozobranchidae). Med Entomol Zool 2008;59:345-349.
  • 11. Dybdahl MF, Lively CM. Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 1998;52:1057-1066. https://doi.org/10.1111/j.1558-5646.1998.tb01833.x
  • 12. Koella JC, Agnew P, Michalakis Y. Coevolutionary interactions between host life histories and parasite life cycles. Parasitology 1998;116:suppl. 47-55. https://doi.org/10.1017/s0031182000084936
  • 13. Nishimura S. Guide to Seashore Animals of Japan with Color Pictures and Keys. I Hoikusha; Osaka, Japan. 1992, pp 376-379.
  • 14. Suzuki D, Ota H, Oh HS, Hikida T. Origin of Japanese populations of Reeves’ pond turtle, Mauremys reevesii (Reptilia: Geoemydidae), as inferred by a molecular approach. Chelonian Conserv Biol 2011;10:237-249.
  • 15. Do MS, Lee JW, Jang HJ, Kim DI, Park J, Yoo JC. Spatial distribution patterns and prediction of hotspot area for endangered herpetofauna species in Korea. Korean J Environ Ecol 2017;31:381-396. (in Korean). https://doi.org/10.13047/KJEE.2017.31.4.381

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Ozobranchus jantseanus (Clitellata: Ozobranchidae) from Reeve’s Turtle, Mauremys reevesii: New Annelid Fauna in Korea
Korean J Parasitol. 2022;60(3):213-215.   Published online June 30, 2022
DOI: https://doi.org/10.3347/kjp.2022.60.3.213
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Ozobranchus jantseanus (Clitellata: Ozobranchidae) from Reeve’s Turtle, Mauremys reevesii: New Annelid Fauna in Korea
Korean J Parasitol. 2022;60(3):213-215.   Published online June 30, 2022
DOI: https://doi.org/10.3347/kjp.2022.60.3.213
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Ozobranchus jantseanus (Clitellata: Ozobranchidae) from Reeve’s Turtle, Mauremys reevesii: New Annelid Fauna in Korea
Image Image Image
Fig. 1 A leech and eggs attached on the carapace of Mauremys reevesii.
Fig. 2 Dorsal (A) and ventral (B) view of a leech under a dissecting microscope.
Fig. 3 (A) The body separated as somites and many branched-branchiae on the body side. (B) The spines are arranged horizontally on the dorsal surface.

Fig. 1

Fig. 2

Fig. 3

Ozobranchus jantseanus (Clitellata: Ozobranchidae) from Reeve’s Turtle, Mauremys reevesii: New Annelid Fauna in Korea
PHD : Parasites, Hosts and Diseases

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