Research Article
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First report of leech parasitism in freshwater turtles for Turkish wetlands

Year 2023, Volume: 9 Issue: 2, 108 - 114, 25.08.2023
https://doi.org/10.17216/limnofish.1270081

Abstract

Research on the diversities of parasites and hosts, as well as their relationship, can provide significant contributions to understanding, utilizing, conserving, and properly managing aquatic ecosystems. The freshwater mud turtle Emys orbicularis and Balkan turtle Mauremys rivulata, as well as the leech Placobdella costata, are distributed; however the relations between these organisms are not well-known in Turkish wetlands. In this study, the parasitism of Glossiphonid leech P. costata on freshwater turtles, E. orbicularis, and M. rivulata was assessed for the first time through field observations and laboratory examinations in Turkish wetlands. The infection prevalence in turtles was found to be 76%, with an intensity of 5.00 and an abundance of 3.82, all of which were higher in females. Although the infection prevalence was similar for both E. orbicularis and M. rivulata, infection intensity and abundance were higher in M. rivulata. Leeches were mostly sampled from the plastron and least from the head. The condition of the parasitic leech was found to be high, and P. costata preferred to feed on and parasitize predominantly female individuals of both turtle species.

Supporting Institution

the Scientific Research Projects Coordination Unit at Süleyman Demirel University

Thanks

Eğirdir Fisheries Research Institute

References

  • Ayaz D, Budak A. 2008. Distribution and morphology of Mauremys rivulata (Valenciennes, 1833)(Reptilia: Testudines: Geoemydidae) in the Lake district and Mediterranean region of Turkey. Turk J Zool. 32(2):137-145.
  • Ayaz D, Fritz U, Atatür MK, Mermer A, Çiçek K, Afsar M. 2008. Aspect of population structure of the European pond turtle (Emys orbicularis) in Lake Yayla, Western Anatolia, Turkey. J Herpetol. 42(3):518-522.
  • Baran İ, Atatür MK. 1998. Turkish Herpetofauna (Frogs and Reptiles). Ankara: Ministry of Environment Publication 214 p.
  • Baran İ, Ilgaz Ç, Avcı A, Kumlutaş Y, Olgun K. 2005. Amphibians and Reptiles of Turkey. Ankara: TUBITAK Pop. Sci. Books 204 p.
  • Bashirichelkasari N, Yadollahvandmiandoab R. 2017. Placobdella costata an Ectoparasite for Mauremys caspica in North of Iran. J Aquac Res Development. 8:506. doi: 10.4172/2155-9546.1000506
  • Bayrakcı Y, Ayaz D, Çiçek K, İlhan S. 2017. Population Dynamics of the European Pond Turtle, Emys orbicularis (L., 1758)(Testudinata: Emydidae) from Lake Eğirdir (Isparta, Turkey). Acta Zool Bulg. 10:31-35.
  • Bielecki A, Cichocka JM, Jablonski A, Jelen I, Ropelewska E, Biedunkiewicz A, Terlecki J, Nowakowski JJ, Pakulnicka J, Szlachciak J. 2012. Coexistence of Placobdella costata (Fr. Muller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis. Biologia. 67:1-8.doi: 10.2478/s11756-012-0069-y
  • Bielecki A, Jabłoński A, Palińska K. 2007. The prevalence of occurrence of parasite Placobdella costata (Fr. Miller, 1846) (Hirudinea: Glossiphoniidae) on the mud turtle Emys orbicularis (L.) Wiad Parazytol. 53:115.
  • Ceylan M, Küçükkara R, Akçimen U, Yener O. 2017. Reproduction efficiency of the horse leech, Haemopis sanguisuga (Linnaeus, 1758). Invertebr Reprod Dev. 61(3):182-188. doi: 10.1080/07924259.2017.1318096
  • Ceylan M. 2016. Determination of ecology, population size and catch efficiency of medicinal leech (Hirudo verbana Carena, 1820) populations in wetlands around Lake Eğirdir [PhD thesis] Süleyman Demirel University. 231 p. [in Turkish]
  • Çiçek K, Arıkan H, Ayaz D. 2015. Blood Cells Morphology and Erythrocytes Count of Two Freshwater Turtles, Emys orbicularis and Mauremys rivulata, from Turkey. Ecol Balk. 7(1):21-27
  • Davies RW, McLoughlin NJ, Oosthuizen JH. 1997. The life-cycle and feeding of the African freshwater leech Helobdella conifera (Glossiphoniidae). Afr Zool. 32(1):1-4. doi: 10.1080/02541858.1997.11448418
  • Elliott JM, Dobson M. 2015. Freshwater leeches of Britain and Ireland: keys to the Hirudinea and a review of their ecology. Cumbria: Freshwater Biological Association 108 p.
  • Fediras S, Rouag R, Ziane N, Olivier A, Béchet A, Benyacoub S. 2017. Prevalence of Placobdella costata (Fr. Mûller, 1846) (Hirudinida: Glossiphoniidae) on the European pond turtle (Emys orbicularis) in the North-East of Algeria. Herpetol Notes. 10:3-8.
  • Friesen OC, Goellner S, Poulin R, Lagrue C. 2020. Parasites shape community structure and dynamics in freshwater crustaceans. Parasitol. 147(2):182-193. doi: 10.1017/S0031182019001483
  • Kaviani M, Rahimibashar MR. 2015. Sexual dimorphism of the European Pond Turtle, Emys orbicularis (Linnaeus, 1758), in Anzali Lagoon, Iran (Reptilia: Emydidae). Zool Middle East. 61(3):231-235. doi: 10.1080/09397140.2015.1070524
  • Kazancı N, Ekingen P, Dügel M, Türkmen G. 2015. Hirudinea (Annelida) species and their ecological preferences in some running waters and lakes. Int J Environ Sci Technol. 12(3):1087-1096. doi: 10.1007/s13762-014-0574-3
  • Kazancı N, Plasa RH, Neubert E, İzbırak A. 1992. On the limnology of Lake Köycegiz (SW Anatolia). Zool Middle East. 6(1):109-126. doi: 10.1080/09397140.1992.10637619
  • Kermanian CS, Buote NJ, Bergman, PJ. 2022. Medicinal leech therapy in veterinary medicine: a retrospective study. J Am Anim Hosp Assoc. 58(6):303-308. doi: 10.5326/JAAHA-MS-7146
  • Laghzaoui EM, Abbad A, El Mouden EH. 2020. Host-parasite association of Placobdella costata (Glossiphoniidae: Hirudinea) and Mauremys leprosa (Geoemydidae: Testudinoidea) in aquatic ecosystems of Morocco. Parasitol Res. 119(10):3459-3467. doi: 10.1007/s00436-020-06809-x
  • Lebboroni M, Chelazzi G. 1991. Activity patterns of Emys orbicularis L.(Chelonia Emydidae) in central Italy. Ethol Ecol Evol. 3(3):257-268.
  • Lovich JE, Ennen JR, Agha M, Gibbons JW. 2018. Where have all the turtles gone, and why does it matter? BioScience. 68(10):771-781. doi: 10.1093/biosci/biy095
  • Lynggaard C, Figueroa-Oceguera A, Kvist S, Gilbert MTP, Bohmann K. 2022. The potential of aquatic bloodfeeding and nonbloodfeeding leeches as a tool for iDNA characterisation. Mol Ecol Resour. 22(2):539-553. doi: 10.1111/1755-0998.13486
  • McCoy CJ, Failey EL, Price SJ, Dorcas ME. 2007. An Assessment of Leech Parasitism on Semi-aquatic Turtles in the Western Piedmont of North Carolina. Southeast Nat. 6(2):191-202.
  • Nesemann H, Neubert E. 1999. Annelida, Clitellata: Branchiobdellida, Acanthobdellea, Hirudinea. Süßwasserfauna von Mitteleuropa 6/2. Elsevier GmbH, Spektrum Akademischer Verlag, Heidelberg, 1-178.
  • O’Keeffe KR, Halliday FW, Jones CD, Carbone I, Mitchell CE. 2021. Parasites, niche modification and the host microbiome: A field survey of multiple parasites. Mol Ecol. 30(10):2404-2416. doi: 10.1111/mec.15892
  • Özbek M, Sarı HM. 2007. Hirudinea (Annelida) fauna of some lakes located in western Black Sea Region. Ege J Fish Aquat Sci. 24(1):83-88.
  • Pfeiffer I, Brenig B, Kutschera U. 2005. Molecular phylogeny of selected predaceous leeches with reference to the evolution of body size and terrestrialism. Theory Biosci. 124(1):55-64. doi: 10.1016/j.thbio.2005.05.002
  • Poulin R, Morand S. 2000. The diversity of parasites. Q Rev Biol. 75(3):277-293.
  • Preston D, Johnson P. 2010. Ecological Consequences of Parasitism. Nat Sci Educ. 3(10):47.
  • Readel AM, Philps CA, Wetzel MR. 2008. Leech parasitism in a turtle assemblage: Effects of host and environmental characteristics. Copeia. 1: 227-233. doi: 10.1643/CH-06-212
  • Sağlam N. 2001. First record of the leech Placobdella costata (Hirudinoidea: Glossiphoniidae) in Turkey. Zool Middle East. 23(1):113-118. doi: 10.1080/09397140.2001.10637876
  • Santori C, Spencer RJ, Thompson MB, Whittington CM, Burd TH, Currie SB, Finter TJ, Van Dyke JU. 2020. Scavenging by threatened turtles regulates freshwater ecosystem health during fish kills. Sci Rep. 10(1):14383. doi: 10.1038/s41598-020-71544-3
  • Sawyer RT. 1986. Leech biology and behaviour. Oxford: Clarendon press 1065 p.
  • Siddall ME, Burreson EM. 1996. Leeches (Oligochaeta?: Euhirudinea), their phylogeny and the evolution of life-history strategies. Hydrobiologia. 334(1):277-285. doi: 10.1007/BF00017378
  • Siddall ME, Desser SS. 1992. Alternative leech vectors for frog and turtle trypanosomes. J Parasitol. 78(3):562-563. doi: 10.2307/3283672
  • Sig AK, Guney M, Guclu AU, Ozmen E. 2017. Medicinal leech therapy—an overall perspective. Integr Med Res. 6(4):337-343. doi: 10.1016/j.imr.2017.08.001
  • Williams KM, Barkdull M, Fahmy M, Hekkala E, Siddall ME, Kvist S. 2020. Caught red handed: iDNA points to wild source for CITES-protected contraband leeches. Eur J Wildl Res. 66(5):80. doi: 10.1007/s10344-020-01419-5
  • Zuffi MAL, Gariboldi A. 1995. Sexual dimorphism of the European pond terrapin, Emys orbicularis (L., 1758) from Italy. Sci Herpetol. 1995:124-129.

Türkiye sulak alanlarındaki tatlı su kaplumbağalarında sülük parazitliğine ilişkin ilk rapor

Year 2023, Volume: 9 Issue: 2, 108 - 114, 25.08.2023
https://doi.org/10.17216/limnofish.1270081

Abstract

Öz: Parazitlerin ve konakçıların çeşitliliğinin yanı sıra aralarındaki ekolojik ilişkilerin araştırılması, sucul ekosistemlerin anlaşılması, kullanılması, korunması ve uygun şekilde yönetilmesine önemli katkılar sağlayabilmektedir. Benekli kaplumbağa Emys orbicularis ve Balkan kaplumbağası Mauremys rivulata ile Placobdella costata sülük türü Türkiye sulak alanlarında yayılış göstermektedir; ancak bu organizmalar arasındaki ilişkiler tam olarak bilinmemektedir. Bu çalışmada, Glossiphonid sülüklerden P. costata türünün tatlı su kaplumbağaları, E. orbicularis ve M. rivulata üzerindeki parazitliği, saha gözlemleri ve laboratuvar incelemeleri yoluyla Türkiye sulak alanlarında ilk kez incelenmiştir. Kaplumbağalardaki enfeksiyon prevalansı %76, yoğunluğu 5,00 ve bolluğu 3,82 olarak bulunmuştur ve bunların hepsi dişilerde daha yüksek bulunmuştur. Enfeksiyon prevalansı hem E. orbicularis hem de M. rivulata için benzer olmasına rağmen, enfeksiyon yoğunluğu ve bolluğunun M. rivulata türünde daha yüksek olduğu belirlenmiştir. Sülükler en çok plastrondan, buna karşın en az ise kafadan örneklenmiştir. Sülüklerin kondisyonlarının yüksek olduğu ve P. costata türünün her iki kaplumbağa türünün ağırlıklı olarak dişi bireylerini parazitlemeyi tercih ettiği dikkat çekmiştir.

References

  • Ayaz D, Budak A. 2008. Distribution and morphology of Mauremys rivulata (Valenciennes, 1833)(Reptilia: Testudines: Geoemydidae) in the Lake district and Mediterranean region of Turkey. Turk J Zool. 32(2):137-145.
  • Ayaz D, Fritz U, Atatür MK, Mermer A, Çiçek K, Afsar M. 2008. Aspect of population structure of the European pond turtle (Emys orbicularis) in Lake Yayla, Western Anatolia, Turkey. J Herpetol. 42(3):518-522.
  • Baran İ, Atatür MK. 1998. Turkish Herpetofauna (Frogs and Reptiles). Ankara: Ministry of Environment Publication 214 p.
  • Baran İ, Ilgaz Ç, Avcı A, Kumlutaş Y, Olgun K. 2005. Amphibians and Reptiles of Turkey. Ankara: TUBITAK Pop. Sci. Books 204 p.
  • Bashirichelkasari N, Yadollahvandmiandoab R. 2017. Placobdella costata an Ectoparasite for Mauremys caspica in North of Iran. J Aquac Res Development. 8:506. doi: 10.4172/2155-9546.1000506
  • Bayrakcı Y, Ayaz D, Çiçek K, İlhan S. 2017. Population Dynamics of the European Pond Turtle, Emys orbicularis (L., 1758)(Testudinata: Emydidae) from Lake Eğirdir (Isparta, Turkey). Acta Zool Bulg. 10:31-35.
  • Bielecki A, Cichocka JM, Jablonski A, Jelen I, Ropelewska E, Biedunkiewicz A, Terlecki J, Nowakowski JJ, Pakulnicka J, Szlachciak J. 2012. Coexistence of Placobdella costata (Fr. Muller, 1846) (Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis. Biologia. 67:1-8.doi: 10.2478/s11756-012-0069-y
  • Bielecki A, Jabłoński A, Palińska K. 2007. The prevalence of occurrence of parasite Placobdella costata (Fr. Miller, 1846) (Hirudinea: Glossiphoniidae) on the mud turtle Emys orbicularis (L.) Wiad Parazytol. 53:115.
  • Ceylan M, Küçükkara R, Akçimen U, Yener O. 2017. Reproduction efficiency of the horse leech, Haemopis sanguisuga (Linnaeus, 1758). Invertebr Reprod Dev. 61(3):182-188. doi: 10.1080/07924259.2017.1318096
  • Ceylan M. 2016. Determination of ecology, population size and catch efficiency of medicinal leech (Hirudo verbana Carena, 1820) populations in wetlands around Lake Eğirdir [PhD thesis] Süleyman Demirel University. 231 p. [in Turkish]
  • Çiçek K, Arıkan H, Ayaz D. 2015. Blood Cells Morphology and Erythrocytes Count of Two Freshwater Turtles, Emys orbicularis and Mauremys rivulata, from Turkey. Ecol Balk. 7(1):21-27
  • Davies RW, McLoughlin NJ, Oosthuizen JH. 1997. The life-cycle and feeding of the African freshwater leech Helobdella conifera (Glossiphoniidae). Afr Zool. 32(1):1-4. doi: 10.1080/02541858.1997.11448418
  • Elliott JM, Dobson M. 2015. Freshwater leeches of Britain and Ireland: keys to the Hirudinea and a review of their ecology. Cumbria: Freshwater Biological Association 108 p.
  • Fediras S, Rouag R, Ziane N, Olivier A, Béchet A, Benyacoub S. 2017. Prevalence of Placobdella costata (Fr. Mûller, 1846) (Hirudinida: Glossiphoniidae) on the European pond turtle (Emys orbicularis) in the North-East of Algeria. Herpetol Notes. 10:3-8.
  • Friesen OC, Goellner S, Poulin R, Lagrue C. 2020. Parasites shape community structure and dynamics in freshwater crustaceans. Parasitol. 147(2):182-193. doi: 10.1017/S0031182019001483
  • Kaviani M, Rahimibashar MR. 2015. Sexual dimorphism of the European Pond Turtle, Emys orbicularis (Linnaeus, 1758), in Anzali Lagoon, Iran (Reptilia: Emydidae). Zool Middle East. 61(3):231-235. doi: 10.1080/09397140.2015.1070524
  • Kazancı N, Ekingen P, Dügel M, Türkmen G. 2015. Hirudinea (Annelida) species and their ecological preferences in some running waters and lakes. Int J Environ Sci Technol. 12(3):1087-1096. doi: 10.1007/s13762-014-0574-3
  • Kazancı N, Plasa RH, Neubert E, İzbırak A. 1992. On the limnology of Lake Köycegiz (SW Anatolia). Zool Middle East. 6(1):109-126. doi: 10.1080/09397140.1992.10637619
  • Kermanian CS, Buote NJ, Bergman, PJ. 2022. Medicinal leech therapy in veterinary medicine: a retrospective study. J Am Anim Hosp Assoc. 58(6):303-308. doi: 10.5326/JAAHA-MS-7146
  • Laghzaoui EM, Abbad A, El Mouden EH. 2020. Host-parasite association of Placobdella costata (Glossiphoniidae: Hirudinea) and Mauremys leprosa (Geoemydidae: Testudinoidea) in aquatic ecosystems of Morocco. Parasitol Res. 119(10):3459-3467. doi: 10.1007/s00436-020-06809-x
  • Lebboroni M, Chelazzi G. 1991. Activity patterns of Emys orbicularis L.(Chelonia Emydidae) in central Italy. Ethol Ecol Evol. 3(3):257-268.
  • Lovich JE, Ennen JR, Agha M, Gibbons JW. 2018. Where have all the turtles gone, and why does it matter? BioScience. 68(10):771-781. doi: 10.1093/biosci/biy095
  • Lynggaard C, Figueroa-Oceguera A, Kvist S, Gilbert MTP, Bohmann K. 2022. The potential of aquatic bloodfeeding and nonbloodfeeding leeches as a tool for iDNA characterisation. Mol Ecol Resour. 22(2):539-553. doi: 10.1111/1755-0998.13486
  • McCoy CJ, Failey EL, Price SJ, Dorcas ME. 2007. An Assessment of Leech Parasitism on Semi-aquatic Turtles in the Western Piedmont of North Carolina. Southeast Nat. 6(2):191-202.
  • Nesemann H, Neubert E. 1999. Annelida, Clitellata: Branchiobdellida, Acanthobdellea, Hirudinea. Süßwasserfauna von Mitteleuropa 6/2. Elsevier GmbH, Spektrum Akademischer Verlag, Heidelberg, 1-178.
  • O’Keeffe KR, Halliday FW, Jones CD, Carbone I, Mitchell CE. 2021. Parasites, niche modification and the host microbiome: A field survey of multiple parasites. Mol Ecol. 30(10):2404-2416. doi: 10.1111/mec.15892
  • Özbek M, Sarı HM. 2007. Hirudinea (Annelida) fauna of some lakes located in western Black Sea Region. Ege J Fish Aquat Sci. 24(1):83-88.
  • Pfeiffer I, Brenig B, Kutschera U. 2005. Molecular phylogeny of selected predaceous leeches with reference to the evolution of body size and terrestrialism. Theory Biosci. 124(1):55-64. doi: 10.1016/j.thbio.2005.05.002
  • Poulin R, Morand S. 2000. The diversity of parasites. Q Rev Biol. 75(3):277-293.
  • Preston D, Johnson P. 2010. Ecological Consequences of Parasitism. Nat Sci Educ. 3(10):47.
  • Readel AM, Philps CA, Wetzel MR. 2008. Leech parasitism in a turtle assemblage: Effects of host and environmental characteristics. Copeia. 1: 227-233. doi: 10.1643/CH-06-212
  • Sağlam N. 2001. First record of the leech Placobdella costata (Hirudinoidea: Glossiphoniidae) in Turkey. Zool Middle East. 23(1):113-118. doi: 10.1080/09397140.2001.10637876
  • Santori C, Spencer RJ, Thompson MB, Whittington CM, Burd TH, Currie SB, Finter TJ, Van Dyke JU. 2020. Scavenging by threatened turtles regulates freshwater ecosystem health during fish kills. Sci Rep. 10(1):14383. doi: 10.1038/s41598-020-71544-3
  • Sawyer RT. 1986. Leech biology and behaviour. Oxford: Clarendon press 1065 p.
  • Siddall ME, Burreson EM. 1996. Leeches (Oligochaeta?: Euhirudinea), their phylogeny and the evolution of life-history strategies. Hydrobiologia. 334(1):277-285. doi: 10.1007/BF00017378
  • Siddall ME, Desser SS. 1992. Alternative leech vectors for frog and turtle trypanosomes. J Parasitol. 78(3):562-563. doi: 10.2307/3283672
  • Sig AK, Guney M, Guclu AU, Ozmen E. 2017. Medicinal leech therapy—an overall perspective. Integr Med Res. 6(4):337-343. doi: 10.1016/j.imr.2017.08.001
  • Williams KM, Barkdull M, Fahmy M, Hekkala E, Siddall ME, Kvist S. 2020. Caught red handed: iDNA points to wild source for CITES-protected contraband leeches. Eur J Wildl Res. 66(5):80. doi: 10.1007/s10344-020-01419-5
  • Zuffi MAL, Gariboldi A. 1995. Sexual dimorphism of the European pond terrapin, Emys orbicularis (L., 1758) from Italy. Sci Herpetol. 1995:124-129.

Details

Primary Language English
Subjects Limnology
Journal Section Research Article
Authors

Mustafa CEYLAN 0000-0002-3283-0637

Osman ÇETİNKAYA 0000-0001-6085-0128

Project Number SDU-BAP 3341-D2-12
Publication Date August 25, 2023
Published in Issue Year 2023Volume: 9 Issue: 2

Cite

APA CEYLAN, M., & ÇETİNKAYA, O. (2023). First report of leech parasitism in freshwater turtles for Turkish wetlands. Journal of Limnology and Freshwater Fisheries Research, 9(2), 108-114. https://doi.org/10.17216/limnofish.1270081