Parasitism (Flamingolepis liguloides Gervais, 1847) with High Prevalence in Brine Shrimp Population from Çamaltı Saltworks
Year 2024,
Volume: 30 Issue: 1, 145 - 152, 09.01.2024
Edis Koru
Abstract
Populations of the species Artemia (Brine shrimp) in saltworks have become a popularity popular field of study for aquaculture for its significance for aquatic ecosystems as being an important source of sustenance for water birds in hypersaline food webs. Besides, species in the genus Artemia are the intermediate host of severe cestode species which are associated with flamingos. This study reports on the prevalence of native Artemia parthenogenetica parasitism of Flamingolepis liguloides in the Çamaltı saltern ecosystem in the Gediz wetland between January and December 2022 in Türkiye. Infected A. parthenogenetica was sampled from April to September 2022 in salt pans where flamingo birds and salt production are available for parasitological diagnosis. The parasites were determined in the abdomen, thorax and near the gut tract of A. parthenogenetica. The highest prevalence of parasite was found in juvenile individuals as 86.67±1.45% and adults as 76.06±1.16% in May. The main intensity was varied from 1.18±0.01 to 1.92±0.06 parasites per infected host depending on the sampling months and age of the brine shrimp. The most abundant parasite infestation was recorded as 1.44±0.02 parasites per investigated host in juvenile brine shrimp in June since seasonal conditions are favorable for such infestation.
Supporting Institution
Çamaltı Saltworks Binbir Food Agriculture Salt Products Industry & Trade Inc
Project Number
It is not a project, only the use of the land was allowed.
Thanks
The study; The cestode parasitism (Flamingolepis liguloides Gervais, 1847) with prevalence in Artemia parthenogenetica throughout the annual cycle in a saltern Gediz wetland from the Western Turkey was supported by the Çamaltı Saltworks Binbir Food Agriculture Salt Products Industry & Trade Inc.
References
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- Amat E, Illescas M E Fernandez J (1991a). Brine Shrimp Artemia Parasitized by Flamingolepis liguloides (Cestoda, Hymenolepididae) Cysticercoids in Spanish Mediterranean Salterns. Quantitative Aspects. Vie et Milieu/Life & Environment 41(4): 237–244. hal-03039955
- Amat F, Gozalbo A, Navarro J C, Hontoria F Varo I (1991b). Some Aspects of Artemia Biology Affected by Cestode Parasitism. Hydrobiologia 212: 39–44. https://doi.org/10.1007/BF00025985 Büke E (2002). Sea Bass (Dicentrarchus labrax L., 1781) Seed Production. Turkish of Fisheries and Aquatic Science 2(1): 61-70
- Balkız Ö, Onmuş O, Sıkı M Ö, Döndürenc O G, Arnaud A Germain C (2015). Zoology in the Middle East Turkey as a Crossroad for Greater Flamingos Phoenicopterus roseus: Evidence from Population Trends and Ring-Resightings (Aves: Phoenicopteridae). J. Zoology in the Middle East 61(3) 201–14.
https://doi.org/10.1080/09397140.2015.1058452
- Bechet A Johnson A R (2008). Anthropogenic and Environmental Determinants of Greater Flamingo Phoenicopterus roseus Breeding Numbers and Productivity in the Camargue (Rhone Delta, Southern France). Ibis 150(1): 69–79. https://doi.org/10.1111/J.1474-919X.2007.00740.X
- Brawne R, Sorgeoos P Troman Clive N A (1991). Artemia Biology. CRC Press, Florida https://doi.org/10.1201/9781351069892
- Britton R H Johnson A R (1987). An Ecological Account of a Mediterranean Salina: The Salin de Giraud, Camargue (S. France). Biological Conservation 42(3): 185–230. https://doi.org/10.1016/0006-3207(87)90133-9
- Bush A O, Lafferty K D, Lotz J M Shostak A W (1997). Parasitology Meets Ecology on Its Own Terms: Margolis et Al. Revisited. Journal of Parasitology 83(4): 575–83. https://doi.org/10.2307/3284227
- Curio E (1988). Parasitology in focus. Facts and trends.In E Curio H Mehlhorn (Eds.), Behavior and parasitism, Springer-Verlag, Berlin, pp.149-160
- Gabrion C MacDonald G (1980). Artemia sp. (Crustacea, Anostracea) as Intermediate Host of Eurycestus Avoceti Clark, 1954 (Cestoda, Cyclophyllidea). Annales de Parasitologie Humaine et Comparée 55: 327–31
Georgiev B B, Sánchez M I A, Green J, Nikolov P N, Vasileva G P Mavrodieva S R (2005). Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: A Systematic Survey of Cysticercoids. Acta Parasitologica 50: 105–17
- Georgiev B B, Sánchez M I, Vasileva G P, Nikolov P N Green A J (2007). Cestode Parasitism in Invasive and Native Brine Shrimps (Artemia spp.) as a Possible Factor Promoting the Rapid Invasion of A. franciscana in the Mediterranean Region. Parasitology Research 101(6): 1647–55. https://doi.org/10.1007/S00436-007-0708-3
- Heltdt H (1929). Sur La Présence d’un Cysticercoide Chez Artémia salina L. Bull SOS.
- Helluy S Holmes J C (2005). Parasitic Manipulation: Further Considerations. Behavioural Processes 68(3): 205–10. https://doi.org/10.1016/J.BEPROC.2004.08.011
- Kaska A (2019). Cytotoxic Activities on Selected Lamiaceae Species from Turkey by Brine Shrimp Lethality Bioassay. Ordu University Journal of Science and Technology 9(2):105-111. e-ISSN: 2146-6459
- Kırkağaç M, Gümüş E & Yokuş G (2017). The Effects of Environmental Factors on Artemia Population in Tuz Lake (Central Anatolia, Turkey). Iğdır Univ. J. Inst. Sci. & Tech. 7(2): 303-312. https://doi: 10.21597/jist.2017.143
- Koru E (2013). The Potential of Artemia Population in Çamaltı Saltworks (Sasalı-İzmir) at Aquaculture. Menba Journal of Fisheries Faculty 2: 30–40
- Koru E (2022). Cestode Infection of the Native Brine Shrimp (Artemia parthenogenetica) in Çamaltı Saltpan (İzmir/Türkiye). Çanakkale Onsekiz Mart University Journal of Marine Sciences and Fisheries 5(1): 56–66. https://doi.org/10.46384/JMSF.1084680.
- Kornyychuk Y, Anufriieva E, & Shadrin N (2023). Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity 15(409): 1-21. https://doi.org/10.3390/d15030409
- Maksimova A P (1979). Branchiopod Crustaceans as Intermediate Hosts of Cestodes of the Family Hymenolepididae. Parazitologiya 4: 349–53. https://doi.org/10.7717/PEERJ.7395/SUPP-4
- Mura G (1995). Cestode Parasitism (Flamingolepis liguloides Gervais, 1847 Spassky & Spasskaja 1954) in An Artemia Population from South-Western Sardinia. International Journal of Salt Lake Research 1995 3:2 3(2): 191–200. https://doi.org/10.1007/BF01990494
- Redón S, Green A J, Georgiev B B, Vasileva G P & Amat F (2015). Influence of Developmental Stage and Sex on Infection of the American Brine Shrimp Artemia franciscana Kellogg, 1906 by Avian Cestodes in Ebro Delta Salterns, Spain. Aquatic Invasions 10(4): 415–23. https://doi.org/10.3391/AI.2015.10.4.05
- Redón S, Vasileva G P, Georgiev B B & Gajardo G (2020). Exploring Parasites in Extreme Environments of High Conservational Importance: Artemia franciscana (Crustacea: Branchiopoda) as Intermediate Host of Avian Cestodes in Andean Hypersaline Lagoons from Salar de Atacama, Chile. Parasitology Research 119(10): 3377–90. https://doi.org/10.1007/S00436-020-06768-3
- Robert F & Gabrion C (1991). Cestodoses de l’avifaune Camarguaise. Rôle d’Artemia (Crustacea, Anostraca) et Stratégies de Rencontre Hôte-Parasite. Annales de Parasitologie Humaine et Comparée 66(5): 226–35. https://doi.org/10.1051/PARASITE/1991665226
- Rode N O, Lievens E J P, Flaven E, Segard A, Jabbour-Zahab R, Sanchez M I & Lenormand T (2013a). Why Join Groups? Lessons from Parasite-Manipulated Artemia. Ecology Letters 16(4): 493–501. https://doi.org/10.1111/ELE.12074
- Rode N O, Landes J, Landes E J P, Lievens E, Flaven A, Segard R Jabbour-Zahab, Michalakis Y, Agnew P, Vivarès C P & Lenormand T (2013b). Cytological, Molecular and Life Cycle Characterization of Anostracospora Rigaudi n. g., n. sp. and Enterocytospora Artemiae n. g., n. sp., Two New Microsporidian Parasites Infecting Gut Tissues of the Brine Shrimp Artemia. Parasitology 140(9): 1168–85. https://doi.org/10.1017/S0031182013000668
- Sánchez M I, Green A J & Castellanos E M (2006). Temporal and Spatial Variation of an Aquatic Invertebrate Community Subjected to Avian Predation at the Odiel Salt Pans (SW Spain). Archiv Für Hydrobiologie 166(2): 199–223. https://doi.org/10.1127/0003-9136/2006/0166-0199
- Sánchez M I, Georgiev B B & Green A J (2007). Avian Cestodes Affect the Behaviour of Their Intermediate Host Artemia parthenogenetica: An Experimental Study. Behavioural Processes 74(3): 293–99. https://doi.org/10.1016/J.BEPROC.2006.11.002
- Sánchez M I, Nikolov P N, Georgieva D D, Georgiev B B, Vasileva G P, Pankov P, Paracuellos, Lafferty D K & Green A J (2013). High Prevalence of Cestodes in Artemia spp. throughout the Annual Cycle: Relationship with Abundance of Avian Final Hosts. Parasitology Research 112(5): 1913–23. https://doi.org/10.1007/S00436-013-3347-X
- Sánchez M I, Varo N, Matesanz C, Ramo C, Amat J A & Green A J (2013). Cestodes Change the Isotopic Signature of Brine Shrimp, Artemia, Hosts: Implications for Aquatic Food Webs. International Journal for Parasitology 43(1): 73–80. https://doi.org/10.1016/J.IJPARA.2012.11.003
- Savage A & Knott B (1998). Artemia parthenogenetica in Lake Hayward, Western Australia. II. Feeding Biology in a Shallow, Seasonally Stratified, Hypersaline Lake. International Journal of Salt Lake Research 1998 7:1 7(1): 13–24. https://doi.org/10.1023/A:1009084902677.
- Thiery A, Robert F & Gabrion C (1990). Distribution Des Populations d’Artemia et de Leur Parasite Flamingolepis liguloides (Cestode, Cyclophyllidea), Dans Les Salins Du Littoral Méditerranéen Français. Canadian Journal of Zoology 68(10): 2199–2204. https://doi.org/10.1139/Z90-305
- Thomas F, Cezilly F, De Meeüs T, Crivelli A & Renaud F (1997). Parasitism and Ecology of Wetlands: A Review. Estuaries 20:3 20(3): 646–54. https://doi.org/10.2307/1352622
- Vasileva G P, Redón S, Amat S F, Nikolov P N, Sánchez, M I, Lenormand T & Georgiev B B (2009). Records of Cysticercoids of Fimbriarioides tadornae Maksimova, 1976 and Branchiopodataenia gvozdevi (Maksimova 1988) (Cyclophyllidea, Hymenolepididae) from Brine Shrimps at the Mediterranean Coasts of Spain and France, with a Key to Cestodes from Artemia. Acta Parasitologica 54(2): 143–50. https://doi.org/10.2478/S11686-009-0025-3
Year 2024,
Volume: 30 Issue: 1, 145 - 152, 09.01.2024
Edis Koru
Project Number
It is not a project, only the use of the land was allowed.
References
- Amarouayache M F, Derbal F Kara M H (2009). The Parasitism of Flamingolepis liguloides (Gervais, 1847) (Cestoda, Hymenolepididae) in Artemia salina (Crustacea, Branchiopoda) in Two Saline Lakes in Algeria. Acta Parasitologica 54(4): 330–34. https://doi.org/10.2478/S11686-009-0049-8
- Amat E, Illescas M E Fernandez J (1991a). Brine Shrimp Artemia Parasitized by Flamingolepis liguloides (Cestoda, Hymenolepididae) Cysticercoids in Spanish Mediterranean Salterns. Quantitative Aspects. Vie et Milieu/Life & Environment 41(4): 237–244. hal-03039955
- Amat F, Gozalbo A, Navarro J C, Hontoria F Varo I (1991b). Some Aspects of Artemia Biology Affected by Cestode Parasitism. Hydrobiologia 212: 39–44. https://doi.org/10.1007/BF00025985 Büke E (2002). Sea Bass (Dicentrarchus labrax L., 1781) Seed Production. Turkish of Fisheries and Aquatic Science 2(1): 61-70
- Balkız Ö, Onmuş O, Sıkı M Ö, Döndürenc O G, Arnaud A Germain C (2015). Zoology in the Middle East Turkey as a Crossroad for Greater Flamingos Phoenicopterus roseus: Evidence from Population Trends and Ring-Resightings (Aves: Phoenicopteridae). J. Zoology in the Middle East 61(3) 201–14.
https://doi.org/10.1080/09397140.2015.1058452
- Bechet A Johnson A R (2008). Anthropogenic and Environmental Determinants of Greater Flamingo Phoenicopterus roseus Breeding Numbers and Productivity in the Camargue (Rhone Delta, Southern France). Ibis 150(1): 69–79. https://doi.org/10.1111/J.1474-919X.2007.00740.X
- Brawne R, Sorgeoos P Troman Clive N A (1991). Artemia Biology. CRC Press, Florida https://doi.org/10.1201/9781351069892
- Britton R H Johnson A R (1987). An Ecological Account of a Mediterranean Salina: The Salin de Giraud, Camargue (S. France). Biological Conservation 42(3): 185–230. https://doi.org/10.1016/0006-3207(87)90133-9
- Bush A O, Lafferty K D, Lotz J M Shostak A W (1997). Parasitology Meets Ecology on Its Own Terms: Margolis et Al. Revisited. Journal of Parasitology 83(4): 575–83. https://doi.org/10.2307/3284227
- Curio E (1988). Parasitology in focus. Facts and trends.In E Curio H Mehlhorn (Eds.), Behavior and parasitism, Springer-Verlag, Berlin, pp.149-160
- Gabrion C MacDonald G (1980). Artemia sp. (Crustacea, Anostracea) as Intermediate Host of Eurycestus Avoceti Clark, 1954 (Cestoda, Cyclophyllidea). Annales de Parasitologie Humaine et Comparée 55: 327–31
Georgiev B B, Sánchez M I A, Green J, Nikolov P N, Vasileva G P Mavrodieva S R (2005). Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: A Systematic Survey of Cysticercoids. Acta Parasitologica 50: 105–17
- Georgiev B B, Sánchez M I, Vasileva G P, Nikolov P N Green A J (2007). Cestode Parasitism in Invasive and Native Brine Shrimps (Artemia spp.) as a Possible Factor Promoting the Rapid Invasion of A. franciscana in the Mediterranean Region. Parasitology Research 101(6): 1647–55. https://doi.org/10.1007/S00436-007-0708-3
- Heltdt H (1929). Sur La Présence d’un Cysticercoide Chez Artémia salina L. Bull SOS.
- Helluy S Holmes J C (2005). Parasitic Manipulation: Further Considerations. Behavioural Processes 68(3): 205–10. https://doi.org/10.1016/J.BEPROC.2004.08.011
- Kaska A (2019). Cytotoxic Activities on Selected Lamiaceae Species from Turkey by Brine Shrimp Lethality Bioassay. Ordu University Journal of Science and Technology 9(2):105-111. e-ISSN: 2146-6459
- Kırkağaç M, Gümüş E & Yokuş G (2017). The Effects of Environmental Factors on Artemia Population in Tuz Lake (Central Anatolia, Turkey). Iğdır Univ. J. Inst. Sci. & Tech. 7(2): 303-312. https://doi: 10.21597/jist.2017.143
- Koru E (2013). The Potential of Artemia Population in Çamaltı Saltworks (Sasalı-İzmir) at Aquaculture. Menba Journal of Fisheries Faculty 2: 30–40
- Koru E (2022). Cestode Infection of the Native Brine Shrimp (Artemia parthenogenetica) in Çamaltı Saltpan (İzmir/Türkiye). Çanakkale Onsekiz Mart University Journal of Marine Sciences and Fisheries 5(1): 56–66. https://doi.org/10.46384/JMSF.1084680.
- Kornyychuk Y, Anufriieva E, & Shadrin N (2023). Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity 15(409): 1-21. https://doi.org/10.3390/d15030409
- Maksimova A P (1979). Branchiopod Crustaceans as Intermediate Hosts of Cestodes of the Family Hymenolepididae. Parazitologiya 4: 349–53. https://doi.org/10.7717/PEERJ.7395/SUPP-4
- Mura G (1995). Cestode Parasitism (Flamingolepis liguloides Gervais, 1847 Spassky & Spasskaja 1954) in An Artemia Population from South-Western Sardinia. International Journal of Salt Lake Research 1995 3:2 3(2): 191–200. https://doi.org/10.1007/BF01990494
- Redón S, Green A J, Georgiev B B, Vasileva G P & Amat F (2015). Influence of Developmental Stage and Sex on Infection of the American Brine Shrimp Artemia franciscana Kellogg, 1906 by Avian Cestodes in Ebro Delta Salterns, Spain. Aquatic Invasions 10(4): 415–23. https://doi.org/10.3391/AI.2015.10.4.05
- Redón S, Vasileva G P, Georgiev B B & Gajardo G (2020). Exploring Parasites in Extreme Environments of High Conservational Importance: Artemia franciscana (Crustacea: Branchiopoda) as Intermediate Host of Avian Cestodes in Andean Hypersaline Lagoons from Salar de Atacama, Chile. Parasitology Research 119(10): 3377–90. https://doi.org/10.1007/S00436-020-06768-3
- Robert F & Gabrion C (1991). Cestodoses de l’avifaune Camarguaise. Rôle d’Artemia (Crustacea, Anostraca) et Stratégies de Rencontre Hôte-Parasite. Annales de Parasitologie Humaine et Comparée 66(5): 226–35. https://doi.org/10.1051/PARASITE/1991665226
- Rode N O, Lievens E J P, Flaven E, Segard A, Jabbour-Zahab R, Sanchez M I & Lenormand T (2013a). Why Join Groups? Lessons from Parasite-Manipulated Artemia. Ecology Letters 16(4): 493–501. https://doi.org/10.1111/ELE.12074
- Rode N O, Landes J, Landes E J P, Lievens E, Flaven A, Segard R Jabbour-Zahab, Michalakis Y, Agnew P, Vivarès C P & Lenormand T (2013b). Cytological, Molecular and Life Cycle Characterization of Anostracospora Rigaudi n. g., n. sp. and Enterocytospora Artemiae n. g., n. sp., Two New Microsporidian Parasites Infecting Gut Tissues of the Brine Shrimp Artemia. Parasitology 140(9): 1168–85. https://doi.org/10.1017/S0031182013000668
- Sánchez M I, Green A J & Castellanos E M (2006). Temporal and Spatial Variation of an Aquatic Invertebrate Community Subjected to Avian Predation at the Odiel Salt Pans (SW Spain). Archiv Für Hydrobiologie 166(2): 199–223. https://doi.org/10.1127/0003-9136/2006/0166-0199
- Sánchez M I, Georgiev B B & Green A J (2007). Avian Cestodes Affect the Behaviour of Their Intermediate Host Artemia parthenogenetica: An Experimental Study. Behavioural Processes 74(3): 293–99. https://doi.org/10.1016/J.BEPROC.2006.11.002
- Sánchez M I, Nikolov P N, Georgieva D D, Georgiev B B, Vasileva G P, Pankov P, Paracuellos, Lafferty D K & Green A J (2013). High Prevalence of Cestodes in Artemia spp. throughout the Annual Cycle: Relationship with Abundance of Avian Final Hosts. Parasitology Research 112(5): 1913–23. https://doi.org/10.1007/S00436-013-3347-X
- Sánchez M I, Varo N, Matesanz C, Ramo C, Amat J A & Green A J (2013). Cestodes Change the Isotopic Signature of Brine Shrimp, Artemia, Hosts: Implications for Aquatic Food Webs. International Journal for Parasitology 43(1): 73–80. https://doi.org/10.1016/J.IJPARA.2012.11.003
- Savage A & Knott B (1998). Artemia parthenogenetica in Lake Hayward, Western Australia. II. Feeding Biology in a Shallow, Seasonally Stratified, Hypersaline Lake. International Journal of Salt Lake Research 1998 7:1 7(1): 13–24. https://doi.org/10.1023/A:1009084902677.
- Thiery A, Robert F & Gabrion C (1990). Distribution Des Populations d’Artemia et de Leur Parasite Flamingolepis liguloides (Cestode, Cyclophyllidea), Dans Les Salins Du Littoral Méditerranéen Français. Canadian Journal of Zoology 68(10): 2199–2204. https://doi.org/10.1139/Z90-305
- Thomas F, Cezilly F, De Meeüs T, Crivelli A & Renaud F (1997). Parasitism and Ecology of Wetlands: A Review. Estuaries 20:3 20(3): 646–54. https://doi.org/10.2307/1352622
- Vasileva G P, Redón S, Amat S F, Nikolov P N, Sánchez, M I, Lenormand T & Georgiev B B (2009). Records of Cysticercoids of Fimbriarioides tadornae Maksimova, 1976 and Branchiopodataenia gvozdevi (Maksimova 1988) (Cyclophyllidea, Hymenolepididae) from Brine Shrimps at the Mediterranean Coasts of Spain and France, with a Key to Cestodes from Artemia. Acta Parasitologica 54(2): 143–50. https://doi.org/10.2478/S11686-009-0025-3