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Artemia parthenogenetica'nın parazitolojik incelenmesi: Ayvalık Tuzlası'nda bir sestod olgusu

Year 2024, Volume: 9 Issue: 1, 94 - 99, 31.03.2024
https://doi.org/10.35229/jaes.1442106

Abstract

Su ürünleri yetiştiriciliği sektörü ve flamingolar (Phoenicopterus roseus) gibi yabani hayvan popülasyonları için temel gıda kaynaklarından biri Artemia'dır (Artemia parthenogenetica). Son yıllarda farklı tuzlalardan gelen vaka ve raporların artmasıyla birlikte Artemia sestod parazitizminin yaygınlığı arttığı görülmektedir. Flamingolepis liguloides yumurtaları Artemia tarafından tüketilir ve son konakçı flamingolarda yetişkin solucanlara dönüşen sistiserkoidlere dönüşür. Bu çalışma Ayvalık tuzlasındaki (Balıkesir, Türkiye) A. parthenogenetica'nın doğal popülasyonlarındaki sestod parazitizminin ilk araştırmasıdır. Toplam 965 A. parthenogenetica incelendi ve bunların 320'sinde F. liguloides enfeksiyonu görüldü. Genel prevalans %33,2 olarak hesaplandı. Parazitlerin çoğu A. parthenogenetica'nın toraks, karın ve bağırsak kanalında bulundu. Parazit yoğunluğu birey başına 1 ila 4 arasında değişmekle birlikte tek bir Artemia örneğinde maksimum 4 sistiserkoid tespit edildi. Ayvalık tuzlasından bildirilen bu ilk rapor, Artemia'da F. liguloides istilası hakkında bilgi vermektedir ve tuzlalardaki türler arasındaki etkileşimler ayrıntılı şekilde araştırılmalıdır.

References

  • Amarouayache, M., 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, 330-334. DOI: 10.2478/s11686-009-0049-8
  • Balta, F. (2020). Kültürü yapılan Karadeniz alabalığı (Salmo trutta labrax)’ndaki Gyrodactylus spp. Enfeksiyonlarının Tedavisi. Journal of Anatolian Environmental and Animal Sciences, 5(4). 630- 635. https://doi.org/10.35229/jaes.827930
  • Balta, F., Balta, Z.D. & Akhan, S. (2019). Seasonal distribution of protozoan parasite infections in rainbow trout (Oncorhynchus mykiss) farms in the Eastern Black Sea of Turkey. Bulletin of the European Association of Fish Pathologists, 39(1), 31-39.
  • Dong, X., Li, C., Wang, Y., Hu, T., Zhang, F., Meng, F., Gao, M., Han, X., Wang, G., Qin, J., Nauwynck, H., Holmes, E.C., Sorgeloos, P., Sui, L., Huang, J. & Shi, W. (2023). Diversity and connectedness of brine shrimp viruses in global hypersaline ecosystems. Science China Life Sciences, 1-16. DOI: 10.1007/s11427-022- 2366-8
  • Gajardo, G.M. & Beardmore, J. A. (2012). The brine shrimp Artemia: adapted to critical life conditions. Frontiers in physiology, 3(185). DOI: 10.3389/fphys.2012.00185
  • Georgiev, B.B., Angelov, A., Vasileva, G.P., Sánchez, M.I., Hortas, F., Mutafchiev, Y., Pankov, P. & Green, A.J. (2014). Larval helminths in the invasive American brine shrimp Artemia franciscana throughout its annual cycle. Acta Parasitologica, 59, 380-389. DOI: 10.2478/s11686-014-0255-x
  • 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, 1647-1655. DOI: 10.1007/s00436-007-0708-3
  • Georgiev, B.B., Sánchez, M.I., Green, A.J., Nikolov, P.N., Vasileva, G.G. & Mavrodieva, R.S. (2005). Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: a systematic survey of cysticercoids. Acta Parasitologica, 50(2):105-117.
  • Jia, Q., Anufriieva, E., Liu, X., Kong, F. & Shadrin, N. (2015). Intentional introduction of Artemia sinica (Anostraca) in the high-altitude Tibetan Lake Dangxiong Co: the new population and consequences for the environment and for humans. Chinese Journal of Oceanology and Limnology, 33, 1451-1460. DOI: 10.1007/s00343-015-4371-8
  • Kornyychuk, Y., Anufriieva, E. & Shadrin, N. (2023). Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity, 15(3), 409. DOI: 10.3390/d15030409
  • 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. DOI: 10.46384/jmsf.1084680
  • Nunes, B.S., Carvalho, F.D., Guilhermino, L.M. & Van Stappen, G. (2006). Use of the genus Artemia in ecotoxicity testing. Environmental pollution, 144(2), 453-462. DOI: 10.1016/j.envpol.2005.12.037
  • Oliveira, T.M.N. & Vaz, C. (2018). Marine toxicology: Assays and perspectives for developing countries. In Bioassays (pp. 387-401). Elsevier, 2018. p. 387-401.
  • Parker, G.A., Chubb, J.C., Roberts, G.N., Michaud, M. & Milinski, M. (2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology, 16(1), 47-54. DOI: 10.1046/j.1420-9101.2003.00504.x
  • Redón, S., Quiroz, M., Lukić, D., Green, A.J. & Gajardo, G. (2024). Phylogenetic Relationships of Avian Cestodes from Brine Shrimp and Congruence with Larval Morphology. Animals, 14(3), 397. DOI: 10.3390/ani14030397
  • Redón, S., Gajardo, G., Vasileva, G.P., Sánchez, M.I. & Green, A.J. (2021). Explaining variation in abundance and species diversity of avian cestodes in brine shrimps in the Salar de Atacama and other Chilean wetlands. Water, 13(13), 1742. DOI: 10.3390/w13131742
  • 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, 3377-3390. DOI: 10.1007/s00436-020- 06768-3
  • Redón, S., Vasileva, G.P., Georgiev, B.B. & Gajardo, G. (2019). First report of cestode infection in the crustacean Artemia persimilis from Southern Chilean Patagonia and its relation with the Neotropical aquatic birds. PeerJ, 7, e7395. DOI: 10.7717/peerj.7395
  • Redón, S., Berthelemy, N.J., Mutafchiev, Y., Amat, F., Georgiev, B.B. & Vasileva, G.P. (2015). Helminth parasites of Artemia franciscana (Crustacea: Branchiopoda) in the Great Salt Lake, Utah: first data from the native range of this invader of European wetlands. Folia Parasitologica, 62(1), 30-30. DOI: 10.14411/fp.2015.030
  • Sanchez, M.I., Paredes, I., Lebouvier, M. & Green, A.J. (2016a). Functional role of native and invasive filter-feeders, and the effect of parasites: learning from hypersaline ecosystems. PloS one, 11(8), e0161478. DOI: 10.1371/journal.pone.0161478
  • Sánchez, M.I., Pons, I., Martínez-Haro, M., Taggart, M.A., Lenormand, T. & Green, A.J. (2016b). When parasites are good for health: cestode parasitism increases resistance to arsenic in brine shrimps. PLoS Pathogens, 12(3), e1005459. DOI: 10.1371/journal.ppat.1005459
  • Sánchez, M.I., Nikolov, P.N., Georgieva, D.D., Georgiev, B.B., Vasileva, G.P., Pankov, P., Paracuellos, M., Lafferty, K.D. & Green, A.J. (2013a). High prevalence of cestodes in Artemia spp. throughout the annual cycle: relationship with abundance of avian final hosts. Parasitology Research, 112, 1913-1923. DOI: 10.1007/s00436-013-3347-x
  • Sánchez, M.I., Varo, N., Matesanz, C., Ramo, C., Amat, J.A. & Green, A.J. (2013b). Cestodes change the isotopic signature of brine shrimp, Artemia, hosts: implications for aquatic food webs. International Journal for Parasitology, 43(1), 73-80. DOI: 10.1016/j.ijpara.2012.11.003
  • 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). Arch. Hydrobiol. 2006, 166, 199-223. DOI: 10.1127/0003-9136/2006/0166-0199
  • Schuster, R.K. (2018). The role of Artemia spp.(Branchiopoda: Artemiidae) as intermediate hosts for avian cestodes. Environmental Analysis and Ecological Studies, 1(4). DOI: 10.31031/EAES.2018.01.000518
  • Serrão, C. & Marques-Santos, L.F. (2023). The genus Artemia, the nanoplastics, the microplastics, and their toxic effects: a review. Environmental Science and Pollution Research, 1-26. DOI: 10.1007/s11356-023-27868-4
  • Sivaji, S. (2016). Evaluation of different feeds for the culture of Artemia parthenogenetica. Advance Research Journal of Medical and Clinical Sciences, 2(3), 8-14. DOI: 10.52845/arjmcs.v2i3.20
  • Sivakumar, S., Hyland, K. & Schuster, R.K. (2020). Tapeworm larvae in Artemia franciscana (Crustacea: Anostraca) in the Godolphin lakes of Dubai (United Arab Emirates) throughout an annual cycle. Journal of helminthology, 94, e5. DOI: 10.1017/S0022149X18000913
  • Van Stappen, G., Sui, L., Hoa, V.N., Tamtin, M., Nyonje, B., de Medeiros Rocha, R., Sorgeloos, P. & Gajardo, G. (2020). Review on integrated production of the brine shrimp Artemia in solar salt ponds. Reviews in Aquaculture, 12(2), 1054- 1071. DOI: 10.1111/raq.12371
  • Varo, N., Green, A.J., Sánchez, M.I., Ramo, C., Gómez, J. & Amat, J.A. (2011). Behavioural and population responses to changing availability of Artemia prey by moulting black-necked grebes, Podiceps nigricollis. Hydrobiologia, 664, 163- 171. DOI: 10.1007/s10750-010-0596-x
  • Wang, Y.T., Shi, C.Y., Sui, L.Y., Ye, S.G., Dong, X. & Huang, J. (2020). Research progress on the risk of Artemia acting as a kind of live feed to spread shrimp pathogens (in Chinese). China Anim Health Inspect 37, 61-67. DOI: 10.3969/j.issn.1005-944X.2020.11.013

Parasitological investigation of Artemia parthenogenetica: A Cestode case from Ayvalık Saltwork

Year 2024, Volume: 9 Issue: 1, 94 - 99, 31.03.2024
https://doi.org/10.35229/jaes.1442106

Abstract

One of the primary food supplies for the aquaculture sector and wild animal populations, such as flamingos (Phoenicopterus roseus), is Artemia (Artemia parthenogenetica). Along with the rise in cases and reports from different salterns in recent years, the prevalence of Artemia cestode parasitism has also grown. Flamingolepis liguloides eggs are consumed by Artemia and transform into cysticercoids which mature into adult worms in the final host, flamingos. We described the first investigation of cestode parasitism in the natural populations of Artemia parthenogenetica from the Ayvalık saltwork (Balıkesir, Türkiye) in this study. A total of 965 A. parthenogenetica were examined and 320 of them had F. liguloides infection. The overall prevalence was estimated to be 33.2%. Most of the parasites were found in the abdomen and intestinal tract of A. parthenogenetica. Parasitism intensity ranged from 1 to 4 per individual, with a maximum of 4 cysticercoids detected in a single Artemia sample. To understand the influence of parasitism on Artemia populations and the transmission of species, it is important to establish Artemia parasitism in the saltwork. This initial report from the Ayvalık saltwork provides information on the infestation of F. liguloides in Artemia; therefore, the interactions between the saltworks’ species should be investigated in depth.

References

  • Amarouayache, M., 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, 330-334. DOI: 10.2478/s11686-009-0049-8
  • Balta, F. (2020). Kültürü yapılan Karadeniz alabalığı (Salmo trutta labrax)’ndaki Gyrodactylus spp. Enfeksiyonlarının Tedavisi. Journal of Anatolian Environmental and Animal Sciences, 5(4). 630- 635. https://doi.org/10.35229/jaes.827930
  • Balta, F., Balta, Z.D. & Akhan, S. (2019). Seasonal distribution of protozoan parasite infections in rainbow trout (Oncorhynchus mykiss) farms in the Eastern Black Sea of Turkey. Bulletin of the European Association of Fish Pathologists, 39(1), 31-39.
  • Dong, X., Li, C., Wang, Y., Hu, T., Zhang, F., Meng, F., Gao, M., Han, X., Wang, G., Qin, J., Nauwynck, H., Holmes, E.C., Sorgeloos, P., Sui, L., Huang, J. & Shi, W. (2023). Diversity and connectedness of brine shrimp viruses in global hypersaline ecosystems. Science China Life Sciences, 1-16. DOI: 10.1007/s11427-022- 2366-8
  • Gajardo, G.M. & Beardmore, J. A. (2012). The brine shrimp Artemia: adapted to critical life conditions. Frontiers in physiology, 3(185). DOI: 10.3389/fphys.2012.00185
  • Georgiev, B.B., Angelov, A., Vasileva, G.P., Sánchez, M.I., Hortas, F., Mutafchiev, Y., Pankov, P. & Green, A.J. (2014). Larval helminths in the invasive American brine shrimp Artemia franciscana throughout its annual cycle. Acta Parasitologica, 59, 380-389. DOI: 10.2478/s11686-014-0255-x
  • 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, 1647-1655. DOI: 10.1007/s00436-007-0708-3
  • Georgiev, B.B., Sánchez, M.I., Green, A.J., Nikolov, P.N., Vasileva, G.G. & Mavrodieva, R.S. (2005). Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: a systematic survey of cysticercoids. Acta Parasitologica, 50(2):105-117.
  • Jia, Q., Anufriieva, E., Liu, X., Kong, F. & Shadrin, N. (2015). Intentional introduction of Artemia sinica (Anostraca) in the high-altitude Tibetan Lake Dangxiong Co: the new population and consequences for the environment and for humans. Chinese Journal of Oceanology and Limnology, 33, 1451-1460. DOI: 10.1007/s00343-015-4371-8
  • Kornyychuk, Y., Anufriieva, E. & Shadrin, N. (2023). Diversity of Parasitic Animals in Hypersaline Waters: A Review. Diversity, 15(3), 409. DOI: 10.3390/d15030409
  • 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. DOI: 10.46384/jmsf.1084680
  • Nunes, B.S., Carvalho, F.D., Guilhermino, L.M. & Van Stappen, G. (2006). Use of the genus Artemia in ecotoxicity testing. Environmental pollution, 144(2), 453-462. DOI: 10.1016/j.envpol.2005.12.037
  • Oliveira, T.M.N. & Vaz, C. (2018). Marine toxicology: Assays and perspectives for developing countries. In Bioassays (pp. 387-401). Elsevier, 2018. p. 387-401.
  • Parker, G.A., Chubb, J.C., Roberts, G.N., Michaud, M. & Milinski, M. (2003). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology, 16(1), 47-54. DOI: 10.1046/j.1420-9101.2003.00504.x
  • Redón, S., Quiroz, M., Lukić, D., Green, A.J. & Gajardo, G. (2024). Phylogenetic Relationships of Avian Cestodes from Brine Shrimp and Congruence with Larval Morphology. Animals, 14(3), 397. DOI: 10.3390/ani14030397
  • Redón, S., Gajardo, G., Vasileva, G.P., Sánchez, M.I. & Green, A.J. (2021). Explaining variation in abundance and species diversity of avian cestodes in brine shrimps in the Salar de Atacama and other Chilean wetlands. Water, 13(13), 1742. DOI: 10.3390/w13131742
  • 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, 3377-3390. DOI: 10.1007/s00436-020- 06768-3
  • Redón, S., Vasileva, G.P., Georgiev, B.B. & Gajardo, G. (2019). First report of cestode infection in the crustacean Artemia persimilis from Southern Chilean Patagonia and its relation with the Neotropical aquatic birds. PeerJ, 7, e7395. DOI: 10.7717/peerj.7395
  • Redón, S., Berthelemy, N.J., Mutafchiev, Y., Amat, F., Georgiev, B.B. & Vasileva, G.P. (2015). Helminth parasites of Artemia franciscana (Crustacea: Branchiopoda) in the Great Salt Lake, Utah: first data from the native range of this invader of European wetlands. Folia Parasitologica, 62(1), 30-30. DOI: 10.14411/fp.2015.030
  • Sanchez, M.I., Paredes, I., Lebouvier, M. & Green, A.J. (2016a). Functional role of native and invasive filter-feeders, and the effect of parasites: learning from hypersaline ecosystems. PloS one, 11(8), e0161478. DOI: 10.1371/journal.pone.0161478
  • Sánchez, M.I., Pons, I., Martínez-Haro, M., Taggart, M.A., Lenormand, T. & Green, A.J. (2016b). When parasites are good for health: cestode parasitism increases resistance to arsenic in brine shrimps. PLoS Pathogens, 12(3), e1005459. DOI: 10.1371/journal.ppat.1005459
  • Sánchez, M.I., Nikolov, P.N., Georgieva, D.D., Georgiev, B.B., Vasileva, G.P., Pankov, P., Paracuellos, M., Lafferty, K.D. & Green, A.J. (2013a). High prevalence of cestodes in Artemia spp. throughout the annual cycle: relationship with abundance of avian final hosts. Parasitology Research, 112, 1913-1923. DOI: 10.1007/s00436-013-3347-x
  • Sánchez, M.I., Varo, N., Matesanz, C., Ramo, C., Amat, J.A. & Green, A.J. (2013b). Cestodes change the isotopic signature of brine shrimp, Artemia, hosts: implications for aquatic food webs. International Journal for Parasitology, 43(1), 73-80. DOI: 10.1016/j.ijpara.2012.11.003
  • 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). Arch. Hydrobiol. 2006, 166, 199-223. DOI: 10.1127/0003-9136/2006/0166-0199
  • Schuster, R.K. (2018). The role of Artemia spp.(Branchiopoda: Artemiidae) as intermediate hosts for avian cestodes. Environmental Analysis and Ecological Studies, 1(4). DOI: 10.31031/EAES.2018.01.000518
  • Serrão, C. & Marques-Santos, L.F. (2023). The genus Artemia, the nanoplastics, the microplastics, and their toxic effects: a review. Environmental Science and Pollution Research, 1-26. DOI: 10.1007/s11356-023-27868-4
  • Sivaji, S. (2016). Evaluation of different feeds for the culture of Artemia parthenogenetica. Advance Research Journal of Medical and Clinical Sciences, 2(3), 8-14. DOI: 10.52845/arjmcs.v2i3.20
  • Sivakumar, S., Hyland, K. & Schuster, R.K. (2020). Tapeworm larvae in Artemia franciscana (Crustacea: Anostraca) in the Godolphin lakes of Dubai (United Arab Emirates) throughout an annual cycle. Journal of helminthology, 94, e5. DOI: 10.1017/S0022149X18000913
  • Van Stappen, G., Sui, L., Hoa, V.N., Tamtin, M., Nyonje, B., de Medeiros Rocha, R., Sorgeloos, P. & Gajardo, G. (2020). Review on integrated production of the brine shrimp Artemia in solar salt ponds. Reviews in Aquaculture, 12(2), 1054- 1071. DOI: 10.1111/raq.12371
  • Varo, N., Green, A.J., Sánchez, M.I., Ramo, C., Gómez, J. & Amat, J.A. (2011). Behavioural and population responses to changing availability of Artemia prey by moulting black-necked grebes, Podiceps nigricollis. Hydrobiologia, 664, 163- 171. DOI: 10.1007/s10750-010-0596-x
  • Wang, Y.T., Shi, C.Y., Sui, L.Y., Ye, S.G., Dong, X. & Huang, J. (2020). Research progress on the risk of Artemia acting as a kind of live feed to spread shrimp pathogens (in Chinese). China Anim Health Inspect 37, 61-67. DOI: 10.3969/j.issn.1005-944X.2020.11.013
There are 31 citations in total.

Details

Primary Language English
Subjects Veterinary Parasitology
Journal Section Articles
Authors

Ezgi Dinçtürk 0000-0002-5826-2383

Tevfik Tansel Tanrıkul 0000-0002-1684-7965

Early Pub Date March 19, 2024
Publication Date March 31, 2024
Submission Date February 24, 2024
Acceptance Date March 11, 2024
Published in Issue Year 2024 Volume: 9 Issue: 1

Cite

APA Dinçtürk, E., & Tanrıkul, T. T. (2024). Parasitological investigation of Artemia parthenogenetica: A Cestode case from Ayvalık Saltwork. Journal of Anatolian Environmental and Animal Sciences, 9(1), 94-99. https://doi.org/10.35229/jaes.1442106


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