Cestode Infection of the Native Brine Shrimp (Artemia parthenogenetica) in Çamaltı Saltpan (İzmir/Türkiye)

Yıl 2022, Cilt: 5 Sayı: 1, 56 - 66, 20.07.2022

Edis Koru

https://doi.org/10.46384/jmsf.1084680

Cited By: 2

Öz

Artemia sp. populations in saltworks throughout the world have been gaining importance due to their extensive use in aquaculture and their importance as the main prey organism for aquatic birds in hypersaline ecosystems. The genus Artemia sp. is also known as the intermediate host of some cestode species that are associated with flamingos. In this study, Flamingolepis liguloides parasitism was determined in Artemia partenogenetica for the first time in Turkiye. Infected A. parthenogenetica was detected in İzmir Çamaltı saltpans between May-August 2018 and the parasite diagnosis was made. Parasites were detected near the abdomen, thorax and the intestinal tract of A. parthenogenetica. The prevalence of parasites was higher in adult Artemia (63.6%). The presence of F. liguloides in A. parthenogenetica was very high with a frequency of 72.2%. The most abundant and prevalent parasite infection was recorded in July which is the most suitable time of the year with respect to number of flamingos in the area. The results show the prevalence of this parasite infection in A. parthenogenetica, which may be important for both the local Artemia population in the area and the flamingos breeding in Çamaltı saltpans.

Anahtar Kelimeler

Aquaculture, Artemia parthenogenetica, Çamaltı saltpan, Flamingolepis liguloides, Live feeds, Parasitism

Destekleyen Kurum

Binbir Gıda Tarım Ürünleri Sanayi ve Ticaret A.Ş. İzmir Çamaltı Tuzlası.

Teşekkür

The author is grateful to Binbir Gıda Tarım Ürünleri Sanayi ve Ticaret A.Ş. İzmir Çamaltı Tuzlası, and Prof. Dr. T. Tansel Tanrıkulu, Research Asst. Ezgi Dinçtürk for valuable information and suggestions in the preparation of this manuscript and doctoral candidate Mehmet Deniz from Lancaster University Department of Politics, Philosophy & Religion Lancester United Kingdom LA1 4YL for editing this manuscript.

Çamaltı Tuzlası’nda (İzmir/Türkiye) Yerli Tuzla Karidesinde(Artemia parthenogenetica) Görülen Sestod Enfeksiyonu

Öz

Tuzlalardaki Artemia sp. popülasyonları, akuakültürde kullanımı ve çok tuzlu ekosistemlerde su kuşlarının besini olmasına göre önem kazanmaktadır. Ayrıca bu besin zincirinde Artemia, flamingo kuşları ile ilgili olarak bazı sestod türlerinde ara konakçıdır. On iki ay süren bu çalışmada Türkiye'de ilk kez Artemia partenogenetica'da Flamingolepis liguloides parazitliği saptanmıştır. Mayıs-Ağustos 2018 tarihleri arasında İzmir Çamaltı Tuzlasında enfekte olan A. parthenogenetica tespit edilmiş ve parazitin teşhisi konmuştur. Parazit, A. parthenogenetica' nın karın, göğüs kafesi ve bağırsak kanalı yakınında tespit edilmiştir. Parazitlerin yayılımı çoğunlukla erişkin bireylerde (%63,3) oranında daha yüksektir. Tuzla havuzlarında, F. liguloides varlığı %72,2 gibi oldukça yüksek bulunmuştur. En bol ve yaygın parazit enfeksiyonu, ekosistemdeki birey sayısı için yılın en uygun zamanı olan temmuz ayında kaydedilmiştir. Elde edilen sonuçlara göre, flamingo kuşlarının çok önemli bir göç noktası olan bu bölgede A. parthenogenetica' da bu parazit enfeksiyonunun yaygınlığı görülmektedir. A. parthenogenetica, bu sestodların parazitleştirdiği ara konaktır. Bu sonuç Türkiye'deki birincil tespittir.

Anahtar Kelimeler

Akuakültür, Artemia parthenogenetica, Çamaltı tuzlası, Flamingolepis liguloides, Canlı yemler, Parazitlik

Kaynakça

• Agh N, Abatzopoulos TJ, Kappas I, Van Stappen G, Razavi Rouhani SM et al. (2007). Coexistence of sexual and parthenogenetic Artemia populations in Lake Urmia and neighboring lagoons. International Review of Hydrobiology, 92(1), 48-60
• Amarouayache M, Derbal F, Kara M (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), 330-334. ISSN 1230-2821, doi: 10.2478/s11686-009-0049-8
• Amat E, Illescas ME, Fernandez J (199la). Brine shrimp Artemia parasitized by Flamingolepis liguloides (Cestoda, Hymenoloepididae) cysticercoids in Spanish Mediterranean salterns. Quantitative aspects. Vie et Milieu 41: 237-244
• Amat F, Gozalbo A, Navarro JC, Hontoria F, Var´o I (1991b). Some aspects of Artemia biology affected by cestode parasitism. Hydrobiology 212, 39–44
• Amat F, Hontoria F, Navarro JC, Vieira N, Mura G (2007). Biodiversity loss in the genus Artemia in the Western Mediterranean Region. Limnetica, 26(2), 387-404
• Anonymous (2019). http://www.visitizmir. org/en/district/ cigli/where-to-visit/-236289
• Balkız Ö, Onmuş O, Sıkı M, Döndürenc Ö, Gül O et al. (2015). Turkey as a crossroad for Greater Flamingos Phoenicopterus roseus: evidence from population trends and ring-resightings (Aves: Phoenicopteridae). Zoology in the Middle East, 61(3), 201-214
• Baxevanis AD, Kappas I, Abatzopoulos TJ (2006). Molecular phylogenetics and asexuality in the brine shrimp Artemia. Molecular phylogenetics and evolution, 40(3), 724-738
• BirdLife International (2004). Birds in Europe: population estimates, trends and conservation status. BirdLife Conservation Series (Cambridge), No. 12, Cambridge, UK.
• Bradley DJ, Forward RBJ (1984). Phototaxis of adult brine shrimp Artemia salina. Can. J. Zool. 62, 2357–2359
• Bray R (2014). Wardium stellorae (Deblock, Biguet & Capron, 1960). In: Costello, M.J.; Bouchet, P.; Boxshall, G.;
• Arvantidis, C.; Appeltans, W. (2014) European Register of Marine Species, accessed through PESI at http://www.eu-nomen.eu/portal/taxon.php?GUID=urn:lsid:marinespecies.org:taxname:105152
• Britton RH, de Groot ER, Johnson AR (1986). The daily cycle of feeding activity of the Greater Flamingo in relation to the dispersion of the prey Artemia. Wildfowl 37, 151–155
• Céspedes V, Sánchez MI, Green AJ (2017). Predator-prey interactions between native brine shrimp Artemia parthenogenetica and the alien boatman Trichocorixa verticalis: influence of salinity, predator sex, and size, abundance and parasitic status of prey. PeerJ, 5, e3554
• Chervy L (2002). The terminology of larval cestodes or metacestodes. Systematic Parasitology, 52: 1-33. Combes C (1996). Parasites, biodiversity, and ecosystem stability. Biodiversity and Conservation 5.953–962 doi: 10.1007/BF00054413
• Cooper SD, Winkler DW, Lenz PH (1984). The effect of grebe predation on the brine shrimp population. J. Anim. Ecol. 53: 51–64
• Curio E (1988). Behavior and parasitism. In: (Ed. Mehlhorn) Parasitology in Focus. Springer-Verlag, New York, pp. 149–160.
• Di Cave D, Cirillo L, Dettori C, Mura G (1990). Artemia salina e Branchinella spinosa (Crustacea, Anostraca) ospiti intermedi di Flamingolepis liguloides. Congresso Societa italiana di Parassitologia, Cagliari
• Di Cave D, Mura G (1990). Flamingolepis liguloides parasite sur Artemia salina et Branchinella spinosa des milieux mesohalines et hyperalines de Sardaigne (Italie). Septieme Congres International de Parasitologie, Paris: pp. 288
• Dobbeleir J, Adam N, Bossuyt E, Bruggeman E, Sorgeloos P (1980). New aspects of the use of inert diets for high density culturing of brine shrimp. In: Persoone G, Sorgeloos P, Roels O, Jaspers E (editors). The Brine Shrimp Artemia. Ecology, Culturing, Use in Aquaculture. Vol. 3. Universa Press. Wetteren Belgium: pp. 165–174.
• Forward RB, Hettler WF (1992). Effects of feeding and predator exposure on photoresponses during dial vertical migration of brine shrimp larvae. Limnol. Oceanogr. 37: 1261–1270.
• Fuhrmann O (1936). Gynandrotaenia stammeri nov. gen. nov. Spec, Revue suisse de zoologie, Vol. 43, N0: 20, pg. 517-518. ISSN: 0035-418X doi: 10.5962/bhl.part.117685
• Gabrion C, MacDonald G (1980). Artemia sp. (Crustacé Anostracé), hote intermrdiaire d'Eurycestus avoceti Clarc, 1954 (Cestode, Cyclophyllidr). Annales de Parasitologie 55: 327-331.
• Gajardo G, Abatzopoulos TJ, Kappas I, Beardmore JA (2002). Evolution and speciation. In Abatzopoulos T.J, Beardmore J., Clegg J.S, Sorgeloos, P (editors). Artemia: Basic and Applied Biology Springer, Dordrecht: pp. 225-250.
• Gajardo MG, Beardmore AJ (2012). The brine shrimp Artemia: adapted to critical life conditions. Frontiers in Physiology Vol: 3, 185. doi: 10.3389/fphys.2012.00185.
• Georgiev BB, Sánchez MI, Green AJ, Nikolov PN, Vasileva GP et al. (2005). Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: a systematic survey of cysticercoids. Acta Parasitologica, 50 (2): 105-117
• Georgiev BB, Sánchez MI, Vasileva GP, Nikolov PN, Green AJ (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): 1647-1655
• Gvozde EV, Maximov AP (1968). New species of tapeworms (Cestoda: Hymenolepididae) from pink flamingo (Phoenicopterus roseus Pall.), Izv. Academy of Sciences of the Kazakh SSR, sir. Biol., Alma-Ata, 5: 30—37
• Hand SC, Denlinger DL, Podrabsky JE, Roy R (2016). Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 310(11), R1193-R1211
• Heldt H (1926). Sur la présence d'un cysticercoide chez Artémia salina L. Bulletin de la Station Oceanographique Salammbo 5: 3-8
• Helluy S, Holmes JC (2005). Parasitic manipulation: further considerations. Behavioural Processes, 68, 205–210. DOI: 10.1016/ j.beproc.2004.08.011
• Koru, E (2013). The potential of Artemia Population in Çamaltı Saltworks (Sasalı-İzmir) at Aquaculture, Menba Journal of Fisheries Faculty, Vol.2, 30-40, ISSN: 2147-2254 (in Turkish with an abstract in English).
• Koru E, Deniz, M (2017). The seasonal changes and algal flora of Çamaltı Saltworks (Sasalı / İzmir). Ege Journal of Fisheries and Aquatic Sciences, 34(4): 431-442. doi: 10.12714/egejfas.2017.34.4.10 2254 (in Turkish with an abstract in English).
• Koru E, Perçin F (2018). Characteristics of Biological Systems in Çamaltı Solar Saltworks (İzmir/Turkey), Qualitative Studies (NWSAQS), 13(3):15-25, doi: 10.12739/NWSA.2018.13.3.E0036
• Lenz PH (1980). Ecology of an alkali adapted variety of Artemia from Mono Lake, California, U.S.A. In: Persoone, G., Sorgeloos, P., Roels, O., Jaspers, E. (Eds.), The Brine Shrimp Artemia, Vol. III. Universa Press, Wetteren, Belgium
• Maksimova A.P. (1976). A new cestode, Fimbriarioides tadornae sp. n., from Tadorna tadorna and its development in the intermediate host. Parazitologiya, 10: 17–24 (In Russian).
• 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, 3(2), 191-200.
• Prenter J, MacNeil C, Dick JT, Dunn AM (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution 19:385–390. doi: 10.1016/j.tree.2004.05.002.
• Provasoli L, Shiraishi K (1959). Axenic cultivation of the brine shrimps Artemia salina. Biol. Bull. 117, 347–35.5
• 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), 226-235
• Rode NO, Landes J, Lievens EJ, Flaven E, Segard et. al. (2013). Cytological, molecular and life cycle characterization of Anostracospora rigaudi ng, n. sp. and Enterocytospora artemiae ng, n. sp., two new microsporidian parasites infecting gut tissues of the brine shrimp Artemia. Parasitology 140 (9): 1168-1185.
• Rode NO, Lievens EJ, Flaven E, Segard A, Jabbour‐Zahab R et al. (2013). Why join groups? Lessons from parasite‐manipulated Artemia. Ecology letters 16 (4): 493-501.
• Rolf KS (2018). The Role of Artemia spp (Branchiopoda: Artemiidae) as Intermediate Hosts for Avian Cestodes. Environ Anal Eco stud. 1(4): EAES.000518.2018. doi: 10.31031/EAES.2018.01.0005183/3
• Sánchez MI, Green AJ, Castellanos EM, (2006). Temporal and spatial variation of an aquatic invertebrate community subjected to avian predation at the Odiel salt pans (SW Spain). Arch. Hydrobiol. 166, 199–223.
• Sánchez MI, Georgiev BB, Green AJ (2007). Avian cestodes affect the behavior of their intermediate host Artemia parthenogenetica: an experimental study. Behavioural Processes 74 (3): 293-299.
• Sánchez MI, Varo N, Matesanz C, Ramo C, Amat JA et al. (2013). Cestodes change the isotopic signature of brine shrimp, Artemia, hosts: implications for aquatic food webs. International Journal for Parasitology 43 (1): 73-80.
• Sánchez MI, Paredes I, Lebouvier M, Green AJ (2016). Functional role of native and invasive filter-feeders, and the effect of parasites: learning from hypersaline ecosystems. PloS one 11 (8): e0161478.
• Savage A, Knott B (1998). Artemia parthenogenetica in Lake Hayward, Western Australia. II. Feeding biology in a shallow, seasonally stratified, hypersaline lake. Int. J. Salt Lake Res. 7: 13–24.
• Thiéry A, Robert F, Gabrion C (1990). Distribution des populations d'Artemia et de leur parasite Flamingolepis liguloides (Cestoda, CyclophylIidea), dans les salins du littoral mediterraneen Francais. Canadian Journal of Zoology 68: 2199-2204.
• Thomas F, Cezilly F, De Meeüs T, Crivelli A, Renaud F (1997). Parasitism and Ecology of Wetlands: a review. Estuaries. 20: 646–654. doi: 10.2307/1352622.
• Torchin ME, Mitchell CE. (2004). Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and the Environment 2: 183–190 doi: 10.1890/1540-9295(2004)002[0183:PPAIBP]2.0.CO;2.
• Triantaphyllidis GV, Abatzopoulos TJ, Sorgeloos P (1998) Review of the biogeography of the genus Artemia (Crustacea, Anostroca). Journal of Biogeography 25: 213–226, http://dx.doi.org/10.1046/j.1365-2699.1998.252190.x
• Vanhaecke P, Tackaert W, Sorgeloos P (1987). The biogeography of Artemia: an updated review. In: Sorgeloos P, Bengtson DA, Decleir W, Jaspers E (editors). Artemia Research and its Applications. Vol. 1. Wetteren, Belgium: Universa Press, pp. 129–155.
• Vasileva GP, Redón S, Amat F, Nikolov PN, Sánchez MI et al. (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 spp. from the Western Mediterranean. Acta Parasitologica 54 (2): 143-150.
• Verkuil Y, van der Have TM, van der Winden J, Chernichko I.I (2003). Habitat use and diet selection of northward migrating waders in the Sivash (Ukraine): the use of brine shrimp Artemia salina in a variably saline lagoon complex. Ardea Vol. 91, Issue Number: 1, pp. 71-83.