The establishment of the non-indigenous cyclopoid copepod Oithona davisae in Hamsilos Bay-Sinop, Southern Black Sea, Turkey

Abstract

Hamsilos Bay, which is located within the first–degree natural protection area, is one of the most important regions on the southern Black Sea coast. Moreover, many fish species utilize this area for breeding and rearing activities. Small copepod Oithona davisae has been encountered in the Black Sea for two decades and spread rapidly the overall Black Sea, and become an important component in the pelagic ecosystem of the Black Sea. In this respect, the present study aims to characterize the distribution and abundance of Oithona davisae in Hamsilos Bay about environmental variables. Zooplankton samples were collected monthly from seven stations from July 2015 to June 2016 by using a plankton net with a mesh size of 112 μm and a diameter mouth opening of 50 cm. O. davisae was observed during the whole sampling period and was the dominant species from July 2015 to December 2015. The highest mean abundance of this species was recorded in September 2015 (3533.33 ind. m–3). However, the lowest mean abundance was observed between January 2016 (170.68 ind. m–3) and May 2016 (0.24 ind. m–3). Copepodites 5–4 were predominant in the O. davisae population in all months and all stations. Adult copepods and their copepodites 5–4 were more abundant between July 2015 and December 2015, whereas the abundance of copepodites 3–1 was maximum between September 2015 and December 2015. The abundance of O. davisae was highly correlated with chlorophyll-α and physiochemical variables (temperature, dissolved oxygen, and salinity). In conclusion, this species, which is known to be distributed only in the autumn conditions in close areas, extended its temporal distribution and prevailed in the copepod communities during warmer periods. This could be attributed to the acclimatization success of this species in Hamsilos Bay ecosystems.

Keywords

• Oithona davisae
• non-native
• invasive species
• abundance
• developmental stages
• physiochemical variables

References

1. Akkan, E. (1975). Sinop Yarımadasının jeomorfolojisi. Ankara University Publisher, Ankara, Turkey, (in Turkish). google scholar
2. Altukhov, D.A., Gubanova, A.D. & Mukhanov, V.S. (2014). New invasive copepod Oithona davisae Ferrari and Orsi, 1984: seasonal dynamics in Sevastopol Bay and expansion along the Black Sea coasts. Marine Ecology an Evolutionary Perspective, 35 (Supplement s1), 28-34. https://doi.org/10.1111/maec.12168. google scholar
3. Anonymous, (2018). Ministry of forestry and water affairs (Orman ve Su Işleri Bakanligi), general directorate of nature conservation and National Parks (Doga Koruma ve Milli Parklar Genel Müdürlügü). http://hamsilos.tabiat.gov.tr/ (accessed 15 February 2018). (in Turkish). google scholar
4. Brog, M.A. (2009). Non-indigenous zooplankton - the role of predatory cladocerans and of copepods in trophic dynamics. [PhD thesis] University of Stockholms, Stockhol, Sweden. google scholar
5. Doğan, G. & İşinibilir Okyar, M. (2016). First report of a new invasive species Oithona davisae Ferrari and Orsi, 1984 (Copepoda: Cyclopoida) in the Sea of Marmara. Turkish Journal of Fisheries and Aquatic Sciences, 16, 469-473. https://doi.org/10.4194/1303-2712-v16_2_27. google scholar
6. Ersoy Karaçuha, M. (2006). Sinop Yarımadası kıyıları Zostera fasieslerinin Crustacea (Arthropoda) faunası ve ekolojik özellikleri (Crustacea (Arthropoda) fauna of Zostera facies in Sinop Peninsula coasts and their bioecological features). [Master’s Thesis] University of Ondokuz Mayıs, Samsun, Turkey (Turkish with English Abstract). google scholar
7. Ferrari, F.D. & Orsi, J. (1984). Oithona davisae, new species, and Limnoithona sinensis (Burckhardt, 1912) (Copepoda: Oithonidae) from the Sacramento-san Joaquin Estuary, California. Journal of Crustacean Biology, 4(1), 106-126. google scholar
8. Gubanova, A. & Altukhov, D. (2007). Establishment of Oithona brevicornis Giesbrecht, 1892 (Copepoda: Cyclopoida) in the Black Sea. Aquatic Invasions, 2, 407-410. doi: 10.3391/ai.2007.2.4.10. google scholar

9. Gubanova, A., Altukhov, D., Stefanova, K., Arashkevich, E., Kamburska, L., Prusova, I., Svetlichny, L., Timofte, F. & Uysal, Z. (2014). Species composition of Black Sea marine planktonic copepods. Journal of Marine System, 135, 44-52. google scholar
10. Hubareva, E.S. & Svetlichny, L.S. (2016). Copepods Oithona similis and Oithona davisae: Two strategies of ecological-physiological adaptation in the Black Sea. Oceanology, 56(2), 241-247. google scholar
11. Khanaychenko, A., Mukhanov, V., Aganesova, L., Besiktepe, S. & Gavrilova, N. (2018). Grazing and feeding selectivity of Oithona davisae in the Black Sea: Importance of cryptophytes. Turkish Journal of Fisheries and Aquatic Sciences, 18, 937-949. http://doi. org/10.4194/1303-2712-v18_8_02. google scholar
12. Lee, C.E., Remfert, J.L. & Gelembiuk, G.W. (2003). Evolution of physiological tolerance and performance during freshwater invasions. Integrative and Comparative Biology, 43(3), 439-449. https://doi.org/10.1093/icb/43.3.439. google scholar
13. Leidenberger, S., Obst, M., Kulawik, R., Stelzer, K., Heyer, K., Hardisty, A. & Bourlat, S.J. (2015). Evaluating the potential of ecological niche modelling as a component in marine non-indigenous species risk assessments. Marine Pollution Bulletin, 97, 470-487. google scholar
14. Lougee, L.A., Bollens, S.M. & Avent, S.R. (2002). The effects of haloclines on the vertical distribution and migration of zooplankton. Journal of Experimental Marine Biology and Ecology, 278, 111-134. https://doi. org/10.1016/S0022-0981(02)00326-X google scholar
15. Mihneva, V. & Stefanova, K. (2013). The non-native copepod Oithona davisae (Ferrari FD and Orsi, 1984) in the Western Black Sea: seasonal and annual abundance variability. Bioinvasions Records, 2(2), 119124. http://dx.doi.org/10.3391/bir.2013.2.2.04. google scholar
16. Parsons, T.R., Maita, Y. & Lalli, C.M. (1984). A manual of chemical and biological methods for seawater analysis. Oxford, United Kingdom. google scholar
17. Razouls, C., Desreumaux, N., Kouwenberg, J. & de Bovee, F. (2023). Biodiversity of Marine Planktonic Copepods (morphology, geographical distribution and biological data). Sorbonne University, CNRS. http://copepodes.obs-banyuls.fr/en (accessed 09 March 2023). google scholar
18. Saiz, E., Calbet, A., Broglio, E. & Marı, P. (2003). Effects of small-scale turbulence on copepods: The case of Oithona davisae. Limnology and Oceanography, 48(3), 1304-1311. https://doi.org/10.4319/ lo.2003.48.3.1304. google scholar
19. Selifonova, Z.P. (2011a). Ships’ ballast as a primary factor for ‘Mediterraneanization’ of pelagic copepod fauna (Copepoda) in the Northeastern Black Sea. Acta Zoologica Bulgarica, 63(1), 77-83. google scholar
20. Selifonova, Z.P. (2011b). Oithona brevicornis Giesbrecht (Copepoda: Cyclopoida), invader into the Black Sea and in the Sea of Azov. Russian Journal of Biological Invasions, 2(2-3), 227-232. http://dx. doi.org/10.1134/s2075111711030131. google scholar
21. Seregin, S.A. & Popova, E.V. (2016). Long-term dynamics of the copepod invader Oithona davisae in coastal waters of the Black Sea. Russian Journal of Biological Invasions, 7(4), 374-382. https://doi.org/10.1134/ s207511171604007x. google scholar
22. Shiganova, T.A. (1998). Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure. Fisheries Oceanography, 7, 305-310. https://doi. org/10.1046/j.1365-2419.1998.00080.x. google scholar
23. Shvelidze, T. (2016). First record of Oithona davisae Ferrari and Orsi, 1984 (Copepoda, Cyclopoida) and seasonal variations in the Georgian Black Sea coast. Academia Journal of Scientific Research, 4(11), 424428. doi: 10.15413/ajsr.2016.0141. google scholar
24. Svetlichny, L. & Hubareva, E. (2014). Salinity tolerance of alien copepods Acartia tonsa and Oithona davisae in the Black Sea. Journal of Experimental Marine Biology and Ecology, 461, 201-208. http://dx. doi.org/10.1016/j.jembe.2014.08.012. google scholar
25. Svetlichny, L., Hubareva E., Khanaychenko A., Gubanova A. & Besiktepe, S. (2016). Adaptive strategy of thermophilic Oithona davisae in the cold Black Sea environment. Turkish Journal of Fisheries and Aquatic Sciences, 16(1), 77-90. https://doi.org/10.4194/1303-2712-v16_1_09. google scholar
26. Svetlichny, L., Hubareva, E. & İşinibilir, M. (2018). Population dynamics of the copepod invader Oithona davisae in the Black Sea. Turkish Journal of Zoology, 42(6), 684-693. https://doi.org/10.3906/zoo-1804-48. google scholar
27. Takahashi, T. & Uchiyama, I. (2007). Morphology of the naupliar stages of some Oithona species (Copepoda: Cyclopoida) occurring in Toyama Bay, southern Japan Sea. Plankton Benthos Research, 2(1), 12-27. https://doi.org/10.3800/pbr.2.12. google scholar
28. Temnykh, A. & Nishida, S. (2012). New record of the planktonic copepod Oithona davisae Ferrari and Orsi in the Black Sea with notes on the identity of “Oithona brevicornis”. Aquatic Invasions, 7(3), 425-431. doi: http://dx.doi.org/10.3391/ai.2012.7.3.013. google scholar
29. Terbıyık Kurt, T. & Beşiktepe, Ş. (2019). First distribution record of the invasive copepod Oithona davisae Ferrari and Orsi, 1984, in the coastal waters of the Aegean Sea. Marine Ecology, 40(3), e12548. https://doi.org/10.1111/maec.12548. google scholar
30. Terbıyık-Kurt, T., Polat, S. & Guy-Haim, T. (2022). New invasive copepod species from the Levantine Sea, north-eastern Mediterranean: Oithona davisae (Ferrari and Orsi, 1984) (Cyclopoida: Oithonidae). Bioinvasions Records, 11(1), 215-226. https://doi.org/10.3391/ bir.2022.11.1.22. google scholar
31. Timofte, F. & Tabarcea, C. (2012). Oithona brevicornis Giesbrecht, 1892 (Copepoda: Cyclopoida)-First record in the Romanian Black Sea waters. Journal of Environmental Protection and Ecology, 13(3A), 1683-1687. google scholar
32. Uchima, M. (1988). Gut content analysis of neritic copepods Acartia omorii and Oithona davisae by a new method. Marine Ecology Progress Series, 48, 93-97. https://doi.org/10.3354/meps048093. google scholar
33. Uriarte, I., Villate, F. &, Iriarte, A. (2016). Zooplankton recolonization of the inner estuary of Bilbao: influence of pollution abatement, climate and non-indigenous species. Journal of Plankton Research, 38(3), 718-731. https://doi.org/10.1093/plankt/fbv060. google scholar
34. Uye, S. & Sano, K. (1995). Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series, 118, 121-128. https://doi. org/10.3354/meps118121. google scholar
35. Uygun, O. (2015). Balık larvalarının Sinop-Akliman kıyılarındaki kompozisyonu (Composition of fish larvae in Sinop-Akliman coast of the Black Sea). [Master’sThesis] University of Sinop, Sinop, Turkey (Turkish with English Abstract). google scholar
36. Ünlülata, Ü., Oğuz, T., Latif, M.A. & Özsoy, E. (1990). On the Physical Oceanography of the Turkish Straits. In Pratt, L.J. (Eds.), The Physical Oceanography of Sea Straits (pp. 25-60). NATO ASI Series, vol 318. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-0677-8_2. ISBN : 978-94-010-6789-8. google scholar
37. Üstün, F. &, Terbiyik Kurt, T. (2016). First report of the occurrence of Oithona davisae Ferrari F. D. & Orsi, 1984 (Copepoda: Oithonidae) in the southern Black Sea, Turkey. Turkish Journal of Fisheries and Aquatic Sciences, 16(2), 413-420. https://dx.doi.org/ 10.4194/1303-2712-v16_2_21. google scholar
38. Üstün, F. (2019). Seasonal cycle of zooplankton abundance and biomass in Hamsilos Bay, Sinop, Southern Black Sea, Turkey. Journal of Natural History, 53(7-8), 365-389. https://doi.org/10.1080/00222933.2019.159 2257. google scholar
39. Üstün, F., Bat L. & Şahin F. (2019). Composition, abundance and biomass of mesozooplankton in the southwestern Black Sea along the coast of İğneada, Turkey. Biologia 74, 851-862. https://doi.org/10.2478/ s11756-019-00219-w. google scholar
40. Üstün, F. & Birinci Özdemir, Z. (2019). Seasonal distribution of gelatinous macrozooplankton in the Hamsilos Bay, Southern Black Sea, Turkey. KSU Journal of Agriculture and Nature, 22(4), 583-592. https://doi. org/10.18016/ksutarimdoga.vi.511807 google scholar
41. Yıldız, İ., Feyzioglu, A.M. & Besiktepe, S. (2017). First observation and seasonal dynamics of the new invasive planktonic copepod Oithona davisae Ferrari and Orsi, 1984 along the southern Black Sea (Anatolian Coast). Journal of Natural History, 51(3-4), 127-139. http:// dx.doi.org/10.1080/00222933.2016.1229060. google scholar
42. Yildiz, İ. & Feyzioğlu, A.M. (2020). Spatial and seasonal variation of the new invader Oithona davisae (Ferrari F. D. & Orsi, 1984) (Cyclopoida: Oithonidae) in the Southeast Black Sea. Acta Zoologica Bulgarica, 72(4), 517-524. google scholar
43. Zagorodnyaya, Y.A. (2002). Oithona brevicornis in the Sevastopol Bay: is it a single event or a new invader in the Black Sea Fauna? Marine Ecology Journal (Morskyj Ecologichny Journal), 61, 43. (in Russian). google scholar