Ecological Changes in the Sea of Marmara

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DOI :10.26650/B/LSB21LSB37.2024.023.015   IUP :10.26650/B/LSB21LSB37.2024.023.015    Full Text (PDF)

Changes in the Zooplankton of the Eastern Sea of Marmara

Melek İşinibilir, Ezgi Türkeri, Nur Eda Topçu Eryalçın, Leonid Svetlıchny, Ahmet Erkan Kıdeyş

 The study conducted in the eastern Sea of Marmara from 2016 to 2022 aimed to investigate the spatio-temporal distributions of mesozooplankton in relation to changing environmental conditions. A total of 43 zooplankton taxa were identified, with the number of species varying between 4 and 19 in the brackish upper layer (resembling the Black Sea) and between 1 and 17 in the saline lower layer (resembling the Mediterranean Sea). The abundances of zooplankton ranged from 28 to 43,359 ind.m-3 in the upper layer and from 5 to 3,851 ind.m-3 in the lower layer. Significant differences were observed between the upper and lower layers in terms of the number of species, total zooplankton abundances, evenness, and Shannon diversity (p<0.0001). The most significant differences in zooplankton abundance and community structure were found to be seasonal rather than inter-year or regional variations. The highest total zooplankton abundance was recorded at station M14 during the summer season (June 2022), primarily due to the presence of Paracalanus parvus and Penilia avirostris (906 ind.m-3 and 722 ind.m-3, respectively). The heterotrophic dinoflagellate Noctiluca scintillans, a major component of net samples in the Sea of Marmara, exhibited a clear seasonal distribution, with higher abundances consistently observed during winter months. The highest abundance of Noctiluca scintillans was recorded in February 2016 at station MD102 (42,514 ind.m-3). Paracalanus parvus, Acartia clausi, and Oithona nana were identified as important year-round species in both the upper and lower layers of the Sea of Marmara. The presence of N. scintillans and P. avirostris distinguished the upper layer communities from the lower layer, with N. scintillans being more prevalent during winter and P. avirostris during summer. Notably, P. avirostris exhibited very low abundances during the summers of 2019, 2021, and 2022. The large-scale mucilage event that occurred in June 2021 had a significant impact on zooplankton, as evidenced by the low abundance and biomass observed during this period. The chlorophyll-a values, which reflect phytoplankton biomass, increased sharply during the dominating mucilage event, ranging from 12.2 to 14.2 µg.l-1. Overall, this study emphasizes the vulnerability of the Sea of Marmara ecosystem, particularly zooplankton, to large-scale environmental disturbances such as mucilage events.


Keywords: Marmara, zooplankton, changes, mucilage, Noctiluca scintillans, Penilia avirostris

References

  • Aktan, Y., Dede, A., & Çiftçi, P. S. (2008). Mucilage event associated with diatoms and dinoflagellates in the Sea of Marmara, Turkey. Harmful Algae News. google scholar
  • APHA (2000). Standard methods for the examination of water and wastewater 20th Edition. Clesceri, L.S., A.E Greenberg and A.D Eaton (eds). American Public Health Association, American Water Works Association and Water Environment Federation. Washington, D.C. google scholar
  • Balkıs, N., & Toklu-Alıçlı, B. (2014). Changes in phytoplankton community structure in the Gulf of Bandirma, Marmara Sea in 2006-2008. google scholar
  • Balkıs-Ozdelice, N., Durmuş, T., & Balcı, M. (2021). A preliminary study on the intense pelagic and benthic mucilage phenomenon observed in the Sea of Marmara. International Journal of Environment and Geoinformatics, 8(4), 414-422. google scholar
  • Batchelder, H.P., Daly, K.L., Davis, C.S., Ji, R., Ohman, M.D., Peterson, W.T., Runge, J.A., (2013). Climate impacts on zooplankton population dynamics in coastal marine ecosystems. Oceanography 26, 34-51. google scholar
  • Cataletto, B., Feoli, E., Umani, S. F., Monti, M., & Pecchiar, I. (1996). Analyses of the relationship between mucous aggregates and phytoplankton communities in the Gulf of Trieste (Northern Adriatic Sea) by multivariate techniques. Marine Ecology, 17(1-3), 291-307. google scholar
  • Clarke, K.R. & Gorley R.N. (2006). PRIMER-E v6: User Manual/Tutorial. PRIMER-E, Plymouth. google scholar
  • Coma, R., Ribes, M., Serrano, E., Jimenez, E., Salat, J., & Pascual, J. (2009). Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proceedings of the National Academy of Sciences, 106(15), 6176-6181. google scholar
  • Çevik C., Kideys, A. E., Tavşanoğlu, Ü. N., Kankılıç, G. B. & Gündoğdu, S. (2022). A review of plastic pollution in aquatic ecosystems of Turkey. Environmental Science & Pollution Research 29: 26230-26249 (https:// doi.org/10.1007/s11356-021-17648-3). google scholar
  • Dogan, G., & Isinibilir, 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(2), 471-475. doi:10.4194/1303-2712-v16_2_27 google scholar
  • Ediger, D., Beken, Ç., Yüksek, A., & Tuğrul, S. (2016). Eutrophication in the Sea of Marmara. In E. Özsoy, M. N. Çağatay, N. Balkıs, N. Balkıs, & B. Öztürk (Eds.), The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance (Vol. 42, pp. 390-400). İstanbul: Turkish Marine Research Foundation (TUDAV). google scholar
  • Egloff, D.A., Fofonoff, P.W., Onbe, T. (1997) Reproductive biology of marine cladocerans. Advances in Marine Biology 31, 79-167. google scholar
  • Eker-Develi E. & A.E. Kideys 2022. First record of the diatom Nitzschia navis-varingica in the Sea of Marmara. Marine Science and Technology Bulletin, 11(2), 231-235. google scholar
  • Eker-Develi E., D. Tekdal, A. E. Demet, H. B. Yıldız and A. E. Kideys (2023). Morphology, molecular genetics and potential importance for mucilage events of the new coccolithophorid Ochrosphaera neapolitana in the Sea of Marmara. Journal of Marine Science and Engineering, 11(3), 468; https://doi.org/10.3390/ jmse11030468 google scholar
  • Fernandez de Puelles M, Gras D, Hernandez-Leon S. (2003). Annual cycle of zooplankton biomass, abundance and species composition in the neritic area of the Balearic Sea, Western Mediterranean. Marine Ecology 24:123-39. google scholar
  • Fonda Umani S, Milani L, Borme D, Olazabal A, Parlato S, Precali R, Kraus R, Lucic D, Njire J, Totti C et al. (2005). Inter-annual variations of planktonic food webs in the northern Adriatic Sea. Sci Total Environ 353: 218-231. google scholar
  • Gubanova A.D., Altukhov D.A., Stefanova K., Arashkevich E.G., Kamburska L., Prusova I.Y., Svetlichny L.S., Timofte F., & Uysal Z. (2014). Species composition of Black Sea marine planktonic copepods. Journal of Marine Systems, 135, 44-52. google scholar
  • Gubanova, A. D., Prusova, I. Y., Niermann, U., Shadrin, N. V., & Polikarpov, I. G. (2001). Dramatic change in the copepod community in Sevastopol Bay (Black Sea) during two decades (1976-1996). Senckenbergiana Maritima, 31(1), 17-27. doi:10.1007/bf03042833 google scholar
  • Hays, G.C., Richardson, A.J. & Robinson, C., 2005. Climate change and marine plankton. Trends Ecol. Evol. 20, 337-344. google scholar
  • Holm, M.W., Kİ0rboe, T., Brun, P., Licandro, P., Almeda, R., Hansen, B.W. (2018) Resting eggs in free living marine and estuarine copepods. Journal of Plankton Research 40, 2-15. google scholar
  • Hubareva E., Svetlichny, L., Kideys, A. E. & Isinibilir, M. (2008). Fate of the Black Sea Acartia clausi and Acartia tonsa (Copepoda) penetrating into the Marmara Sea through the Bosphorus. Estuarine, Coastal & Shelf Science 76(1): 131-140. google scholar
  • Inanmaz, Ö., Bekbolet, I., M. & Kideys, A. E. (2003). A new scyphozoan species in the Sea of Marmara: Chrysaora hysoscella (Linne, 1766). In: Oceanography of Eastern Mediterranean and Black Sea - Similarities and Differences of Two Interconnected Basins (Ed. A. Yilmaz), TUBITAK Publishers, Ankara, Turkey, pp.857-859. google scholar
  • Isinibilir, M., Tarkan, A.N., Kideys, A.E. & Yilmaz, I.N. (2008). Annual cycle of zooplankton abundance and species composition in Izmit Bay (the northeastern Marmara Sea). Estuarine, Coastal & Shelf Science 78 739-747. google scholar
  • Isinibilir, M. (2009). Annual crustacean zooplankton succession (Copepoda and Cladocera) in the upper layer of Ahirkapi coastal waters (northeastern Sea of Marmara). Crustaceana, 82(6), 669-678. doi:10.1163/156854008x380273 google scholar
  • Isinibilir, M., Svetlichny, L., Hubareva, E., Ustun, F., Yilmaz, I.N., Kideys, A.E., Bat, L. (2009). Population dynamics and morphological variability of Calanus euxinus in the Black and Marmara Seas. Italian Journal of Zoology 76(4): 403-414. google scholar
  • Isinibilir, M. (2010a). Spatial and temporal variation of zooplankton in two bays in the southern Sea of Marmara. google scholar
  • Crustaceana, 83(2), 233-244. doi:10.1163/001121609x12512848343568 google scholar
  • Isinibilir, M. (2010b). Marmara Denizi zooplanktonunun son yıllardaki değişimi ve müsilaj’ın etkisi. Öztürk B.,Ed. Marmara Denizi 2010 Sempozyumu, TUDAV 2010, p. 469-482 google scholar
  • Isinibilir, M., Svetlichny, L., Hubareva, E., Yilmaz, I. N., Ustun, F., Belmonte, G., & Toklu-Alicli, B. (2011). Adaptability and vulnerability of zooplankton species in the adjacent regions of the Black and Marmara Seas. Journal of Marine Systems, 84(1-2), 18-27. doi:10.1016/j.jmarsys.2010.08.002 google scholar
  • Isinibilir, M., Hubareva, E., & Svetlichny, L. (2014). Interpopulation dynamics between Acartia clausi (Copepoda) and Noctiluca scintillans (Dinoflagellata) in the Bosphorus area of the Black and the Marmara Seas. Italian Journal of Zoology, 81(3), 451-456. doi:10.1080/11250003.2014.942711 google scholar
  • Isinibilir Okyar, M., Üstün, F., & Orun, D. A. (2015). Changes in abundance and community structure of the zooplankton population during the 2008 mucilage event in the northeastern Marmara Sea. Turkish Journal of Zoology, 39(1), 28-38. google scholar
  • Isinibilir M., Svetlichny L., Hubareva E. (2016). Competitive advantage of the invasive copepod Oithona davisae over the indigenous copepod Oithona nana in the Marmara Sea and Golden Horn Estuary. Marine and Freshwater Behavior and Physiology. 49 (6):392-405. google scholar
  • Isinibilir Okyar, M. (2023). Changes in zooplankton populations after mucilage events in the northeastern Marmara Sea. In Mucilage Problem in the Sea of Marmara (Ed. M. Albay), Vol. 5316, pp. 166-175. İstanbul: Istanbul University Press. google scholar
  • Kabasakal, H. (2009). On the occurrence of the bluntnose sixgill shark, Hexanchus griseus (Chondrichthyes: Hexanchidae), in the Sea of Marmara. Marine Biodiversity Records, 2, E110. doi:10.1017/ S1755267209001018 google scholar
  • Kahraman, A. E., Yıldız, T., Uzer, U. & Çanak, Ö. (2021). Growth pattern, mortality and reproductive biology of common sole, Solea solea (Linneaus, 1758), in the Sea of Marmara, Turkey” Oceanological and Hydrobiological Studies, vol.50, no.4, pp.398-410. https://doi.org/10.2478/oandhs-2021-0034 google scholar
  • Kideys A.E. (2013). Marmara denizinin mevcut kirlilik kaynaklari ve yansımalar. Derdimiz, Değerimiz, Denizimiz: MARMARA, Marmara Belediyeler Birliği Yayınları No 79 (Ed A. C. Kahraman). google scholar
  • Kideys A.E., Roohi, A., Eker-Develi, E., Melin, F. & Beare, D. (2008). Increased chlorophyll levels in the southern Caspian Sea following an invasion of jellyfish. Research Letters in Ecology, Volume 2008, Article ID 185642, 4 pages, doi:10.1155/2008/185642. google scholar
  • Kideys A.E., Soydemir, N., Eker, E., Vladymyrov, V., Soloviev, D. & Melin, F. (2005). Phytoplankton distribution in the Caspian Sea during March 2001. Hydrobiologia 543: 159-168. google scholar
  • Kocataş, A., Koray, T., Kaya, M. & Kara, Ö.F. (1993). A rewiev of the fishery resouces and their environment in the Sea of Marmara. In: Studies and Reviews General Fisheries Council for the Mediterranean, FAO, 64, Roma. google scholar
  • Kokal, A. T., Ismailoglu, I., Musaoglu, N. & Tanik, A. (2023). Detection of surface temperature anomaly of the Sea of Marmara, Advances in Space Research, Volume 71, Issue 7, google scholar
  • Kovalev, A., Mazzocchi, M., Siokou, I., & Kideys, A. (2001). Zooplankton of the Black Sea and the Eastern Mediterranean: Similarities and dissimilarities. Mediterranean Marine Science, 2(1), 69-78. google scholar
  • Lakkis, S. (1974). Distributions saisonnieres du zooplancton dans les eaux libanaises. Rapp. P.-v. Reun. Commn int. Explor. scient. Mer Mediterr, 22(9), 117-118. google scholar
  • Lampitt R.S. & Gamble J.C. (1982). Diet and respiration of the small planktonic copepod Oithona nana. Marine Biology 66:185-90 google scholar
  • MacKenzie, L., Sims, I., Beuzenberg, V., & Gillespie, P. (2002). Mass accumulation of mucilage caused by dinoflagellate polysaccharide exudates in Tasman Bay, New Zealand. Harmful Algae, 1(1), 69-83. google scholar
  • Malej A. & Harris R. (1993). Inhibition of copepod grazing by diatom exudates: a factor in the development of mucus aggregates. Mar Ecol Prog Ser 96: 33-42. google scholar
  • Mutlu, E. (2005). A comparison of the contribution of zooplankton and nekton taxa to the near-surface acoustic structure of three Turkish seas. Marine Ecology, 26: 17-32. google scholar
  • Richardson, A.J. (2008). In hot water: zooplankton and climate change. ICES J. Mar. Sci. 65, 279-295. google scholar
  • Rinaldi, A., Vollenweider, R., Montanari, G., Ferrari, C., & Ghetti, A. (1995). Mucilages in Italian seas: the Adriatic and Tyrrhenian seas, 1988-1991. Science of The Total Environment, 165(1-3), 165-183. google scholar
  • Robert, D., Murphy, H.M., Jenkins, G.P. & Fortier, L. (2014). Poor taxonomical knowledge of larval fish prey preference is impeding our ability to assess the existence of a “critical period” driving year-class strength. ICES J. Mar. Sci. 71, 2042-2052. google scholar
  • Saygu, I., Akoğlu, E., Gül, G., Bedikoğlu, D. & Demirel Erol, N. (2023). Fisheries impact on the Sea of Marmara ecosystem structure and functioning during the last three decades. Frontiers in Marine Science, 9. google scholar
  • Siokou-Frangou, I., Shiganova, T., Christou, E.D., Kamburska, L., Gubanova, A., Konsulov, A., Musaeva, E., Skryabin, V. & Khoroshilov, V. (2004). Mesozooplankton communities in the Aegean and Black Sea: a comparative study. Marine Biology 144, 1111-1126 google scholar
  • Steinberg, D. K., & Landry, M. R. (2017). Zooplankton and the ocean carbon cycle. Annual review of marine science, 9, 413-444. google scholar
  • Svetlichny, L., Kideys, A.E., Hubareva, E.S., Isinibilir M. & A. Shmeleva 2006. Zooplankton community state in the Northeastern Marmara Sea during early autumn with comments on mass mortality of the Black Sea species due to the salinity gradient. J. Black Sea / Mediterranean Environment, 12, 213-231. google scholar
  • Svetlichny, L., Isinibilir, M., Mykitchak, T., Eryalçın, K. M., Türkeri, E. E., Yuksel, E. & Kideys, A. E. (2021). Microplastic consumption and physiological response in Acartia clausi and Centropages typicus: Possible roles of feeding mechanisms. Regional Studies in Marine Science 43, 101650, 1-9. https://doi.org/10.1016/j. rsma.2021.101650. google scholar
  • Svetlichny, L., Isinibilir, M. & Kideys, A.E. 2023. First finding of live specimens of non-native copepod Calanus finmarchicus (Gunnerus, 1770) in the Sea of Marmara. Aquatic Sciences and Engineering 38(2): 6-11. google scholar
  • Svetlichny, L., Kideys, A.E., Hubareva, E.S., Isinibilir M. & Shmeleva, A. (2006). Zooplankton community state in the Northeastern Marmara Sea during early autumn with comments on mass mortality of the Black Sea species due to the salinity gradient. J. Black Sea / Mediterranean Environment, 12, 213-231. google scholar
  • Svetlichny, L., Lehtiniemi, M., Setâlâ, O., Samchyshyna, L., Lehto, AM., Gromova, Y., Isinibilir, M., Türkeri, E., Eryalçın, M., Kayadelen, G.C., & Kideys, A.E. (2022). Oxygen consumption rates and respiratory carbon losses in three species of copepods (Acartia clausi, Calanus helgolandicus and Limnocalanus macrurus) during starvation. Turkish Journal of Zoology 46: 249-260. doi:10.3906/zoo-2110-16. google scholar
  • Tarkan, A. N., Isinibilir, M. & Tarkan, A. S. (2005). Seasonal variations of the zooplankton composition and abundance in the Istanbul Strait. Pakistan Journal of Biological Sciences, 8(9), 1327-1336. google scholar
  • Tarkan, A.N. & Erguven, H., (1988). The main copepod species of Marmara Sea. Journal of Aquatic Products 2, 71-72. google scholar
  • Tas, S., Kus, D. & Yilmaz, I. N. (2020). Temporal variations in phytoplankton composition in the northeastern Sea of Marmara: potentially toxic species and mucilage event. Mediterranean Marine Science, 21(3), 668-683. google scholar
  • Turan, C., Ergüden, D. & Gürlek, M. (2016). Climate change and biodiversity effects in Turkish Seas. Natural and Engineering Sciences, 1(2), 15-24. google scholar
  • Turkoglu, M. (2013). Red tides of the dinoflagellate Noctiluca scintillans associated with eutrophication in the Sea of Marmara (the Dardanelles, Turkey). Oceanologia, 55(3), 709-732. google scholar
  • Turner, J. T. (2004). The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoological studies, 43(2), 255-266. google scholar
  • Ulman, A., Zengin, M., Demirel, N. & Pauly, D. (2020). The lost fish of Turkey: A recent history of disappeared species and commercial fishery extinctions for the Turkish Marmara and Black Seas. Frontiers in Marine Science, 7, 650. google scholar
  • Unal, E., Shmeleva, A.A., Zagordnyaya, J. & Kideys, A.E. (2000). Zooplankton structure and copepod species of the Sea of Marmara in spring 1998. In: Ozturk, B., Kadıoglu, M., Ozturk, H. (Eds.), Marmara Sea 2000 Symposium. Turkish Marine Research Foundation (TUDAV) Publications 5, İstanbul, pp. 450-460. google scholar
  • V ardar, S., Onay, T. T., Demirel, B. & Kideys, A. E. (2021). Evaluation of microplastics removal efficiency at a wastewater treatment plant discharging to the Sea of Marmara. Environmental Pollution 289, 117862: 1-9. google scholar
  • V illate, F., Moral, M. & Valencia, V. (1997). Mesozooplankton community changes in a shelf area of the inner Bay of Biscay throughout 1988 to 1990. Journal of Plankton Research 19: 1617-36. google scholar
  • Y ilmaz, I. N. (2015). Collapse of zooplankton stocks during Liriope tetraphylla (Hydromedusa) blooms and dense mucilaginous aggregations in a thermohaline stratified basin. Marine Ecology, 36(3), 595-610. google scholar
  • Y ıldız, T., Ulman, A. & Demirel, N. (2020). A comparison of market landings during fish spawning seasons to better understand the effectiveness of the temporal fishery closure in Turkey. Ocean & Coastal Management, 198, 105353. google scholar
  • Y uksek, A., Yilmaz, N., Okus, E., Uysal, Z., Shmeleva, A.A., Gubanova, A.D., Altukhov, D., & Polat-Beken, S.C. (2002). Spatio-temporal variations in zooplankton communities and influence of environmental factors on them in SW Black Sea and the Sea of Marmara. In: Yilmaz A, editor. Oceanography of the eastern mediterranean and Black Sea: Similarities and differences of two interconnected basins. Ankara, Turkey: TUBITAK Publishers. pp. 774-784. google scholar


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