Mucilage Problem in the Semi-Enclosed Seas: Recent Outbreak in the Sea of Marmara

Abstract

Mucilage is an exopolymeric organic substance that occurs in the marine environment due to the overgrowth of a type of sea algae. Extreme blooms of algae are often triggered by rising seawater temperatures and human-induced pressures such as domestic and industrial wastes, insufficient treatment levels, excessive fishing. In semi-enclosed seas, this phenomenon creates growing concern, as it has a detrimental impact on the entire ecology, particularly benthic organisms. The Sea of Marmara is filled for months with mucilage that clogs the networks of fishers, suffocates marine life, and threatens tourism and the economy. Although the mucilage did not occur in the Sea of Marmara for the first time, nor is the occurrence unique to the area, it is thought to be one of the worst mucilage outbreaks ever. This study aims to provide information on the possible causes and consequences of mucilage and related research in the Sea of Marmara.

Keywords

• Mucilage
• Enzymatic activity
• the Sea of Marmara
• Nutrients
• Organic matter

Supporting Institution

Istanbul University Research Fund (BAP)

Project Number

MAB-2019-34967

References

1. Aktan, Y., & Topaloğlu, B. (2011). First record of Chrysophaeum taylorii Lewis & Bryan and their benthic mucilaginous aggregates in the Aegean Sea (Eastern Mediterranean). J. Black Sea/Medit. Environ, 17(2), 159-170.
2. Aktan, Y., Dede, A., Ciftci, P.S. (2008). Mucilage event associated with diatoms and dinoflagellates in Sea of Marmara, Turkey. Harmful Algae News, IOC-UNESCO, 1-3.
3. Alldredge, A. L., & Crocker, K. M. (1995). Why do sinking mucilage aggregates accumulate in the water column?. Science of the total environment, 165(1-3), 15-22.
4. Altıok, Η., & Kayişoğlu, M. (2015). Seasonal and interannual variability of water exchange in the Strait of Istanbul. Mediterranean Marine Science, 16(3), 644-655.
5. Artüz O.B., Artüz M.L. The project “Changing Oceanographic Conditions of the Sea Of Marmara” MAREM (Marmara Environmental Monitoring). GFCM Workshop on Algal and Jellyfish Blooms in the Mediterranean and Black Sea 6 th /8th October 2010, Istanbul, Turkey.
6. Azam, F. (1998). Microbial control of oceanic carbon flux: the plot thickens. Science, 280(5364), 694-696.
7. Azam, F., & Long, R. A. (2001). Sea snow microcosms. Nature, 414(6863), 495-498.
8. Balkis, N., Atabay, H., Türetgen, I., Albayrak, S., Balkis, H., & Tüfekçi, V. (2011). Role of single-celled organisms in mucilage formation on the shores of Buyukada Island (the Marmara Sea). Marine Biological Association of the United Kingdom. Journal of the Marine Biological Association of the United Kingdom, 91(4), 771.

9. Balkis-Ozdelice, N., Durmus, T., Toklu-Alicli, B., & Balci, M. (2020). Phytoplankton composition related to the environmental conditions in the coastal waters of the Gulf of Erdek. Berthon, J. F., Zibordi, G., & Hooker, S. B. (2000). Marine optical measurements of a mucilage event in the northern Adriatic Sea. Limnology and oceanography, 45(2), 322-327.
10. Beşiktepe, Ş. T. (2003). Density currents in the two-layer flow: an example of Dardanelles outflow. Oceanologica Acta, 26(3), 243-253.
11. Beşiktepe, Ş. T., Lermusiaux, P. F., & Robinson, A. R. (2003). Coupled physical and biogeochemical data-driven simulations of Massachusetts Bay in late summer: real-time and postcruise data assimilation. Journal of Marine Systems, 40, 171-212.
12. Beşiktepe, S., Ryabushko, L., Ediger, D., Yilmaz, D., Zenginer, A., Ryabushko, V., & Lee, R. (2008). Domoic acid production by Pseudo-nitzschia calliantha Lundholm, Moestrup et Hasle (bacillariophyta) isolated from the Black Sea. Harmful Algae, 7(4), 438-442.
13. Bianchi, G. (1746). Notizie sulla vasta fioritura algale del 1729. Raccolta d'opuscoli scientifici e filologici, 34, 256–257. Bidle, K. D., & Azam, F. (1999). Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature, 397(6719), 508-512.
14. Burak, S., Bilge, A. H., & Ülker, D. (2021). Assessment and simulation of water transfer for the megacity Istanbul. Physical Geography, 1-25.
15. Burak, S., Unlu, S., & Gazıoglu, C. (2009). Environmental stress created by chemical pollution in the Marmara sea (Turkey). Asian Journal of Chemistry, 21(4), 3166-3174.
16. Cardak, M., Altug, G., & Turetken, P. S. (2015). Variations of Culturable and Metabolically Active Bacteria in a Stratified Water Column: The Example of Istanbul and Çanakkale Straits, Turkey. International Journal of Environmental Research, 9(4), 1333-1340.
17. Cardak, M., Özbek, E. Ö., & Kebapçioğlu, T. (2015). Seasonal abundance and diversity of culturable heterotrophic bacteria in relation to environmental factors in the Gulf of Antalya, Eastern Mediterranean, Turkey. World Journal of Microbiology and Biotechnology, 31(4), 569-582.
18. Caronni, S., Calabretti, C., Cavagna, G., Ceccherelli, G., Delaria, M. A., Macri, G., ... & Panzalis, P. (2017). The invasive microalga Chrysophaeum taylorii: Interactive stressors regulate cell density and mucilage production. Marine environmental research, 129, 156-165.
19. Cozzi, S., Ivančić, I., Catalano, G., Djakovac, T., & Degobbis, D. (2004). Dynamics of the oceanographic properties during mucilage appearance in the Northern Adriatic Sea: analysis of the 1997 event in comparison to earlier events. Journal of Marine Systems, 50(3-4), 223-241.
20. Danovaro, R., Umani, S. F., & Pusceddu, A. (2009). Climate change and the potential spreading of marine mucilage and microbial pathogens in the Mediterranean Sea. PLoS One, 4(9), e7006.
21. De Lazzari, A., Berto, D., Cassin, D., Boldrin, A., & Giani, M. (2008). Influence of winds and oceanographic conditions on the mucilage aggregation in the Northern Adriatic Sea in 2003–2006. Marine Ecology, 29(4), 469-482.
22. Del Negro, P., Crevatin, E., Larato, C., Ferrari, C., Totti, C., Pompei, M., ... & Umani, S. F. (2005). Mucilage microcosms. Science of the Total Environment, 353(1-3), 258-269.
23. Ediger, D., Beken, Ç., Yüksek, A., & Tuğrul, S. (2016). Eutrophication in the Sea of Marmara. The Sea of, 723.
24. Ergül, H. A., Aksan, S., & İpşiroğlu, M. (2018). Assessment of the consecutive harmful dinoflagellate blooms during 2015 in the Izmit Bay (the Marmara Sea). Acta Oceanologica Sinica, 37(8), 91-101.
25. Flander-Putrle, V., & Malej, A. (2008). The evolution and phytoplankton composition of mucilaginous aggregates in the northern Adriatic Sea. Harmful Algae, 7(6), 752-761.
26. Fukao, T., Kimoto, K., Yamatogi, T., Yamamoto, K. I., Yoshida, Y., & Kotani, Y. (2009). Marine mucilage in Ariake Sound, Japan, is composed of transparent exopolymer particles produced by the diatom Coscinodiscus granii. Fisheries Science, 75(4), 1007-1014.
27. Funari, E., & Ade, P. (1999). Human health implications associated with mucilage in the northern Adriatic Sea. Annali dell'Istituto superiore di sanità, 35(3), 421-425.
28. Giani, M., Savelli, F., Berto, D., Zangrando, V., Ćosović, B., & Vojvodić, V. (2005). Temporal dynamics of dissolved and particulate organic carbon in the northern Adriatic Sea in relation to the mucilage events. Science of the Total Environment, 353(1-3), 126-138.
29. Gigliotti, A. (2013). Extracting temporal and spatial distributions information about marine mucilage phenomenon based on Modis satellite images; a case study of the Tyrrhenian and the Adriatic Sea, 2010-2012 (Doctoral dissertation).
30. Gotsis-Skretas, O. (1995). Mucilage appearances in Greek waters during 1982-1994. Science of the total environment, 165(1-3), 229-230.
31. Herndl, G. J., & Peduzzi, P. (1988). The ecology of amorphous aggregations (Marine Snow) in the Northern Adriatic Sea. Marine Ecology, 9(1), 79-90.
32. Isinibilir-Okyar, M., Ustun, 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: 28-38.
33. Kiørboe, T., & Jackson, G. A. (2001). Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnology and Oceanography, 46(6), 1309-1318.
34. Kraus, R., & Supić, N. (2015). Sea dynamics impacts on the macroaggregates: A case study of the 1997 mucilage event in the northern Adriatic. Progress in oceanography, 138, 249-267.
35. Lancelot, C. (1995). The mucilage phenomenon in the continental coastal waters of the North Sea. Science of the total environment, 165(1-3), 83-102.
36. 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.
37. Maryam, B., & Büyükgüngör, H. (2019). Wastewater reclamation and reuse trends in Turkey: Opportunities and challenges. Journal of Water Process Engineering, 30, 100501.
38. Mecozzi, M., Pietrantonio, E., Di Noto, V., & Pápai, Z. (2005). The humin structure of mucilage aggregates in the Adriatic and Tyrrhenian seas: hypothesis about the reasonable causes of mucilage formation. Marine chemistry, 95(3-4), 255-269.
39. Oguz, T., Özsoy, E., Latif, M. A., Sur, H. I., & Ünlüata, Ü. (1990). Modeling of hydraulically controlled exchange flow in the Bosphorus Strait. Journal of Physical Oceanography, 20(7), 945-965.
40. Oguz, T., Özsoy, E., Latif, M. A., Sur, H. I., & Ünlüata, Ü. (1990). Modeling of hydraulically controlled exchange flow in the Bosphorus Strait. Journal of Physical Oceanography, 20(7), 945-965.
41. Okuş, E., Aslan-Yilmaz, A., Yüksek, A., Taş, S., & Tüfekçi, V. (2002). Nutrient distribution in the Bosphorus and surrounding areas. Water science and technology, 46(8), 59-66.
42. Okyar, M. İ., 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.
43. Özsoy, E., Çağatay, M.N., Balkıs, N., Balkıs, N., Öztürk, B. (Eds.) (2016). The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine Research Foundation (TUDAV), Publication No: 42, Istanbul, TURKEY.
44. Ozturk, A., Yarci, C., & Ozyigit, I. I. (2017). Assessment of heavy metal pollution in Istanbul using plant (Celtis australis L.) and soil assays. Biotechnology & Biotechnological Equipment, 31(5), 948-954.
45. Peduzzi, P., & Weinbauer, M. G. (1993). Effect of concentrating the virus‐rich 2‐2nm size fraction of seawater on the formation of algal flocs (marine snow). Limnology and Oceanography, 38(7), 1562-1565.
46. Polat, C., & Tugrul, S. (1996). The annual influxes of phosphorus, nitrogen and organic carbon into the Marmara Sea from the Black Sea and Istanbul wastes. Oceanographic Literature Review, 4(43), 411.
47. Polat, S. Ç., & Tugrul, S. (1995). Nutrient and organic carbon exchanges between the Black and Marmara Seas through the Bosphorus Strait. Continental Shelf Research, 15(9), 1115-1132.
48. Precali, R., Giani, M., Marini, M., Grilli, F., Ferrari, C. R., Pečar, O., & Paschini, E. (2005). Mucilaginous aggregates in the northern Adriatic in the period 1999–2002: typology and distribution. Science of the Total Environment, 353(1-3), 10-23.
49. Rinaldi, A., Vollenweider, R. A., Montanari, G., Ferrari, C. R., & Ghetti, A. (1995). Mucilages in Italian seas: the Adriatic and Tyrrhenian seas, 1988–1991. Science of the Total Environment, 165(1-3), 165-183.
50. Simon, M., Grossart, H. P., Schweitzer, B., & Ploug, H. (2002). Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic microbial ecology, 28(2), 175-211.
51. Tas, S., & Yilmaz, I. N. (2015). Potentially harmful microalgae and algal blooms in a eutrophic estuary in Turkey. Mediterranean Marine Science, 16(2), 432-443.
52. Taş, S., Ergül, H. A., & Balkıs, N. (2016). Harmful algal blooms (HABs) and mucilage formations in the Sea of Marmara. The Sea of, 768.
53. 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.
54. Tassan, S. (1993). An algorithm for the detection of the White-Tide (“mucilage”) phenomenon in the Adriatic Sea using AVHRR data. Remote sensing of environment, 45(1), 29-42.
55. Toklu-Alicli, B., Balkis-Ozdelice, N., Durmus, T., & Balci, M. (2021). Relationship between environmental factors and zooplankton diversity in the Gulf of Bandırma (the Sea of Marmara). Biologia, 76(6), 1727-1736.
56. Toklu-Alicli, B., Polat, S., & Balkis-Ozdelice, N. (2020). Temporal variations in the abundance of picoplanktonic Synechococcus (Cyanobacteria) during a mucilage event in the Gulfs of Bandırma and Erdek. Estuarine, Coastal and Shelf Science, 233, 106513.
57. Tüfekçi, V., Balkis, N., Beken, Ç. P., Ediger, D., & Mantikci, M. (2010). Phytoplankton composition and environmental conditions of the mucilage event in the Sea of Marmara. Turkish Journal of Biology, 34(2), 199-210.
58. Tugrul, S., Beşiktepe, T., & Salihoglu, I. (2002). Nutrient exchange fluxes between the Aegean and Black Seas through the Marmara Sea. Mediterranean Marine Science, 3(1), 33-42.
59. Umani, S. F., Del Negro, P., Larato, C., De Vittor, C., Cabrini, M., Celio, M., ... & Azam, F. (2007). Major inter-annual variations in microbial dynamics in the Gulf of Trieste (northern Adriatic Sea) and their ecosystem implications. Aquatic Microbial Ecology, 46(2), 163-175.
60. Volterra, L., & Conti, M. E. (2000). Algae as biomarkers, bioaccumulators and toxin producers. International Journal of Environment and Pollution, 13(1-6), 92-125.
61. Weinbauer, M. G., Fuks, D., & Peduzzi, P. (1993). Distribution of viruses and dissolved DNA along a coastal trophic gradient in the northern Adriatic Sea. Applied and Environmental Microbiology, 59(12), 4074-4082.
62. Yentur, R. E., Büyükateş, Y., Özen, Ö., & Altın, A. (2013). The environmental and socio-economical effects of a biologic problem: Mucilage. Marine Science and Technology Bulletin, 2(2), 13-15.
63. Yilmaz, 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.
64. Zambianchi, E., Calvitti, C., Cecamore, P., D'Amico, F., Ferulano, E., & Lanciano, P. (1992). The mucilage phenomenon in the Northern Adriatic Sea, summer 1989: a study carried out with remote sensing techniques. In Marine Coastal Eutrophication,581-598.
65. Zingone, A., Escalera, L., Aligizaki, K., Fernández-Tejedor, M., Ismael, A., Montresor, M., ... & Totti, C. (2021). Toxic marine microalgae and noxious blooms in the Mediterranean Sea: A contribution to the Global HAB Status Report. Harmful Algae, 102, 101843.