Turgay DURMUŞ, Neslihan BALKIS-OZDELICE, Seyfettin TAŞ, Fatma BAYRAM PARTAL, Muharrem BALCI, Cem DALYAN, Mustafa SARI

New Records for Microalgae Species of the Turkish Seas Under the Effect of Intense Mucilage in the Sea of Marmara

Objective: New records of microalgae species for Turkish seas taking into account the species lists published to date have been reported in this study conducted in the Sea of Marmara and the Aegean Sea. Furthermore, new records of microalgae species for the Sea of Marmara and the Aegean Sea were listed. Materials and Methods: New record species for Turkish seas were described by their morphological and ecological features and also their images were taken under a light microscope with epifluorescence attachment, and also some of them were photographed on a scanning electron microscope. Results: A total of 66 new record species were identified in this study. A total of 25 microalgae taxa belonging to 11 taxonomic classes were recorded for the first time for Turkish seas. Two taxa were freshwater or brackish water form, which is known from the lakes. The class Prymnesiophyceae had seven taxa that were recorded for the first time, followed by Bacillariophyceae and Dinophyceae with four taxa and the other classes. Furthermore, a total of 65 taxa belonging to 16 taxonomic classes were recorded for the first time for the Sea of Marmara. Twelve taxa were freshwater or brackish water form, which is known from the lakes. Among these, Dinophyceae had 24 taxa, followed by Prymnesiophyceae with 11 taxa, and Bacillariophyceae with 9 taxa and the other classes. In addition, one new record taxon was detected for the Aegean Sea. Conclusion: New records of microalgae detected in the Sea of Marmara during this study period will provide an important contribution to both the microalgae checklist of Turkish seas, the Sea of Marmara and the Aegean Sea.

Keywords:

Mucilage, new records, phytoplankton, biodiversity, Turkish coastal waters,

PDF

___

1. Koray T. A check-list for phytoplankton of Turkish seas. EgeJFAS 2001; 18(1-2): 1-23. google scholar
2. Balkis N. List of phytoplankton of the Sea of Marmara. J Black Sea/ Medit Environ 2004; 10: 123-41. google scholar
3. Balkis N, Tas S. Phytoplankton of the Sea of Marmara: A review. Özsoy, E., Çağatay, M. N., Balkis, N., Balkis, N., Öztürk, B., editors. The Sea of Marmara: Marine Biodiversity, fisheries, conservation and governance. Istanbul: Turkish Marine Research Foundation (TUDAV), İstanbul; 2016.p.326-43. google scholar
4. Tas S, Hernandez-Becerril DD. Diversity and distribution of planktonic diatom genus Chaetoceros (Bacillariophyceae) in the Golden Horn Estuary (Sea of Marmara). Diatom Res 2017; 32(3): 309-23. google scholar
5. Balci M, Balkis N. Assessment of phytoplankton and environmental variables for water quality and trophic state classification in the Gemlik Gulf, Marmara Sea (Turkey)”. Mar Pollut Bull 2017; 115: 17289. google scholar
6. Balkis-Ozdelice N, Durmus T, Toklu-Alicli B, Balci M. Phytoplankton composition related to the environmental conditions in the coastal waters of the Gulf of Erdek. Indian J Mar Sci 2020; 49(9): 1545-59. google scholar
7. Balkis-Ozdelice N, Durmus T, Balci M. A preliminary study on the intense pelagic and benthic mucilage phenomenon observed in the Sea of Marmara. Int J Environ Geoinformatics 2021; 8(4): 41422. google scholar
8. Kayadelen Y, Balkis-Ozdelice N, Durmus T. Determination of seasonal changes in phytoplankton community of the coastal waters of Burgaz Island (the Sea of Marmara). J Mar Biolog Assoc UK 2022; 102(3-4): 1-13. google scholar
9. Eker-Develi E, Kideys AE. First record of the diatom Nitzschia navis-varingica in the Sea of Marmara. Mar Sci Tech Bull 2022; 11(2): 23135. google scholar
10. Yüce H. Investigation of the Mediterranean water in the Black Sea. Bülten 1988; 5: 121-57. google scholar
11. Yüce H,Türker A. Marmara Denizi’nin fiziksel oşinografiközellikleri ve Akdeniz suyunun Karadeniz’e girişi. Uluslararası çevre sorunları sempozyumu tebliğleri. İstanbul: Türkiye; 1991.p.284-303. google scholar
12. Beşiktepe ŞT, Sur Hİ, Özsoy E, Abdullatif MA, Oğuz T, Ünlüata Ü. The circulation and hydrography of the Marmara Sea. Prog Oceanogr 1994; 34: 285-334. google scholar
13. Beşiktepe Ş, Özsoy E, Latif MA, Oğuz T. Marmara Denizi’nin hidrografisi ve Dolaşımı, (Hydrography and Circulation of the Marmara Sea). Marmara Sea 2000 Symposium; 2000 Nov 11-2; İstanbul: Türkiye.p.1-14. google scholar
14. Aksu A, Caglar-Balkis N, Taskin Ö. Müsilajın çevresel şartlarda değişen kimyasal karakterizasyonunun incelenmesi (in Turkish). Ozturk İ, Seker M, editors. Marmara Denizi’nin Ekolojisi: Deniz Salyası Oluşumu, Etkileşimleri ve Çözüm Önerileri. Ankara: TÜBA; 2021.p.127-35. google scholar
15. Ergül H, Balkis-Ozdelice N, Koral M, Aksan S, Durmuş T, Kaya M, Kayal M, Ekmekçi F, Oltan C. The early stage of mucilage formation in the Marmara Sea during spring 2021. J Black Sea/Medit Environ 2021; 27(2): 232-57. google scholar
16. Throndsen J. Preservation and storage. Sournia A, editor. Phytoplankton Manual. Paris: UNESCO; 1978.p.69-74. google scholar
17. Utermöhl H. Zur vervollkommung der quantitativen phytoplankton methodik. Mitt - Int Ver Theor Angew Limnol 1958; 9: 1-38. google scholar
18. Sukhanova IN. Settling without the inverted microscope. Sournia A, editor. Phytoplankton Manual. Paris: UNESCO; 1978.p.97. google scholar
19. Semina HJ. Treatment of an aliquot sample. Sournia A, editor. Phytoplankton Manual. Paris: UNESCO; 1978.p.181. google scholar
20. Hendey NI. A revised check-list of British marine diatoms. J Mar Biolog Assoc UK 1974; 54(2): 277-300. google scholar
21. Battarbee RW, Cameron NG, Golding P, Brooks SJ, Switsur R, Harkness D, McGovern A. Evidence for holocene climate variability from the sediments of a Scottish remote mountain lake. J Quat Sci 2001; 16(4): 339-46. google scholar
22. Perez-Lopez H, Duran-Riveroll L, Gomez-Lizarraga L, Mendoza-Garfias M. Simple method for preparing delicate dinoflagellate of the genus Amphidinium for scanning electron microscopy. Microsc Microanal 2020; 26(2): 1366-9. google scholar
23. Heimdal BR. Modern Coccolithophorids. Tomas CR, editor. Marine Phytoplankton. California: Academic Press; 1993.p.147-236. google scholar
24. Throndsen J. The planktonic marine flagellates. Tomas CR, editor. Marine Phytoplankton. California: Academic Press; 1993. p. 7-146. google scholar
25. Hasle GR, Syvertsen EE. Marine diatoms. Tomas CR, editor. Identifying Marine Phytoplankton. California: Academic Press; 1997. p. 5-385. google scholar
26. Steidinger KA, Tangen K. Dinoflagellates. Tomas CR, editor. Identifying Marine Phytoplankton. California: Academic Press; 1997.p.387-570. google scholar
27. World Register of Marine Species. Chromista. Accessed at: https:// www.marinespecies.org/aphia.php?p=taxdetails&id=7. Accessed on 1 Oct 2022. google scholar
28. Algaebase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org. Accessed on 1 Oct 2022. google scholar
29. Cleve PT. Synopsis of the Naviculoid diatoms (Part I). K Sven Vetensk Akad Handl 1894; 26(2): 1-194. google scholar
30. Schmidle W. Bemerkungen zu einigen Süsswasseraigen. Ber Deutsch Bot Ges 1903; 21: 346-55. google scholar
31. Hustedt F. Bacillariophyta (Diatomeae). In: Die Süsswasser-Flora Mitteleuropas (Ed: Pascher A, 2nd edition). Jena: Verlag von Gustav Fischer; 1930. google scholar
32. Gantt E, Conti SF. The ultrastructure of Porphyridium cruentum. J Cell Biol 1965; 26(2): 365-81. google scholar
33. Bukry D. Phytoplankton stratigraphy, deep sea drilling project leg 20, Western Pacific Ocean. Initial Rep Deep Sea Drill Proj 1973; 20: 307-17. google scholar
34. Fukuyo Y. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bull Japan Soc Sci Fish 1981; 47(8): 967-78. google scholar
35. V0rs N. Heterotrophic amoebae, flagellates and heliozoa from the Tvärminne area, Gulf of Finland, in 1988-1990. Ophelia 1992; 36: 1-109. google scholar
36. Young JR, Geisen M, Cros L, Kleijne A, Sprengel C, Probert I, Ostergaard JB. A guide to extant coccolithophore taxonomy. Journal of Nannoplankton Research 2003; Special Issue 1: 1-125. google scholar
37. Haywood AJ, Steidinger KA, Truby EW, Bergquist PR, Bergquist PL, Adamson J, MacKenzie L. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J Phycol 2004; 40: 165-79. google scholar
38. Fresnel J, Probert I. The ultrastructure and life cycle of the coastal coccolithophorid Ochrosphaera neapolitana (Prymnesiophyceae). Eur J Phycol 2005; 40(1): 105-22. google scholar
39. Hoppenrath M, Elbrachter M, Drebes G. Marine phytoplankton. Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung; 2009. google scholar
40. Takano Y, Matsuoka K. A comparative study between Prorocentrum shikokuense and P. donghaiense (Prorocentrales, Dinophyceae) based on morphology and DNA sequences. Plankton Benthos Res 2011; 6(4): 179-86. google scholar
41. Idei M, Sato S, Watanabe T, Nagumo T, Mann DG. Sexual reproduction and auxospore structure in Diploneis papula (Bacillariophyta). Phycologia 2013; 52(3): 295-308. google scholar
42. Hardardottir S, Lundholm N, Moestrup OE, Nielsen TG. Description of Pyramimonas diskoicola sp. nov. and the importance of the flagellate Pyramimonas (Prasinophyceae) in Greenland sea ice during the winter-spring transition. Polar Biol 2014; 37: 1479-94. google scholar
43. Han Y, Graf L, Reyes CP, Melkonian B, Andersen RA, Yoon HS, Melkonian M. A Re-investigation of Sarcinochrysis marina (Sarcinochrysidales, Pelagophyceae) from its type locality and the descriptions of Arachnochrysis, Pelagospilus, Sargassococcus and Sungminbooa genera nov. Protist 2018; 169(1): 79-106. google scholar
44. Young JR, Bown PR, Lees JA. International Nannoplankton Association. www.mikrotax.org/Nannotax3. Accessed on 12 Oct 2022. google scholar
45. Holmes MJ, Lewis RJ, Jones A, Hoy AW. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat Toxins 1995;3(5):355-62. google scholar
46. Faust, MA, Gulledge RA. Identifying harmful marine dinoflagellates. Contributions from the United States National Herbarium, National Museum of Natural History, 2002; 42: 1-144. google scholar
47. Aktan Y, Topaloglu B. First record of Chrysophaeum taylorii Lewis & Bryan and their benthic mucilaginous aggregates in the Aegean Sea (Eastern Mediterranean). J Black Sea/Medit Environ 2011; 17(2): 159-70. google scholar
48. Pedrotti ML, Fiorini S, Kerros ME, Middelburg JJ, Gattuso JP. Variable production of transparent exopolymeric particles by haploid and diploid life stages of coccolithophores grown under different CO2 concentrations. J Plankton Res 2012; 34(5): 388-98. google scholar
49. Lundholm N, Churro C, Fraga S, Hoppenrath M, Iwataki M, Larsen J, Mertens K, Moestrup 0, Zingone A (Eds) (2009 onwards). IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae. https:// www.marinespecies.org/hab. Accessed on 7 Nov 2022. google scholar
50. Coesel PFM, Meesters KJ. European Flora of the Desmid Genera Staurastrum and Staurodesmus. Utrecht: KNNV Publishing; 2014. google scholar
51. Akcaalan R, Kaleli A, Koker L. Distribution of marine benthic diatoms on the coasts of the Sea of Marmara and their responses to environmental variables. J Mar Syst 2022; 234: 103780. google scholar
52. Nissimov JI, Vandzura R, Johns CT, Natale F, Haramaty L, Bidle KD. Dynamics of transparent exopolymer particle production and aggregation during viral infection of the coccolithophore, Emiliania huxleyi. Environ Microbiol 2018; 20(8); 2880-97. google scholar
53. Rhodes L. World-wide occrence of the toxic dinoflagellate genus Ostreopsis schmidt. Toxicon 2011; 57: 400-7. google scholar
54. Bizsel N, Aligizaki K. Detection of Ostreopsis cf ovata in coastal waters of Turkey (Eastern Aegean Sea). International Conference on Ostreopsis Development; April 2011; Villefranche: France. google scholar
55. Lewis NI, Wolny JL, Achenbach JC, Ellis L, Pitula JS, Rafuse C, Rosales DS, McCarron P. Identification, growth and toxicity assessment of Coolia Meunier (Dinophyceae) from Nova Scotia, Canada. Harmful Algae 2018; 75: 45-56. google scholar
56. Holmes MJ, Lewis RJ, Jones A, Hoy AWW. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat Toxins 1995; 3: 355-62. google scholar
57. Aquino-Cruz A, Okolodkov YB. Impact of increasing water temperature on growth, photosynthetic efficiency, nutrient consumption, and potential toxicity of Amphidinium cf. carterae and Coolia monotis (Dinoflagellata). Rev Biol Mar Oceanogr 2016; 51(3): 565-80. google scholar