Abstract
Coccolithophores have had an effect on global climate change for a few million years. The marine phytoplankton group is responsible for approximately 20% of the total carbon fixation in marine systems. They can form blooms spreading hundreds of thousands of square kilometers, are recognized by elegant coccolith structures formed from calcium carbonate exoskeletons, and are visible from space. Although carbon is transferred to the sediments in organic matter and calcite form by coccolithophores, carbon dioxide (CO2) is released by the calcification process. Therefore, they have a complex effect on the carbon cycle due to their activity regarding CO2 production and consumption. This review represents the first attempt to present temporal and vertical distributions of Emiliania huxleyi (Lohmann) Hay & Mohler, 1967 (Ehux), which is one of the most important species of the coccolithophores in the bloom periods and the interaction of this species with other phytoplankton groups in the Sea of Marmara. This study may also indicate the advance of this species from the Black Sea region through the Sea of Marmara and the Dardanelles under favorable conditions.
Keywords
- Phytoplankton
- coccolithophore
- Emiliania huxleyi
- bloom dynamics
- Sea of Marmara
1. Introduction
The Sea of Marmara is a very important water passage between the Aegean Sea and the Black Sea via the Dardanelles and the Bosphorus. It has two current systems that run in opposite directions. Deep water high in density (38.0 ppt) coming from the Aegean Sea flows into the Black Sea. Surface water low in density (18.0 ppt) coming from the Black Sea flows into the Aegean Sea. Therefore, Marmara is affected by both neighbor systems [1–3].
Coccolithophores are marine haptophyte phytoplankton. They are one of the most important groups of phytoplankton in today’s oceans and contain about 300 species.
The coccolithophore
The main phytoplankton groups in the Sea of Marmara are dinoflagellates, diatoms, coccolithophores, and cyanobacteria. Although there are many different phytoplankton species—more than 150 in the Sea of Marmara—the blooms tend to be extremely rich in a single, or only a few, predominant species such as
This study looks at
2. Methodology
The methodology adopted by this review study on the bloom dynamics of the coccolithophore
3. Emiliania huxleyi (Lohmann) Hay & Mohler, 1967
3.1. General characters
3.2. Global distribution and abundance
3.3. Climate change and harmful algal blooms
It is predicted that climate change will seriously impact aquatic ecosystems, both freshwater and marine. Together with nutrient pollution, these climatic impacts might bring about increases in the densities and field effects of harmful algal blooms (HABs). Climate change might affect HABs in many ways as a result of increased water temperature, higher CO2 values, changes in rainfall and salinity, coastal upwelling, rise in sea levels.
As waters warms more than usual due to climate change, HABs will increase both in number and area. HABs usually occur in warm summer periods. Warm waters favor the formation of HABs in a number of ways. For example, nanoplankton and picoplankton species such as the more toxic cyanobacteria and coccolithophores prefer warmer waters. High temperature levels at the surface prevent mixing of the water column, which allows HABs to become thicker and grow faster. It is generally accepted that warm waters favor the proliferation of tiny phytopkankton bloom species and allow them to survive much easier in the surface waters. It is known that algal blooms absorb solar radiation, which makes the water even warmer than usual and facilitates more algal blooms. On the other hand, climate change might lead to more drought seasons, making freshwater saltier. So, marine algal bloom species could spread to freshwater and brackish water ecosystems.
Phytoplankton species need dissolved CO2 to proliferate. Higher CO2 levels—first in the air and then water—might lead to rapid phytoplankton increase, particularly picoplanktonic species that float on the surface layer of the water. Moreover, climate change might affect precipitation dynamics, leading to alternating periods of drought and intense storms. The main source of nutrients is rain and river water discharge into aquatic ecosystems, supporting more algal blooms.
In view of current sea level rise, more scientists predict that sea levels will rise by as much as 1 m by 2100. Rising sea levels would create an increase in shallow and coastal waters—perfect conditions for the growth of phytoplankton and other algae. Another important factor is the increase in coastal upwelling events due to climate change. Coastal upwelling is a transport process from ocean deep-layer waters rich in nutrients to surface-layer waters of coastal zones due to the drifting of surface waters by offshore winds. Waters rich in nutrients delivered by upwelling lead to more algal blooms.
On the other hand, it is important to remember that this is a two-way process in which climate change affects HABs and HABs affect climate change. Looked at from the perspective of global excessive
4. Bloom dynamics of Emiliania huxleyi in the Sea of Marmara
4.1. Effect of temperature, salinity, and CO2 in the Sea of Marmara
Average annual air temperature anomalies between 1981 and 2014 in Turkey (Fig. 3) confirm increased annual average temperature. For example, looking at temperature changes in the last 5 years the average temperature in 2014 (14.9°C) exceeds the average between 1971 and 2010 (13.5°C) (Figs. 3
The increase in average air temperature also causes an increase in surface water temperature in the Sea of Marmara and Black Sea—as is the case in other Turkish seas (Fig. 5). Due to the similar climatic behavior coupled with the effect of Black Sea surface waters via the Bosphorus, sea surface temperature variations in the Sea of Marmara are largely similar to the time series of basin mean winter anomalies of sea surface temperature (SSTA), surface atmosphere temperature (SATA), and the meridional component of surface wind (WA, m/s, dashed lines) for the Black Sea [25].
The Sea of Marmara has two current systems that flow in opposite directions: upper-layer water that originates from less salty Black Sea surface water (18.0 ppt) and lower-layer water that originates from very salty Mediterranean water (39.0 ppt). Therefore, there is stratification in terms of both temperature and salinity during the year. However, the stratification in temperature in summer and winter in the Sea of Marmara is reversed, but the stratification in salinity is not. Hence, surface waters are consistently cold in winter (8–12°C) and hot in summer (20–25°C) irrespective of temperature during the year. When it comes to minimum and maximum temperature variations the Sea of Marmara provides the most favorable conditions for massive
In the summer
4.2. Effect of nutrient and nutrient ratios on Emiliania huxleyi blooms in the Sea of Marmara
There is experimental and natural evidence for the exceptional competitive ability of
However, another examination of mesocosm experiments over several years showed that
Turkoglu [9, 10] demonstrated that N:P ratios are significantly lower than the assimilatory optimal of the Redfield ratio (16:1) in the Sea of Marmara during
On the other hand, vertical profiles of inorganic nutrients in bloom periods show that both nitrogen and phosphate concentrations in the Sea of Marmara are higher (Figs. 10
In actuality, what triggers
In
Merico et al. [46] showed low N:P ratios in the southeastern Bering Sea during the
On the other hand, inorganic N:P ratios may not be good indicators of phosphorus stress if organic forms of nitrogen and phosphorus are available to phytoplankton. Organic forms of nitrogen and phosphorus are used by many phytoplankton and may be important in their nutrition, but data on organic nutrient forms, bioavailability, and species-specific abilities to use them are still limited [47, 48].
4.3. Phytoplankton chlorophyll a levels in the Sea of Marmara
Turkoglu (2008) revealed that, in the summer
SeaWiFS (Sea-Viewing Wide Field-of-View Sensor) satellite images for chlorophyll
5. Emiliania huxleyi bloom characters of the Sea of Marmara
5.1. Interactions of Emiliania huxleyi and other phytoplankton
Various scientists studying phytoplankton taxonomy have listed over 150 different types of phytoplankton in the Sea of Marmara [1, 52]. However, the blooms tend to be extremely rich in a single, or only a few, predominant species. This sea has a three-phase phytoplankton bloom sequence. Diatoms tend to predominate in March, dinoflagellates in April, and the dramatically colorful blooms of
The Moderate Resolution Imaging Spectroradiometer (SeaWiFS/MODIS) produced true-color images of the extensive bloom events of
The abundance of
MODIS images (Figs. 15
The sea level in these bodies of water is in equilibrium—were it not the surface of these seas would be rising or falling. The flow of water into one is counterbalanced by an approximately equal flow of water out of another. The flow of surface water out of the Black Sea and the Sea of Marmara into the Aegean Sea is approximately 600 km3 y-1. The water flow is balanced by annual freshwater discharge of about 300 km3 from rivers, especially from the Danube River, which discharges into the Black Sea, and by annual saline water input of about 300 km3 coming from the Mediterranean Sea via the Bosphorus. Black Sea surface-layer water is substantially less saline than Mediterranean water due to the freshwater discharge of rivers [28, 56, 57]. Input of less saline water from the Black Sea and the Sea of Marmara, accompanied by the clouds of coccoliths, is very important to the physicochemical oceanography of the Aegean Sea. The movement of the turquoise water, which stays in the surface layer due to its lower density, can be tracked through the Aegean Sea (Figs. 15
During both the
6. Management of HABs and Emiliania huxleyi blooms
HABs can be managed in three ways: (1) prevention, (2) mitigation, and (3) control efforts. Prevention involves reducing the incidence and extent of HABs by controlling or decreasing the input of anthropogenic waste water, rich in nutrients and other pollutants, and ballast water, rich in invasive species, before HAB onset. HAB mitigation generally involves monitoring for blooms and their toxins, public communication programs, and the transfer/removal of fish cages from critical areas to less critical regions. HAB control involves a number of methods: biological, chemical, ultrasonic, ozonation, chemical and clay flocculation.
Nature dictates that all organisms are controlled by other organisms. There are many host-specific viruses, predators, parasites, and pathogens involved in the biological control of many HAB species. To date, the control mechanisms on the distribution of
Recently, amplified segments of the major capsid protein (MCP) gene from viruses that infect
7. Conclusion
The overutilization of nutrients by summer and winter diatom blooms immediately before
Because of their potential impact on global carbon and sulfur cycles [41],
However, there is general agreement that—in light of the high levels of nutrients, changing nutrient ratios, chlorophyll
References
- 1.
Turkoglu M, Unsal M, Ismen A, Mavili S, Sever TM, Yenici E, Kaya S, Coker, T. Dynamics of lower and high food chain of the Dardanelles and Saros Bay (North Aegean Sea). Tubitak Project Final Report, TUBITAK-YDABÇAG-101Y081; 2004a. 314 p. - 2.
Turkoglu M, Baba A, Ozcan H. Determination and evaluation of some physicochemical parameters in the Dardanelles (Canakkale Strait-Turkey) using multiple probe system and geographic information system. Hydrology Research (previously: Nordic Hydrology). 2006; 37 (3): 293–301. DOI: 10.2166/nh.2006.012. - 3.
Baba A, Deniz O, Turkoglu M, Ozcan H. Investigation of discharge of fresh water in the Çanakkale Strait (Dardanelles-Turkey). In: Linkov I, Kiker GA, Wenning RJ, editors. Environmental Security in Harbors and Coastal Areas. NATO Science for Peace and Security Series C: Environmental Security, Springer, Netherlands; 2007. p. 421–427. DOI: 10.1007/978-1-4020-5802-8_30. - 4.
Balch WM, Holigan PM, Ackleson SG, Voss KJ. Biological and optical properties of mesoscale coccolithophore blooms in the Gulf of Maine. Limnology and Oceanography. 1991; 36: 629–643. - 5.
Balch WM, Holigan PM, Kilpatrick KA. Calcification, photosynthesis and growth of the bloom-forming coccolithophore, Emiliania huxleyi . Cont. Shelf Res. 1992; 12: 1353–1374. DOI: 10.1016/0278-4343(92)90059-S. - 6.
Nanninga HJ, Tyrrell T. The importance of light for the formation of algal blooms by Emiliania huxleyi . Marine Ecology Progress Series. 1996; 136, 195–203. - 7.
Hattori H, Koike M, Tachikawa K, Saito H, Nagasawa K. Spatial variability of living coccolithophore distribution in the Western Subarctic Pacific and Western Bering Sea. Journal of Oceanography. 2004; 60: 505–515. DOI: 10.1023/B:JOCE.0000038063.81738.ab. - 8.
Smyth TJ, Tyrrell T, Tarrant B. Time series of coccolithophore activity in the Barents Sea, from twenty years of satellite imagery. Geophysical Research Letters. 2004; 31: L11302. DOI: 10.1029/2004GL019735. - 9.
Turkoglu M. Synchronous blooms of the coccolithophore Emiliania huxleyi (Lohmann) Hay & Mohler and three dinoflagellates in the Dardanelles (Turkish Straits System). Journal of the Marine and Biological Association of the United Kingdom. 2008; 88 (3): 433–441. DOI: doi:10.1017/S0025315408000866. - 10.
Turkoglu M. Winter bloom and ecological behaviors of coccolithophore Emiliania huxleyi (Lohmann) Hay & Mohler, 1967 in the Dardanelles. Hydrology Research. 2010a; 41 (2): 104–114. DOI: 10.2166/nh.2010.124. - 11.
Turkoglu M. Emiliania huxleyi bloom in winter period in the Dardanelles, Turkey. Rapp. Comm. Int. Mer Médit. 2010b; 39: 410–410. - 12.
Fabry VJ. Calcium carbonate production by coccolithophorid algae in long-term carbon dioxide sequestration. San Marcos (US): California State University; 2003. 20 p. DOI: DE-FC26-01NT41132. - 13.
Dacey JWH, Wakeham S. Oceanic dimethylsulfide: Production during zooplankton grazing on phytoplankton. Science. 1986; 233 (4770): 1314–1316. DOI: 10.1126/science.233.4770.1314. - 14.
Turkoglu M. Red tides of the dinoflagellate Noctiluca scintillans associated with eutrophication in the Sea of Marmara (The Dardanelles, Turkey). Oceanologia. 2013; 55 (3): 709–732. DOI: 10.5697/oc.55-3.709. - 15.
Unsal M, Turkoglu M, Yenici E. Biological and physicochemical researches in the Dardanelles. Tubitak Project Final Report, TUBITAK-YDABÇAG-100Y075; 2003. 133 p. - 16.
Turkoglu M, Oner C. Short time variations of winter phytoplankton, nutrient and chlorophyll-a of Kepez harbor in the Dardanelles (Çanakkale Strait, Turkey). Turkish Journal of Fisheries and Aquatic Sciences. 2010; 10 (4): 537–548. - 17.
NASA 2015. National Aeronautics and Space Administration, US. Available from: https://earthdata.nasa.gov/labs/worldview/ [Accessed: 2015-06-15]. - 18.
Hay WW, Mohler HP, Roth PH, Schmidt RR, Boudreaux JE. Calcareous nanoplankton zonation of the Cenozoic of the Gulf Coast and Caribbean–Antillean area, and transoceanic correlation. Transactions of the Gulf Coast Association of Geological Societies, 1967; 17: 428–480. - 19.
Schaechter M. Eukaryotic Microbes. 1st ed. Amsterdam: Academic Press and Elsevier; 2012. 479 p. DOI: 10.1111/j.1550-7408.2012.00637.x - 20.
Tyrell T, Holligan PM, Mobley CD. Optical impacts of oceanic coccolithophore blooms. Journal of Geophysical Research. 1999; 104: 3223–3241. DOI: 10.1029/1998JC900052. - 21.
Kinkel H, Baumann KH, Cepek M. Coccolithophores in the equatorial Atlantic Ocean: response to seasonal and Late Quaternary surface water variability. Marine Micropaleontology. 2000; 39 (1–4): 87–112. DOI: 10.1016/S0377-8398(00)00016-5. - 22.
Beaufort L, Probert I, De Garidel-Thoron T, Bendif EM, Ruiz-Pino D, Metzl N, Goyet C, Buchet N, Coupel P, Grelaud M, Rost B, Rickaby REM, De Vargas C. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature. 2011; 476 (7358): 80–83. DOI: 10.1038/nature10295. - 23.
Beatrice G. 2015. What's fueling the rise of coccolithophores in the oceans? [Internet]. 2015. Avaliable from: www.csmonitor.com (The Christian Science Monitor). [Accessed: 2015-11- 30]. - 24.
OSIB-MGM 2015. Seasonal temperature analysis (Mevsimlik Sıcaklık Analizi). Turkish Ministry of Forestry and Water Affairs (T.C. Orman Su İşleri Bakanlığı), Turkish State Meterological Service (Meteoroloji Genel Müdürlüğü) [Internet]. Available from: http://www.mgm.gov.tr/veridegerlendirme/sicaklik-analizi.aspx?s=m/[Accessed:2015-12-01]. - 25.
Kazmin AS. Zatsepin AG, Kontoyiannis H. Comparative analysis of the long-term variability of winter surface temperature in the Black and Aegean Seas during 1982–2004 associated with the large-scale atmospheric forcing. International Journal of Climatology. 2009; 30 (9): 1349–1359. DOI: 10.1002/joc.1985. - 26.
Sorrosa JM, Satoh M, Shiraiwa Y. Low temperature stimulates cell enlargement and intracellular calcification of coccolithophorids. Mar. Biotech. 2005; 7 (2), 128–133. DOI: 10.1007/s10126-004-0478-1. - 27.
Tyrrell T, Taylor AH. A modelling study of Emiliania huxleyi in the NE Atlantic. Journal of Marine Systems. 1995; 9: 195–203. DOI: doi:10.1016/0924-7963(96)00019-X. - 28.
Oguz T, Ducklow HW, Malanotte-Rizzoli P, Murray JW, Shushkina EA, Vedernikov VI, Unluata U. A physical-biochemical model of plankton productivity and nitrogen cycling in the Black Sea. Deep Sea Research Part I. 1999; 46 (4): 597–636. DOI: 0.1016/S0967-0637(98)00074-0. - 29.
Watts A. A study: The temperature rise has caused the CO2 increase, not the other way around [Internet]. 2010. Available from: http://wattsupwiththat.com/2010/06/09/a-study-the-temperature-rise-has-caused-the-co2-increase-not the-other-way-around/ [Accessed: 2015-12-01]. - 30.
Riegman R, Noordeloos GC, Cede AA. 1992. Phaeocystis blooms and eutrophication of the continental coastal zones of the North Sea. Mar. Biol., 112: 479–484. DOI: 10.1007/BF00356293. - 31.
Riegman R, Stolte W, Noordeloos AAM, Slezak D. Nutrient uptake and alkaline phosphatase (EC 3:1:3:1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. J. Phycol. 2000; 36: 87– 96. DOI: 10.1046/j.1529-8817.2000.99023.x. - 32.
Kuenzler EJ, Perras JP. Phosphatases of marine algae. Biol. Bull. 1965; 128: 271–284. - 33.
Egge JK, Heimdal BR. Blooms of phytoplankton including Emiliania huxleyi (Haptophyta). Effects of nutrient supply in different N:P ratios. Sarsia. 1994; 79: 333–348. DOI: 10.1080/00364827.1994.10413565. - 34.
Aksnes DL, Egge JK, Rosland R, Heimdal BR. Representation of Emiliania huxleyi in phytoplankton simulation models. A first approach. Sarsia. 1994; 79: 291–300. DOI: 10.1080/00364827.1994.10413561. - 35.
Eker E, Georgieva L, Senichkina L, Kideys AE. Phytoplankton distribution in the western and eastern Black Sea in spring and autumn 1995. ICES Journal of Marine Science. 1999; 56: 15–22. DOI: 10.1006/jmsc.1999.0604. - 36.
Eker-Develi E. Distribution of phytoplankton in the southern Black Sea in summer 1996, spring and autumn 1998. Journal of Marine Systems. 2003; 39 (3–4): 203–211. DOI: 10.1016/S0924-7963(03)00031-9. - 37.
Turkoglu M, Koray T. Phytoplankton species succession and nutrients in the Southern Black Sea (Bay of Sinop). Turk J Bot. 2002; 26 (4): 235–252. - 38.
Turkoglu M. Succession of picoplankton (coccoid cyanobacteria) in the Southern Black Sea (Sinop Bay, Turkey). Pak J Bio Sci. 2005; 8 (9), 1318–1326. - 39.
Turkoglu M, Erdogan Y. Diurnal variations of summer phytoplankton and interactions with some physicochemical characteristics under eutrophication of surface water in the Dardanelles (Çanakkale Strait, Turkey). Turk J Bio. 2010; 34 (2): 211–225. DOI: 10.3906/biy-0807-7. - 40.
Turkoglu M, Koray T. Algal blooms in surface waters of the Sinop Bay in the Black Sea, Turkey. Pak J Bio Sci. 2004; 7 (9): 1577–1585. - 41.
Holligan PM, Viollier M, Harbour DS, Camus P, Champagne-Philippe G, Muller K. A biogeochemical study of the coccolithophore, Emiliania huxleyi , in the North Atlantic. Global Biogeochemical Cycles. 1993; 7: 879–900. DOI: 10.1029/93GB01731. - 42.
Broerse ATC, Tyrrell T, Young JR, Poulton AJ, Merico A, Balch WM, Miller PI. The cause of bright waters in the Bering Sea in winter. Continental Shelf Research. 2003; 23, 1579–1596. DOI: 10.1016/j.csr.2003.07.001. - 43.
Cokacar T, Kubilay N, Oguz T. Structure of Emiliania huxleyi blooms in the Black Sea surface waters as detected by SeaWiFS imagery. Geophys. Res. Letters. 2001; 28(24): 4607-4610. DOI: 10.2001GL013770. - 44.
Oguz T, Merico A. Factors controlling the summer Emiliania huxleyi bloom in the Black Sea: A modeling study. Journal of Marine Systems. 2006; 59 (3–4): 173–188. DOI: 10.1016/j.jmarsys.2005.08.002. - 45.
Zeichen MM, Robinson IS. Detection and monitoring of algal blooms using SeaWiFS imagery. International Journal of Remote Sensing. 2004; 25: 1389-395. DOI: 10.1080/01431160310001592346. - 46.
Merico A, Tyrrell T, Lessard EJ, Oguz T, Stabeno PJ, Zeeman SI, Whitledge TE. Modelling phytoplankton succession on the Bering Sea shelf ecosystem: Role of climate influences and trophic interactions in generating Emiliania huxleyi blooms 1997–2000. Deep-Sea Research. I. 2004; 51: 1803–1826. DOI: 10.1016/j.dsr.2004.07.003. - 47.
Palenik B, Dyrhman S. Recent progress in understanding the regulation of marine primary productivity by phosphorus, p. 26–38. In: Lynch JP, Deikman J. editors. Phosphorus in plant biology: Regulatory roles in molecular, cellular, organismic and ecosystem processes. American Society of Plant Physiologists, Rockville, MD, 1998. pp. 26–38. - 48.
Berman T, Bronk DA. Dissolved organic nitrogen: A dynamic participant in aquatic ecosystems. Aquat. Microb. Ecol. 2003; 31: 279–305. DOI: 10.2003/31/a031p279. - 49.
Palenik B, Henson SE. The use of amides and other organic nitrogen sources by the phytoplankton Emiliania huxleyi . Limnol. Oceanogr. 1997; 42: 1544–1551. DOI: 10.4319/lo.1997.42.7.1544. - 50.
Ikis D. Temporal and spatial changes of primary productivity in the Sea of Marmara obtained by remote sensing. Middle East Technical University, Graduated School of Natural and Applied Sciences, Biology Section, Master Thesis, 2007. 49 p. - 51.
Turkoglu M, Tugrul S. Long time variations of chlorophyll a and nutrients in the coastal waters of the Sea of Marmara. Rapp. Comm. Int. Mer Medit. 2013; 40: 900–900. - 52.
Balkis N. List of phytoplankton of the Sea of Marmara. J. Black Sea/Mediterranean Environment. 2004; 10: 123–141. - 53.
Tyrrell T, Taylor AH. A modelling study of Emiliania huxleyi in the NE Atlantic. J. Mar. Syst. 1996; 9: 83–112. DOI: 10.1016/0924-7963(96)00019-X. - 54.
Tyrrell T, Merico A. Emiliania huxleyi : Bloom observations and the conditions that induce them. In: Thierstein HR, Young JR. editors. Coccolithophores: from molecular processes to global impact. Berlin, German: Springer; 2004. 75–97 p. - 55.
Aubert M, Revillon P, Aubert J, Leger G, Drai C, Arnoux A, Diana C. Transfert de pollutants entre la Mer Noire, la Mer de Marmara et la Mer Egée. Mers D’Europe. Etudes hydrobiologiques, chimiques et biologiques, Volume 3, Nice: CERBOM, Rev. Int. Ocean. Méd., 1990. 57 p. - 56.
Besiktepe S, Sur HI, Ozsoy E, Latif MA, Oguz T, Unluata U. The circulation and hydrography of the Marmara Sea. Progress in Oceanography. 1994; 34: 285–334. DOI: 10.1016/0079-6611(94)90018-3. - 57.
Polat SC, Tugrul S. Chemical exchange between the Mediterranean and Black Sea via the Turkish strait. Bull. Inst. Oceanography. 1996; 17: 167-186. - 58.
Jacquet S, Heldal M, Iglesias-Rodriguez D, Larsen A, Wilson W, Bratbak G. Flow cytometric analysis of an Emiliania huxleyi bloom terminated by viral infection. Aquat. Microb. Ecol. 2002; 27:111–124. DOI: 10.3354/ame027111. - 59.
Wilson WH, Tarran GA, Schroeder D, Cox M, Oke J, Malin G. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. U.K. 2002; 82:369–377. DOI: 10.1017/S0305004102005534. - 60.
Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature. 1999; 399: 541–548. DOI: 10.1038/21119. - 61.
Wommack KE, Colwell RR. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 2000; 64:69–114. DOI: 10.1128/MMBR.64.1.69114.2000. - 62.
Cottrell MT, Suttle CA. Genetic diversity of algal viruses which lyse the photosynthetic picoflagellate Micromonas pusilla (Prasinophyceae). Appl. Environ. Microbiol. 1995; 61:3088–3091. - 63.
Cottrell MT, Suttle CA. Widespread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan, eukaryotic marine phytoplankter, Micromonas pusilla . Mar. Ecol. Prog. Ser. 1991; 78:1–9. - 64.
Short SM, Suttle CA. Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl. Environ. Microbiol. 2002; 68:1290–1296. DOI: 10.1128/AEM.68.3.1290-1296.2002. - 65.
Tarutani K, Nagasaki K, Yamaguchi M. Viral impacts on total abundance and clonal composition of the harmful bloom-forming phytoplankton Heterosigma akashiwo . Appl. Environ. Microbiol. 2000; 66:4916–4920. DOI: 0.1007/978-0-387-95919-1_208. - 66.
Bratbak G, Egge JK, Heldal M. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 1993; 93:39–48. - 67.
Bratbak G, Wilson W, Heldal M. Viral control of Emiliania huxleyi blooms? J. Mar. Syst. 1996; 9:75–81. - 68.
Brussaard CPD, Kempers RS, Kop AJ, Riegman R, Heldal M. Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat. Microb. Ecol. 1996; 10:105–113. - 69.
Castberg T, Larsen A, Sandaa RA, Brussaard CPD, Egge JK, Heldal M, Thyrhaug R, van Hannen EJ, Bratbak G. Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Mar. Ecol. Prog. Ser. 2001; 221:39–46. - 70.
Castberg T, Thyrhaug R, Larsen A, Sandaa RA, Heldal M, Van Etten JL, Bratbak G. Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). J. Phycol. 2002; 38:767–774. DOI: 10.1046/j.1529-8817.2002.02015.x. - 71.
Van Etten JL, Graves MV, Muller DG, Boland W, Delaroque N. Phycodnaviridae—large DNA algal viruses. Arch. Virol. 2002; 147:1479–1516. DOI: 10.1007/s00705-002-0822-6. - 72.
Schroeder DC, Oke J, Malin G, Wilson WH. Coccolithovirus (Phycodnaviridae): characterisation of a new large dsDNA algal virus that infects Emiliania huxleyi . Arch. Virol. 2002; 147:1685–1698. DOI: 10.1007/s00705-002-0841-3. - 73.
Schroeder DC, Oke J, Hall M, Malin G, Wilson WH, Virus succession observed during an Emiliania huxleyi bloom. Applied and Environmental Microbiology. 2003; 69: 2484–2490. DOI: 10.1128/AEM.69.5.2484-2490.2003. - 74.
Turkoglu M, Buyukates Y, Kaya S. Blooms of Coccolithophore Emiliania huxleyi and Some Dinoflagellates in the Dardanelles, Turkey. Turkish Journal of Aquatic Science. 2004b; 2 (3): 423–423 (in Turkish). - 75.
Brown CW, Yoder JA. Coccolithophorid blooms in the global ocean. J. Geophys. Res. 1994; 99: 7467–7482. DOI: 10.1029/93JC02156. - 76.
Turkoglu M. Short time variations of chlorohyll a and nutrients in the Dardanelles, Turkey. Rapp. Comm. Int. Mer Medit., 2010c; 39: 411-411. - 77.
Turkoglu M. Temporal variations of surface phytoplankton, nutrients and chlorophyll-a in the Dardanelles (Turkish Straits System): A coastal station sample in weekly time intervals. Turk J Bio. 2010d; 34 (3): 319–333. DOI:10.3906/biy-0810-17. - 78.
Turkoglu M. Hyper-eutrophycation and Intensive Foam Formation in the Dardanelles, Turkey. OMICS Group Conferences, Hydrology & Ground Water Expo; September 10–12, 2012, Hilton San Antonio Airport, Los Angeles, USA: 2012. p. 38–38. - 79.
Turkoglu M. First bloom record of toxic dinoflagellate Prorocentrum lima (Ehrenberg) F. Stein, 1878 and climate change interactions in the Dardanelles (Turkish Straits Sistem). OMICS Group Conferences, 4th International Conference on Earth Science & Climatic Change; June 16–18, 2015; Alicante, Valencia, Spain: 2015. p. 40–40. - 80.
Turkoglu M, Erdogan Y. Daily variations of summer phytoplankton in the Dardanelles. Rapp. Comm. Int. Mer Medit. 2007; 38: 399–399.