Pilot application of drone observations and pigment marker detection by HPLC in studies of cyanobacterial harmful algal blooms in Bulgarian inland waters

References

Ballot, A., Bernard, C., and Fastner, J. (2017). Saxitoxin and analogues. In ‘Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis’. (Eds J. Meriluoto, L. Spoof, and G. A. Codd.) pp. 148–154. (Wiley: Singapore.)

Boon, M. A., Greenfield, R., and Tefamichael, S. (2016). Wetland assessment using unmanned aerial vehicle (UAV) photogrammetry. The International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences XLI, 781–788.
| Wetland assessment using unmanned aerial vehicle (UAV) photogrammetry.Crossref | GoogleScholarGoogle Scholar |

Carmichael, W. W. (1994). The toxins of cyanobacteria. Scientific American 270, 78–86.
| The toxins of cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 8284661PubMed |

Carmichael, W. W., and Boyer, G. L. (2016). Health impacts from cyanobacteria harmful algae blooms: implications for the North American Great Lakes. Harmful Algae 54, 194–212.
| Health impacts from cyanobacteria harmful algae blooms: implications for the North American Great Lakes.Crossref | GoogleScholarGoogle Scholar | 28073476PubMed |

Carvalho, L., McDonald, C., de Hoyos, C., Mischke, U., Phillips, G., Borics, G., Poikane, S., Skjelbred, B., Solheim, A. L., Van Wichelen, J., and Cardoso, A. C. (2013). Sustaining recreational quality of European lakes, minimizing the health risks from algal blooms through phosphorus control. Journal of Applied Ecology 50, 315–323.
| Sustaining recreational quality of European lakes, minimizing the health risks from algal blooms through phosphorus control.Crossref | GoogleScholarGoogle Scholar |

Catherine, A., Bernard, C., Spoof, L., and Bruno, M. (2017). Microcystins and nodularins. In ‘Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis’. (Eds J. Meriluoto, L. Spoof, and G. A. Codd.) pp. 109–126. (Wiley: Singapore.)

Chorus, I., and Bartram, J. (Eds) (1999). ‘Toxic Cyanobacteria in Water. A Guide to their Public Health Consequences, Monitoring and Management.’ (WHO and CRC Press: Boca Raton, FL, USA.)

Codd, G. A. (1995). Cyanobacterial toxins: occurrence, properties and biological significance. Water Science and Technology 32, 149–156.
| Cyanobacterial toxins: occurrence, properties and biological significance.Crossref | GoogleScholarGoogle Scholar |

Codd, G. A., Bell, S. G., and Brooks, W. P. (1989). Cyanobacterial toxins in water. Water Science and Technology 21, 1–13.
| Cyanobacterial toxins in water.Crossref | GoogleScholarGoogle Scholar |

Codd, G. A., Bell, S. G., Kaya, K., Ward, C. J., Beattie, K. A., and Metcalf, J. S. (1999). Cyanobacterial toxins, exposure routes and human health. European Journal of Phycology 34, 405–415.
| Cyanobacterial toxins, exposure routes and human health.Crossref | GoogleScholarGoogle Scholar |

Codd, G. A., Morrison, L. F. M., and Metcalf, J. S. (2005a). Cyanobacterial toxins: risk management for health protection. Toxicology and Applied Pharmacology 203, 264–272.
| Cyanobacterial toxins: risk management for health protection.Crossref | GoogleScholarGoogle Scholar | 15737680PubMed |

Codd, G. A., Lindsay, J., Young, F. M., Morrison, L. F. M., and Metcalf, J. S. (2005b). Harmful cyanobacteria. From mass mortalities to management measures. In ‘Harmful Cyanobacteria’. (Eds J. Huisman, H. C. P. Matthijs, and P. M. Visser.) pp. 1–23. (Springer: Dordrecht, Netherlands.)

Descy, J. P. (2017). SOP5: estimation of cyanobacteria biomass by marker pigment analysis. In ‘Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis’, 1st edn. (Eds J. Meriluoto, J. Codd, and L. Spoof.) pp. 343–349. (Wiley: Singapore.)

Descy, J.-P., Higgins, H. W., Mackey, D. J., Hurley, J. P., and Frost, T. M. (2000). Pigment ratios and phytoplankton assessment in northern Wisconsin lakes. Journal of Phycology 36, 274–286.
| Pigment ratios and phytoplankton assessment in northern Wisconsin lakes.Crossref | GoogleScholarGoogle Scholar |

Descy, J. P., Leprieur, F., Pirlot, S., Leporcq, B., Van Wichelen, J., Peretyatko, A., Teissier, S., Codd, G. A., Triest, L., Vyverman, W., and Wilmotte, A. (2016). Identifying the factors determining blooms of cyanobacteria in a set of shallow lakes. Ecological Informatics 34, 129–138.
| Identifying the factors determining blooms of cyanobacteria in a set of shallow lakes.Crossref | GoogleScholarGoogle Scholar |

Descy, J.-P., Stoyneva-Gärtner, M. P., Uzunov, B. A., Dimitrova, P. H., Pavlova, V. Ts., and Gärtner, G. (2018). Studies on cyanoprokaryotes of the water bodies along the Bulgarian Black Sea Coast (1890–2017): a review, with special reference to new, rare and harmful taxa. Acta Zoologica Bulgarica 11, 43–52.

Dimitrova, R. E., Nenova, E. P., Uzunov, B. A., Shihiniova, M. D., and Stoyneva, M. P. (2014a). Phytoplankton abundance and structural parameters of the critically endangered protected area Vaya Lake (Bulgaria). Biotechnology, Biotechnological Equipment 28, 871–877.
| Phytoplankton abundance and structural parameters of the critically endangered protected area Vaya Lake (Bulgaria).Crossref | GoogleScholarGoogle Scholar |

Dimitrova, R. E., Nenova, E. P., Uzunov, B. A., Shihiniova, M. D., and Stoyneva, M. P. (2014b). Phytoplankton composition of Vaya Lake (2004–2006). Bulgarian Journal of Agricultural Science 1, 165–172.

Dimitrova, P. H., Stoyneva-Gärtner, M. P., Uzunov, B. A., and Gärtner, G. (2018). Review of the algological studies of Bulgarian Black Sea coastal water bodies (1890–2017) with special attention to the newly described and threatened species. Acta Zoologica Bulgarica 11, 27–42.

Downing, J. A., Watson, S. B., and McCauley, E. (2001). Predicting cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences 58, 1905–1908.
| Predicting cyanobacteria dominance in lakes.Crossref | GoogleScholarGoogle Scholar |

Elliott, J. A. (2012). Is the future blue–green? A review of the current model predictions of how climate change could affect pelagic freshwater cyanobacteria. Water Resources Journal 46, 1364–1371.

Forsberg, C., Ryding, S. O., Claesson, A., and Forsberg, A. (1978). Water chemical analyses and/or algal assay? Sewage efficient and polluted water studies. Mitteilungen – Internationale Vereinigung Für Theoretische und Angewandte Limnologie 21, 352–363.

Gons, H. J., Hakvoort, H., Peters, S. M. W., and Simis, S. G. H. (2005). Optical detection of cyanopbacterial blooms. Shipboard observation and remote sensing. In ‘Harmful Cyanobacteria.’ (Eds J. Huisman, H. C. P. Matthijs, and P. M. Visser.) pp. 177–199. (Springer: Dordrecht, Netherlands.)

Graham, L. E., Graham, J. M., and Wilcox, L. W. (2009). ‘Algae.’ (Benjamin Cummings: Munich, Germany.)

International Organization for Standardization (2005). ISO 20179:2005. Water quality – determination of microcystins – method using solid phase extraction (SPE) and high performance liquid chromatography (HPLC) with ultraviolet (UV) detection. ISO/TC 147/SC 2 Physical, Chemical and Biochemical Methods, Technical Committee, International Organization for Standardization. Available at https://www.iso.org/standard/34098.html [Verified 6 May 2019].

Jeffrey, S. W., Mantoura, R. F. C., and Wright, S. W. (1997). ‘Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods.’ (Scientific Committee on Organic Research, UNESCO: Paris, France.)

Jung, S., Cho, H., Kim, D., Kim, K., Han, J.-I., and Muyng, H. (2017). Development of algal bloom removal system using unmanned aerial vehicle and surface vehicle. IEEE Access – Practical Innovations, Open Solutions 5, 22166–22176.
| Development of algal bloom removal system using unmanned aerial vehicle and surface vehicle.Crossref | GoogleScholarGoogle Scholar |

Kokociński, M., Cameán, M. A., Carmeli, S., Guzmán-Guillén, R., Jos, A., Mankiewicz-Boczek, J., Metcalf, S. J., Moreno, M. I., Prieto, I. A., and Sukenik, A. (2017a). Cylindrospermopsin and congeners. In ‘Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis’, 1st edn. (Eds J. Meriluoto, L. Spoof, and G. A. Codd.) pp. 127–137. (Wiley: Singapore.)

Kokociński, M., Akçaalan, R., Salmaso, N., Stoyneva-Gärtner, M., and Sukenik, A. (2017b). Expansion of alien/invasive cyanobacteria. In ‘Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis’. (Eds J. Meriluoto, L. Spoof, and G. A. Codd.) pp. 28–40. (Wiley: Singapore.)

Liyanage, H. M., Arachchi, D. N., Abeysekara, T., and Guneratne, L. (2016). Toxicology of freshwater cyanobacteria. Journal of Environmental Science and Health – C. Environmental Carcinogenesis and Ecotoxicology Reviews 34, 137–168.
| Toxicology of freshwater cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 27229761PubMed |

Mackey, M. D., Mackey, D. J., Higgins, H. W., and Wright, S. W. (1996). CHEMTAX – a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Marine Ecology Progress Series 144, 265–283.
| CHEMTAX – a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Maršálek, B., Bláha, L., and Hindák, F. (2000). Review of toxicity of cyanobacteria in Slovakia. Biologia 55, 645–652.

Merel, S., Walker, D., Chicana, R., Snyder, S., Baurès, E., and Thomas, O. (2013). State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environment International 59, 303–327.
| State of knowledge and concerns on cyanobacterial blooms and cyanotoxins.Crossref | GoogleScholarGoogle Scholar | 23892224PubMed |

Meriluoto, J., and Codd, G. A. (Eds) (2005). ‘TOXIC: Cyanobacterial Monitoring and Cyanotoxin Analysis.’ (Åbo Akademi University Press: Turku, Finland.)

Metcalf, J. S., and Codd, G. A. (2012). Cyanotoxins. In ‘Ecology of Cyanobacteria II: Their Diversity in Space and Time’. (Ed. B. A. Whitton.) pp. 651–675. (Springer Science +Business Media BV: London, UK.)

Michev, T. M., and Stoyneva, M. P. (Eds) (2007). ‘Inventory of Bulgarian Wetlands and Their Biodiversity. Part 1: Non-Lotic Wetlands.’ (Publishing House Elsi-M: Sofia, Bulgaria.)

Mitrovic, S. M., Allis, O., Furey, A., and James, K. J. (2005). Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Cladophora fracta. Ecotoxicology and Environmental Safety 61, 345–352.
| Bioaccumulation and harmful effects of microcystin-LR in the aquatic plants Lemna minor and Wolffia arrhiza and the filamentous alga Cladophora fracta.Crossref | GoogleScholarGoogle Scholar | 15922800PubMed |

Mowe, M. A. D., Porojan, C., Abbas, F., Mitrovic, S. M., Lim, R. P., Furey, A., and Yeo, D. C. J. (2015). Rising temperatures may increase growth rates and microcystin production in tropical Microcystis species. Harmful Algae 50, 88–98.
| Rising temperatures may increase growth rates and microcystin production in tropical Microcystis species.Crossref | GoogleScholarGoogle Scholar |

Oliver, R. L., and Ganf, G. G. (2000). Freshwater blooms. In ‘The Ecology of Cyanobacteria. Their Diversity in Time and Space’. (Eds B. A. Whitton and M. Potts.) pp. 149–194. (Kluwer Academic Publishers: Dordrecht, Netherlands.)

Overbeck, J. (1988). Ecosystem concepts. In ‘Guidelines of Lake Management. Vol. 1. Principles of Lake Management’. (Eds S. E. Jørgensen and R. A. Vollenweider.) pp. 19–36. (International Lake Environment Committee and United Nations Environment Programme: Shiga, Japan.)

Paerl, H. W. (2001). Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climate pressures. Toxins 10, 1124–1134.

Paerl, H. W., Pinckney, J. L., Dyble, J., Valdes, L. M., Piehler, M. F., and Moisander, P. H. (2003). Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. Bioscience 53, 953–964.
| Phytoplankton photopigments as indicators of estuarine and coastal eutrophication.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., Hall, N. S., and Calandrino, E. S. (2011). Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. The Science of the Total Environment 409, 1739–1745.
| Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change.Crossref | GoogleScholarGoogle Scholar | 21345482PubMed |

Pavlova, V. (2007). Hygiene and analytical aspects of microcystins occurrence in surface water. Ph.D. Thesis, National Center of Public Health Protection, Sofia, Bulgaria. [In Bulgarian].

Pavlova, V., Babica, P., Todorova, D., Bratanova, Z., and Maršalek, B. (2006). Contamination of some reservoirs and lakes in Republic of Bulgaria by microcystins. Acta Hydrochimica et Hydrobiologica 34, 437–441.
| Contamination of some reservoirs and lakes in Republic of Bulgaria by microcystins.Crossref | GoogleScholarGoogle Scholar |

Pavlova, V., Stoyneva, M., Babica, P., Kohoutek, J., and Bratanova, Z. (2007). Microcystins contamination and cyanoprokaryote blooms in some coastal Bulgarian wetlands. In ‘Conference Preprint Book of Second International Conference and Exhibition of Water Resources, Technologies and Services’, 6–7 June 2007, Sofia, Bulgaria. pp. 221–226. (Bulaqua: Sofia, Bulgaria.)

Pavlova, V., Stoyneva, M., and Bratanova, Z. (2013). Cyanoprokaryotes (Cyanobacteria) and cyanotoxins in some Bulgarian reservoirs. Journal of Balkan Ecology 16, 257–260.

Pavlova, V., Stoyneva, M., Georgieva, V., Donchev, D., Spoof, L., Meriluoto, J., Bratanova, Z., and Karadjova, I. (2014). New records of microcystins in some Bulgarian water bodies of health and conservational importance. Journal of Water Resource and Protection 6, 446–453.
| New records of microcystins in some Bulgarian water bodies of health and conservational importance.Crossref | GoogleScholarGoogle Scholar |

Pavlova, V., Stoyneva-Gärtner, M., Uzunov, B., Bratanova, Z., Lazarova, A., and Karadjova, I. (2015). Microcystins-LR, -YR and -RR in six Bulgarian water bodies of health and conservational importance (2012–2014). Journal of Water Resource and Protection 7, 1375–1386.
| Microcystins-LR, -YR and -RR in six Bulgarian water bodies of health and conservational importance (2012–2014).Crossref | GoogleScholarGoogle Scholar |

Petkoff, S. (1898). Contribution to the investigation of Bulgarian single-celled green freshwater algae. Periodichno Spisanie Bulgarsko Knizhovno Druzhestvo 57, 111–135.

Ragueno, N., Ford, R., and Vodacek, A. (2017). Investigating harmful algal blooms using: satellites, drones, boats, citizen science. In ‘2017 STRATUS Workshop’, 19–20 October 2017, Rochester, NY, USA. pp. 1–22. Available at http://proceedings.esri.com/library/userconf/proc17/papers/2017_488.pdf [Verified 4 April 2019].

Reynolds, C. S., Huszar, V., Kruk, C., Naselli-Flores, L., and Melo, S. (2002). Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24, 417–428.
| Towards a functional classification of the freshwater phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Roelke, D., and Buyukates, Y. (2001). The diversity of harmful algal bloom-triggering mechanisms and the complexity of bloom initiation. Human and Ecological Risk Assessment 7, 1347–1362.
| The diversity of harmful algal bloom-triggering mechanisms and the complexity of bloom initiation.Crossref | GoogleScholarGoogle Scholar |

Salmaso, N., Bernard, C., Humbert, J. F., Akçalaan, R., Albay, M., Ballot, A., Catherine, A., Fastner, J., Häggqvist, K., Horecká, M., Izydorszyk, K., Köker, L., Komárek, J., Maloufi, S., Mankiewisz-Boszek, J., Metcalf, S. J., Quesada, A., Quiblier, C., and Yéprémian, C. (2017). Basic guide to detection and monitoring of potentially toxic cyanobacteria. In ‘Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis’, 1st edn. (Eds J. Meriluoto, L. Spoof, and G. A. Codd.) pp. 46–49. (Wiley: Singapore.)

Sarmento, H., and Descy, J.-P. (2008). Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes. Journal of Applied Phycology 20, 1001–1011.
| Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes.Crossref | GoogleScholarGoogle Scholar |

Schlüter, L., Lauridsen, T. L., Krogh, G., and Jørgensen, T. (2006). Identification and quantification of phytoplankton groups in lakes using new pigment ratios – a comparison between pigment analysis by HPLC and microscopy. Freshwater Biology 51, 1474–1485.
| Identification and quantification of phytoplankton groups in lakes using new pigment ratios – a comparison between pigment analysis by HPLC and microscopy.Crossref | GoogleScholarGoogle Scholar |

Srivastava, A., Singh, S., Ahn, C. Y., Oh, H. M., and Asthana, R. K. (2013). Monitoring approaches for a toxic cyanobacterial bloom. Environmental Science & Technology 47, 8999–9013.
| Monitoring approaches for a toxic cyanobacterial bloom.Crossref | GoogleScholarGoogle Scholar |

Stoyneva, M. P. (2000a). Algological studies of Bulgarian coastal wetlands. I. Species composition of the phytoplankton of Durankulak and Shabla-Ezeretz lakes. In ‘Annual of Sofia University “St Kliment Ohridski”, Faculty of Biology, Book 2 – Botany 91’. pp. 27–48. (St Kliment Ohridski University Press: Sofia, Bulgaria.)

Stoyneva, M. P. (2000b). Planktic green algae of Bulgarian coastal wetlands. Hydrobiologia 438, 25–41.
| Planktic green algae of Bulgarian coastal wetlands.Crossref | GoogleScholarGoogle Scholar |

Stoyneva, M. P. (2003). Steady-state phytoplankton assemblages in shallow Bulgarian wetlands. Hydrobiologia 502, 169–176.
| Steady-state phytoplankton assemblages in shallow Bulgarian wetlands.Crossref | GoogleScholarGoogle Scholar |

Stoyneva, M. P. (2014). Contribution to the studies of the biodiversity of hydro- and aerobiontic prokaryotic and eukaryotic algae in Bulgaria. D.Sc. Thesis, Sofia University ‘St Kliment Ohridski’, Sofia, Bulgaria. [In Bulgarian, English summary].

Stoyneva, M. P. (2016). Allochtonous planctonic algae recorded in Bulgaria during the last 25 years and their possible dispersal agents. Hydrobiologia 764, 53–64.
| Allochtonous planctonic algae recorded in Bulgaria during the last 25 years and their possible dispersal agents.Crossref | GoogleScholarGoogle Scholar |

Stoyneva, M. P., Traykov, I. T., Tosheva, A. G., Uzunov, B. A., Zidarova, R. P., and Descy, J. P. (2015). Comparison of ecological state/potential assessment of 19 Bulgarian water bodies based on macrophytes and phytoplankton (2011–2012). Biotechnology Equipment 29, S33–S38.
| Comparison of ecological state/potential assessment of 19 Bulgarian water bodies based on macrophytes and phytoplankton (2011–2012).Crossref | GoogleScholarGoogle Scholar |

Stoyneva-Gärtner, M. P., Descy, J.-P., Latli, A., Uzunov, B., Pavlova, V., Bratanova, Zl., Babica, P., Maršálek, B., Meriluoto, J., and Spoof, L. (2017). Assessment of cyanoprokaryote blooms and of cyanotoxins in Bulgaria in a 15-years period (2000–2015). Advances in Oceanography and Limnology 8, 131–152.
| Assessment of cyanoprokaryote blooms and of cyanotoxins in Bulgaria in a 15-years period (2000–2015).Crossref | GoogleScholarGoogle Scholar |

Van Dolah, F. M., Roelke, D., and Greene, R. M. (2001). Health and ecological impacts of harmful algal blooms: risk assessment needs. Human and Ecological Risk Assessment 7, 1329–1345.
| Health and ecological impacts of harmful algal blooms: risk assessment needs.Crossref | GoogleScholarGoogle Scholar |

Van Wichelen, J., van Gremberghe, I., Vanormelingen, P., Debeer, A.-E., Leporcq, B., Menzel, D., Codd, G. A., Descy, J.-P., and Vyverman, W. (2010). Strong effects of amoebae grazing on the biomass and genetic structure of a Microcystis bloom (Cyanobacteria). Environmental Microbiology 12, 2797–2813.
| 20545742PubMed |

Vollenweider, R. A. (1993). Global problems of eutrophication and its control. In ‘Conservation and Management of Lakes (Symposia Biologica Hungarica 38)’. (Eds J. Sálanki and S. Herodek.) pp. 19–42. (Akadémiai Kiadó: Budapest, Hungary.)

Vollenweider, R. A., and Kerekes, J. (1982). ‘Eutrophication of Waters. Monitoring, Assessment and Control.’ (OECD: Paris, France.)

Walker, H. C. (2015). ‘Harmful Algal Blooms in Drinking Water. Removal of Cyanobacterial Cells and Toxins.’ (CRC Press: Boca Raton, FL, USA.)

Whitton, B. A., and Potts, M. (2012). Introduction to the Cyanobacteria. In ‘Ecology of Cyanobacteria II: Their Diversity in Space and Time’. (Ed. B. A. Whitton.) pp. 1–14. (Springer: London, UK.)

Williams, A. (2014). Seek & destroy. Combating algal blooms with unmanned ultrasonic technology. Water and Wastewater International. Available at https://www.lgsonic.com/wp-content/uploads/Water-Wastewater-International.pdf [Verified 15 September 2018].

World Health Organization (1998). ‘Guidelines for Drinking-Water Quality, Health Criteria and other Supporting Information. 2nd edn. Addendum to Vol. 2.’ (WHO: Geneva, Switzerland.)

Wright, S. W., and Jeffrey, S. W. (2006). Pigment markers for phytoplankton production. In ‘Marine Organic Matter: Biomarkers, Isotopes and DNA’. (Ed. J. H. Volhman.) pp. 71–104. (Springer Verlag: Berlin, Germany.)