Water residence time and the dynamics of toxic cyanobacteria

Freshwater Biology

Volumn 58, Issue 3, 2013, Pages 513-522

  Romo, Susana ^a   Soria, Juan ^a   Fernández, Francisca ^b   Ouahid, Youness ^b   Barón Solá, Ángel ^b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Mediterranean; Microcystin; Microcystis; Restoration; Shallow lake

Indexed keywords

CYANOBACTERIA; MICROCYSTIS; MICROCYSTIS AERUGINOSA;

EID: 84873467068     PISSN: 00465070     EISSN: 13652427     Source Type: Journal    
DOI: 10.1111/j.1365-2427.2012.02734.x     Document Type: Article

References (63)

1. APHA (1992) Standard Methods for the Examination of Water and Wastewater, 18th edn. American Public Health Association, Washington, DC.
2. Arim M., Bozinovic F. & Marquet P.A. (2007) On the relationship between tropic position, body mass and temperature: reformulating the energy limitation hypothesis. Oikos, 116, 1524-1530.
3. Beklioglu M., Romo S., Kagalou I., Quintana X. & Bécares E. (2007) State of the art in the functioning of shallow Mediterranean lakes: workshop conclusions. Hydrobiologia, 584, 317-326.
4. Blanco S. & Romo S. (2006) Ictiofauna del lago de la Albufera de Valencia: evolución histórica y situación actual. Boletín Real Sociedad Española Historia Natural (Sección Biología.), 101, 45-56.
5. Blanco S., Romo S., Villena M.J. & Martínez S. (2003) Fish communities and food web interactions in six shallow Mediterranean lakes. Hydrobiologia, 506, 473-480.
6. Bradt S. & Villena M.J. (2002) Detection of microcystins in the coastal lagoon La Albufera de Valencia, Spain by an enzyme-linked immunosorbent assay (ELISA). Limnetica, 20, 187-196.
7. Butterwick C., Heaney S.I. & Talling J.F. (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshwater Biology, 50, 291-300.
8. Chorus I. (2001) Cyanotoxins: Occurrence, Causes, Consequences. Springer-Verlag, Berlin.
9. Chorus I. & Bartram J. (1999) Toxic Cyanobacteria in Water. A Guide to Public Health Consequences, Monitoring and Management. WHO, London.
10. Codd G.A., Lindsay J., Young F.M., Morrison L.F. & Metcalf J.S. (2005) Harmful cyanobacteria. From mass mortalities to management measures. In: Harmful Cyanobacteria (Eds J. Huisman, H. Matthijs & P. Visser ), pp. 1-23. Springer, The Netherlands.
11. Cook C., Vardaka E. & Lanaras T. (2004) Toxic cyanobacteria in Greek freshwaters, 1997-2000: Occurrence, toxicity and impacts in the Mediterranean region. Acta Hydrochimica et Hydrobiologica, 32, 107-124.
12. Davis T.W., Berry D.L., Boyer G.L. & Gobler C.J. (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae, 8, 715-725.
13. de Senerpont Domis L.N., Mooij W.M. & Huisman J. (2007) Climate-induced shifts in an experimental phytoplankton community: a mechanistic approach. Hydrobiologia, 584, 403-413.
14. Elliott J.A. (2010) The seasonal sensitivity of cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Global Change Biology, 16, 864-876.
15. Fastner J., Flieger I. & Neumann U. (1998) Optimised extraction of microcystins from field samples: a comparison of different solvents and procedures. Water Research, 32, 3177-3181.
16. Gkelis S., Harjunpää V., Lanaras T. & Sivonen K. (2005) Diversity of hepatotoxic microcystins and bioactive anabaenopeptins in cyanobacterial blooms from Greek freshwaters. Environmental Toxicology, 20, 249-256.
17. Gkelis S., Lanaras T. & Sivonen K. (2006) The presence of microcystins and other cyanobacterial bioactive peptides in aquatic fauna collected from Greek freshwaters. Aquatic Toxicology, 78, 32-41.
18. Gyllström M., Hansson L.A., Jeppesen E., García-Criado F., Gross E., Irvine K. et al. (2005) The role of climate in shaping zooplankton communities of shallow lakes. Limnology and Oceanography, 50, 2008-2021.
19. Hansson L.A. (1996) Algal recruitment from lake sediments in relation to grazing, sinking and dominance patterns in the phytoplankton community. Limnology and Oceanography, 41, 1312-1323.
20. Harvey L.D.D. (2000) Climate and Global Environmental Change. Prentice Hall, London.
21. Hillebrand H., Urselen C., Kirschtel D., Pollingher U. & Zohary T. (1999) Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35, 403-424.
22. Huisman J., Matthijs H. & Visser P. (Eds) (2005) Harmful Cyanobacteria. Springer, The Netherlands.
23. IUCN (the World Conservation Union) (2002) Report on Climate Change, Water and Wetlands: Building Linkages for Their Integrated Management. The World Conservation Union, Geneva.
24. Jagtman E., Van Der Molen D.T. & Vermij S. (1992) The influence of flushing on nutrient dynamics, composition and densities of algae and transparency in Veluwemeer, The Netherlands. Hydrobiologia, 233, 187-196.
25. Jeppesen E., Søndergaard M. & Jensen J.P. (2003) Climatic warming and regime shifts in lake food webs-some comments. Limnology and Oceanography, 48, 1346-1349.
26. Jöhnk K.D., Huisman J., Sharples J., Sommeijer B., Visser P.M. & Stroom J.M. (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology, 14, 495-512.
27. Kagalou I., Papadimitriou T., Bacopoulos V. & Leonardos I. (2008) Assessment of microcystins in lake water and the omnivorous fish (Carassius gibelio, Bloch) in Lake Pamvotis (Greece) containing dense cyanobacterial bloom. Environmental Monitoring and Assessment, 137, 185-195.
28. Kardinaal W. & Visser P. (2005) Dynamics of cyanobacterial toxins. Sources of variability in microcystin concentrations. In: Harmful Cyanobacteria (Eds J. Huisman, H. Matthijs & P. Visser ), pp. 41-64. Springer, The Netherlands.
29. Kardinaal W.E.A., Tonk L., Janse I., Hol S., Slot P., Huisman J. et al. (2007) Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Applied and Environmental Microbiology, 73, 2939-2946.
30. Kosten S., Huszar V., Bécares E., Costa L., van Donk E., Hansson L.-A. et al. (2012) Warmer climate boosts cyanobacterial dominance in lakes. Global Change Biology, 18, 118-126.
31. Kotak B.G., Lam A.K., Prepas E.E., Hrudey S.E. & Kenefick S.L. (1995) Variability of the hepatotoxin, microcystin-LR, in hypereutrophic drinking water lakes. Journal of Phycology, 31, 248-263.
32. Meijer M.L. & Hosper H. (1997) Effects of biomanipulation in the large and shallow lake Wolderwijd, the Netherlands. Hydrobiología, 342/343, 335-349.
33. Mooij W.M., Huisman J., de Senerpont Domis L., Nolet P., Bodelier P., Boers M.L. et al. (2005) The impact of climate change on lakes in the Netherlands: a review. Aquatic Ecology, 39, 381-400.
34. Mooij W.M., Janse J.H., de Senerpont Domis L.N., Hülsmann S. & Ibelings B.W. (2007) Predicting the effect of climate change on temperate shallow lakes with the ecosystem model PCLake. Hydrobiología, 584, 443-454.
35. Moss B. (1998) Ecology of freshwaters. Man and Medium, Past to Future, 3rd edn. Blackwell Science, Oxford.
36. Moss B., Stephen D., Balayla D.M., Bécares E., Collings S.E., Fernández-Aláez C. et al. (2004) Continental-scale patterns of nutrient and fish effects on shallow lakes: synthesis of a pan-European mesocosm experiment. Freshwater Biology, 49, 1633-1649.
37. Ouahid Y. & Fernández F. (2009) Typing of toxinogenic Microcystis from environmental samples by multiplex PCR. Applied Microbiology and Biotechnology, 85, 405-412.
38. Özen A., Karapinar B., Kucuk I., Jeppesen E. & Beklioglu M. (2010) Drought-induced changes in nutrient concentrations and retention in two shallow Mediterranean lakes subjected to different degrees of management. Hydrobiologia, 646, 61-72.
39. Paerl H.W. (1988) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnology and Oceanography, 33, 823-847.
40. Paerl H. & Huisman J. (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports, 1, 27-37.
41. Papadimitriou T., Kagalou I., Bacopoulos V. & Leonardos I. (2010) Accumulation of microcystins in water and fish tissues: an estimation of risks associated with microcystins in most of the Greek lakes. Environmental Toxicology, 25, 418-427.
42. Reynolds C.S. (1997). Vegetation process in the pelagic: a model for ecosystem theory. In: Excellence in Ecology (Ed Kinne O.), pp. 1-371. ECI Series, Oldendorf.
43. Romo S. & Miracle M.R. (1993) Long-term periodicity of Planktothrix agardhii, Pseudanabaena galeata and Geitlerinema sp. in a shallow hypertrophic lagoon, Albufera of Valencia (Spain). Archiv für Hydrobiologie, 126, 469-486.
44. Romo S. & Villena M.J. (2005) Phytoplankton strategies and diversity under different nutrient levels and planktivorous fish densities in a shallow Mediterranean lake. Journal of Plankton Research, 27, 1273-1286.
45. Romo S., Miracle R., Villena M.J., Rueda J., Ferriol C. & Vicente E. (2004) Mesocosm experiments on nutrient and fish effects on shallow lake food webs in a Mediterranean climate. Freshwater Biology, 49, 1593-1607.
46. Romo S., Villena M.J., Sahuquillo M., Soria J., Giménez M., Alfonso T. et al. (2005) Response of a shallow Mediterranean lake to nutrient diversion: does it follow similar patterns as northern shallow lakes? Freshwater Biology, 50, 1706-1717.
47. Romo S., García-Murcia A., Villena M.J., Sánchez V. & Ballester A. (2008) Tendencias del fitoplancton en el lago de la Albufera de Valencia e implicaciones para su ecología, gestión y recuperación. Limnetica, 27, 11-28.
48. Romo S., Fernández F., Ouahid Y. & Barón-Solá A. (2011) Assessment of microcystins in lake water and fish (Mugilidae, Liza sp.) in the largest Spanish coastal lake. Environmental Monitoring and Assessment. Doi: 10.1007/s10661-011-2011-0.
49. Sánchez E., Gallardo C., Gaertner M.A., Arribas A. & Castro M. (2004) Future climate extreme events in the Mediterranean simulated by a regional climate model: a first approach. Global and Planetary Change, 44, 163-180.
50. Søndergaard M., Jensen J.P. & Jeppesen E. (2003) Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia, 506, 135-145.
51. Soria J.M. & Vicente E. (2002) Estudio de los aportes hídricos al parque natural de la Albufera. Limnetica, 21, 105-115.
52. Tonk L., Bosch K., Visser P.M. & Huisman J. (2007) Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquatic Microbial Ecology 46, 117-123.
53. Van de Waal D.B., Verspagen J.M.H., Lürling M., Van Donk E., Visser P. & Huisman J. (2009) The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecology Letters, 12, 1326-1355.
54. Vardaka E., Moustaka-Gouni M., Cook C.M. & Lanaras T. (2005) Cyanobacterial blooms and water quality in Greek waterbodies. Journal of Applied Phycology, 17, 391-401.
55. Verspagen J.M.H., Snelder E., Visser P.M., Huisman J., Mur L.R. & Ibelings B.W. (2004) Recruitment of benthic Microcystis (Cyanophyceae) to the water column: internal buoyancy changes or resuspension? Journal of Phycology, 40, 260-270.
56. Verspagen J.M.H., Snelder E., Visser P.M., Jöhnk K.D., Ibelings B.W., Mur L.R. et al. (2005) Benthic-pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis. Freshwater Biology, 50, 854-867.
57. Verspagen J.M.H., Passarge J., Jöhnk K.D., Visser P.M., Peperzak L., Boers P. et al. (2006) Water management strategies against toxic Microcystis blooms in the Dutch delta. Ecological Applications, 16, 313-327.
58. Villena M.J. & Romo S. (2003) Temporal changes of cyanobacteria in the largest coastal Spanish Lake. Archiv für Hydrobiologie, 109, 593-608.
59. Visser P., Ibelings B., Mur L. & Walsby A. (2005) The ecophysiology of the harmful cyanobacterium Microcystis. Features explaining its success and measures for its control. In: Harmful Cyanobacteria (Eds Huisman J., Matthijs H. & Visser P.), pp. 109-142. Springer-Verlag, The Netherlands.
60. Wagner C. & Adrian R. (2009) Cyanobacteria dominance: quantifying the effects of climate change. Limnology and Oceanography, 54, 2460-2468.
61. Welker M., von Döhren H., Tauscher H., Steinberg C.E.W. & Erhard M. (2003) Toxic Microcystis in shallow Lake Müggelsee (Germany): dynamics, distribution, diversity. Archiv für Hydrobiology, 157, 227-248.
62. WHO (2003) Guidelines for Safe Recreational Water Environments. Coastal and Freshwaters. WHO Document, Geneva.
63. Wiedner C., Visser P.M., Fastner J., Metcalf J.S., Codd G.A. & Mur L.R. (2003) Effects of light on the microcystin content of Microcystis strain PCC 7806. Applied and Environmental Microbiology, 69, 1475-1481.