Phytoplankton pigments and epifluorescence microscopy as tools for ecological status assessment in coastal and estuarine waters, within the Water Framework Directive

Marine Pollution Bulletin

Volumn 62, Issue 7, 2011, Pages 1484-1497

  Seoane, Sergio ^a   Garmendia, Maialen ^b   Revilla, Marta ^b   Borja, Ángel ^b   Franco, Javier ^b   Orive, Emma ^a   Valencia, Victoriano ^b  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b MARINE RESEARCH DIVISION   (Spain)

Author keywords

Epifluorescence microscopy; Eutrophication; HPLC CHEMTAX; Phytoplankton; Water Framework Directive

Indexed keywords

ANTHROPOGENIC ORIGIN; ECOLOGICAL STATUS; EPIFLUORESCENCE MICROSCOPY; ESTUARINE WATERS; HETEROTROPHIC CELLS; HPLC-CHEMTAX; PHYTOPLANKTON COMMUNITY; PHYTOPLANKTON COMPOSITION; PHYTOPLANKTON PIGMENTS; RAPID SCREENING; STUDY AREAS; TROPHIC CONDITIONS; VARIABILITY PATTERNS; WATER FRAMEWORK DIRECTIVE; WATER FRAMEWORK DIRECTIVES; WATER QUALITY MONITORING;

EUTROPHICATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; PHYTOPLANKTON; WATER CONSERVATION; WATER QUALITY;

ALGAE CONTROL;

CHLOROPHYLL A; FUCOXANTHIN; PERIDININ; PIGMENT; UNCLASSIFIED DRUG; ZEAXANTHIN;

COASTAL WATER; COMMUNITY RESPONSE; ECOLOGICAL IMPACT; ESTUARY; EUTROPHICATION; MICROSCOPY; PHOTOAUTOTROPHY; PHYTOPLANKTON; WATER QUALITY;

ARTICLE; BIOMASS; COASTAL WATERS; COMMUNITY STRUCTURE; CONTROLLED STUDY; CYANOBACTERIUM; DIATOM; DINOFLAGELLATE; ENVIRONMENTAL MONITORING; EPIFLUORESCENCE MICROSCOPY; ESTUARY; EUTROPHICATION; GEOGRAPHIC DISTRIBUTION; HAPTOPHYTA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NANOPLANKTON; NONHUMAN; ORGANISM COMMUNITY; PHYSICAL CHEMISTRY; PHYTOPLANKTON; PICOPLANKTON; POPULATION ABUNDANCE; RIVER BASIN; SEASONAL VARIATION; WATER QUALITY;

CHLOROPHYLL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ECOSYSTEM; ENVIRONMENTAL MONITORING; ENVIRONMENTAL POLICY; EUTROPHICATION; FRESH WATER; MICROSCOPY, FLUORESCENCE; PHYTOPLANKTON; PIGMENTS, BIOLOGICAL; SEAWATER; WATER POLLUTANTS, CHEMICAL; WATER POLLUTION;

EID: 79959351557     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2011.04.010     Document Type: Article

References (80)

1. Andersen J.H., Schluter L., Aertebjerg G. Coastal eutrophication: recent developments in definitions and implications for monitoring strategies. J. Plankton Res. 2006, 28:621-628.
2. Ansotegui A., Trigueros J.M., Orive E. The use of pigment signatures to assess phytoplankton assemblage structure in estuarine waters. Estuar. Coast. Shelf Sci. 2001, 52:689-703.
3. Ansotegui A., Sarobe A., Trigueros J.M., Urrutxurtxu I., Orive E. Size distribution of algal pigments and phytoplankton assemblages in a coastal-estuarine environment: contribution of small eukaryotic algae. J. Plankton Res. 2003, 25:341-355.
4. Bald J., Borja A., Muxika I., Franco J., Valencia V. Assessing reference conditions and physico-chemical status according to the European Water Framework Directive: a case-study from the Basque Country (Northern Spain). Mar. Pollut. Bull. 2005, 50:1508-1522.
5. Basque-Government, 2008. Udalplan 2008. Department of Environmental and Regional Planning, Basque Government. http://www.1.euskadi.net/udalplan/visor/viewer.htm.
6. Borja Á., Galparsoro I., Solaun O., Muxika I., Tello E.M., Uriarte A., Valencia V. The European Water Framework Directive and the DPSIR, a methodological approach to assess the risk of failing to achieve good ecological status. Estuar. Coast. Shelf Sci. 2006, 66:84-96.
7. Borja Á., Bricker S.B., Dauer D.M., Demetriades N.T., Ferreira J.G., Forbes A.T., Hutchings P., Jia X., Kenchington R., Marques J.C., Zhu C. Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. Mar. Pollut. Bull. 2008, 56:1519-1537.
8. Bricker S.B., Ferreira J.G., Simas T. An integrated methodology for assessment of estuarine trophic status. Ecol. Model. 2003, 169:39-60.
9. Calvo-Díaz A., Morán X.A.G., Suárez L.A. Seasonality of picophytoplankton chlorophyll a and biomass in the central Cantabrian Sea, southern Bay of Biscay. J. Mar. Syst. 2008, 72:271-281.
10. Carletti, A., Heiskanen, A.S., 2009. Water Framework Directive Intercalibration Technical Report. Part 3: Coastal and Transitional Waters. JRC Scientific and Technical Reports. European Communities, Luxembourg.
11. Costa L.S., Huszar V.L.M., Ovalle A.R. Phytoplankton functional groups in a tropical estuary: hydrological control and nutrient limitation. Estuar. Coasts 2009, 32:508-521.
12. Crane K.W., Grover J.P. Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities. J. Theor. Biol. 2010, 262:517-527.
13. Devlin M., Best M., Coates D., Bresnan E., O'Boyle S., Park R., Silke J., Cusack C., Skeats J. Establishing boundary classes for the classification of UK marine waters using phytoplankton communities. Mar. Pollut. Bull. 2007, 55:91-103.
14. Devlin M., Barry J., Painting S., Best M. Extending the phytoplankton tool kit for the UK Water Framework Directive: indicators of phytoplankton community structure. Hydrobiologia 2009, 633:151-168.
15. Domingues R.B., Barbosa A., Galvão H. Constraints on the use of phytoplankton as a biological quality element within the Water Framework Directive in Portuguese waters. Mar. Pollut. Bull. 2008, 56:1389-1395.
16. Duarte C.M., Agustí S., Gasol J.M., Vaqué D., Vázquez-Domínguez E. Effect of nutrient supply on the biomass structure of planktonic communities: an experimental test on a Mediterranean coastal community. Mar. Ecol. Prog. Ser. 2000, 206:87-95.
17. Eker-Develi E., Berthon J.F., Van Der Linde D. Phytoplankton class determination by microscopic and HPLC-CHEMTAX analyses in the southern Baltic Sea. Mar. Ecol. Prog. Ser. 2008, 359:69-87.
18. European Commission, 2003. CIS WFD Transitional and Coastal Waters - Typology, Reference Conditions and Classification Systems. Luxembourg.
19. Ferreira J.G., Bricker S.B., Simas T.C. Application and sensitivity testing of a eutrophication assessment method on coastal systems in the United States and European Union. J. Environ. Manage. 2007, 82:433-445.
20. Franco, J., 1994. Variabilidad espacio-temporal de la biomasa y producción del fitoplancton en el estuario de Urdaibai. Ph.D. Thesis Dissertation. University of the Basque Country, Spain.
21. Gameiro C., Cartaxana P., Brotas V. Environmental drivers of phytoplankton distribution and composition in Tagus Estuary, Portugal. Estuar. Coast. Shelf Sci. 2007, 75:21-34.
22. García A. Métodos avanzados de estadística aplicada 2005, Métodos Robustos y de Remuestreo, Madrid, Spain.
23. Garibotti I.A., Vernet M., Kozlowski W.A., Ferrario M.E. Composition and biomass of phytoplankton assemblages in coastal Antarctic waters: a comparison of chemotaxonomic and microscopic analyses. Mar. Ecol. Prog. Ser. 2003, 247:27-42.
24. Garmendia, M., Revilla, M., Bald, J., Franco, J., Laza-Martínez, A., Orive, E., Seoane, S., Valencia, V., Borja, Á., 2010. Phytoplankton communities and biomass size structure (fractionated chlorophyll " a" ), along trophic gradients of the Basque coast (northern Spain). Biogeochemistry. doi:10.1007/s10533-010-9445-2.
25. Gieskes W.W.C., Kraay G.W. Dominance of Cryptophyceae during the phytoplankton spring bloom in the central North Sea detected by HPLC analysis of pigments. Mar. Biol. 1983, 75:179-185.
26. Glibert P.M., Heil C.A., Hollander D., Revilla M., Hoare A.M., Alexander J., Murasko S. Evidence for dissolved organic nitrogen and phosphorus uptake during a cyanobacterial bloom in Florida Bay. Mar. Ecol. Prog. Ser. 2004, 28:73-83.
27. Haas L.W. Improved epifluorescence microscopy for observing planktonic micro-organisms. Analles del Institut Oceanographique de Paris 1982, 58:261-266.
28. Havskum H., Schluter L., Scharek R., Berdalet E., Jacquet S. Routine quantification of phytoplankton groups - microscopy or pigment analyses?. Mar. Ecol. Prog. Ser. 2004, 273:31-42.
29. Heil C.A., Revilla M., Glibert P.M., Murasko S. Nutrient quality drives differential phytoplankton community composition on the southwest Florida shelf. Limnol. Oceanogr. 2007, 52:1067-1078.
30. Henriksen, P., Revilla, M., Lehtinen, S., Kauppila, P., Kaitala, S., Agustí, S., Icely, J., Basset, A., Moncheva, S., Sorensen, K., 2011. WISER Deliverable D4.1-2: Assessment of Pigment Data Potential for Multi-Species and Assemblage Indices. http://www.wiser.eu/programme-and-results/deliverables/.
31. Huber P.J. Robust Statistics 1981, Wiley, New York.
32. Hunt C.D., Borkman D.G., Libby P.S., Lacouture R.V., Turner J.T., Mickelson M.J. Phytoplankton Patterns in Massachusetts Bay 1992-2007. Estuaries and Coasts 2010, 33:448-470.
33. Irigoien X., Meyer B., Harris R., Harbour D. Using HPLC pigment analysis to investigate phytoplankton taxonomy: the importance of knowing your species. Helgoland Mar. Res. 2004, 58:77-82.
34. Jaanus A., Toming K., Hällfors S., Kaljurand K., Lips I. Potential phytoplankton indicator species for monitoring Baltic coastal waters in the summer period. Hydrobiologia 2009, 629:157-168.
35. Jeffrey S.W. Chlorophyll and carotenoid extintion coefficients. Phytoplankton Pigments in Oceanography 1997, 595-596. UNESCO Publishing, Paris. S.W. Jeffrey, R.F.C. Mantoura, S.W. Wright (Eds.).
36. Latasa M., Scharek R., Le Gall F., Guillou L. Pigment suites and taxonomic groups in Prasinophyceae. J. Phycol. 2004, 40:1149-1155.
37. Laza-Martínez A., Seoane S., Zapata M., Orive E. Phytoplankton pigment patterns in a temperate estuary: from unialgal cultures to natural assemblages. J. Plankton Res. 2007, 29:913-929.
38. Lehman P.W. Environmental factors associated with long-term changes in chlorophyll concentration in the Sacramento-San Joaquin delta and Suisun bay, California. Estuaries 1992, 15:335-348.
39. Lionard M., Muylaert K., Tackx M., Vyverman W. Evaluation of the performance of HPLC-CHEMTAX analysis for determining phytoplankton biomass and composition in a turbid estuary (Schelde, Belgium). Estuar. Coast. Shelf Sci. 2008, 76(4):809-817.
40. Llewellyn C.A., Fishwick J.R., Blackford J.C. Phytoplankton community assemblage in the English Channel: a comparison using chlorophyll a derived from HPLC-CHEMTAX and carbon derived from microscopy cell counts. J. Plankton Res. 2005, 27(1):103-119.
41. Mackey M.D., Mackey D.J., Higgins H.W., Wright S.W. CHEMTAX - a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar. Ecol. Prog. Ser. 1996, 144:265-283.
42. Maier G., Glegg G.A., Tappin A.D., Worsfold P.J. The use of monitoring data for identifying factors influencing phytoplankton bloom dynamics in the eutrophic Taw Estuary, SW England. Mar. Pollut. Bull. 2009, 58:1007-1015.
43. Muylaert K., Gonzales R., Franck M., Lionard M., Van der Zee C., Cattrijsse A., Sabbe K., Chou L., Vyverman W. Spatial variation in phytoplankton dynamics in the Belgian coastal zone of the North Sea studied by microscopy, HPLC-CHEMTAX and underway fluorescence recordings. J. Sea Res. 2006, 55(4):253-265.
44. Muylaert K., Sabbe K., Vyverman W. Changes in phytoplankton diversity and community composition along the salinity gradient of the Schelde estuary (Belgium/The Netherlands). Estuar. Coast. Shelf Sci. 2009, 82:335-340.
45. Not F., Zapata M., Pazos Y., Campaña E., Doval M., Rodríguez F. Size-fractionated phytoplankton diversity in the NW Iberian coast: a combination of microscopic, pigment and molecular analyses. Aquat. Microb. Ecol. 2007, 49:255-265.
46. Olsen Y., Agustí S., Andersen T., Duarte C.M., Gasol J.M., Gismervik I., Heiskanen A.-S., Hoell E., Kuuppo P., Lignell R., Reinertsen H., Sommer U., Stibor H., Tamminen T. A comparative study of responses in planktonic food web structure and function in contrasting European coastal waters exposed to experimental nutrient addition. Limnol. Oceanogr. 2006, 51:488-503.
47. Paerl H.W., Valdes L.M., Pinckney J.L., Piehler M.F., Dyble J., Moisander P.H. Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. BioScience 2003, 53:953-964.
48. Pereira G.C., Figuiredo A.R., Jabor P.M., Ebecken N.F.F. Assessing the ecological status of plankton in Anjos Bay: a flow cytometry approach. Biogeosci. Discuss 2010, 7:6243-6264.
49. Porter K.G., Feig Y.S. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 1980, 25:943-948.
50. Revilla M., Iriarte A., Madariaga I., Orive E. Bacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary. Estuar. Coast. Shelf Sci. 2000, 50:297-313.
51. Revilla M., Ansotegui A., Iriarte A., Madariaga I., Orive E., Sarobe A., Trigueros J.M. Microplankton metabolism along a trophic gradient in a shallow-temperate estuary. Estuaries 2002, 25:6-18.
52. Revilla M., Franco J., Bald J., Borja Á., Laza A., Seoane S., Valencia V. The assessment of the phytoplankton ecological status in the Basque coast (northern Spain) according to the European Water Framework Directive. J. Sea Res. 2009, 61:60-67.
53. Revilla, M., Franco, J., Garmendia, M., Borja, Á., 2010a. A new method for phytoplankton quality assessment in the Basque estuaries (northern Spain), within the European Water Framework Directive. Revista de Investigación Marina17(7), 149-164. http://www.azti.es.
54. Revilla, M., Agustí, S., Garmendia, M., Kauppila, P., Kaitala, S., Lehtinen, S., 2010b. WISER Deliverable D4.1-1: Report on Identification of Typespecific Phytoplankton Assemblages for Three Ecoregions. http://www.wiser.eu/programme-and-results/deliverables/.
55. Rodríguez F., Pazos Y., Maneiro J., Zapata M. Temporal variation in phytoplankton assemblages and pigment composition at a fixed station of the Ría Pontevedra (NW Spain). Estuar. Coast. Shelf Sci. 2003, 58:499-515.
56. Sakka Hlaili A., Grami B., Niquil N., Gosselin M., Hamel D., Troussellier M., Hadj Mabrouk H. The planktonic food web of the Bizerte lagoon (south-western Mediterranean) during summer: I. Spatial distribution under different anthropogenic pressures. Estuar. Coast. Shelf Sci. 2008, 78:61-77.
57. Santos V.S., Villac M.C., Tenenbaum D.R., Paranhos R. Auto- and heterotrophic nanoplankton and filamentous bacteria of Guanabara Bay (RJ, Brazil): estimates of cell/filament numbers versus carbon content. Braz. J. Oceanogr. 2007, 55(2):133-143.
58. Sarmento H., Descy J. Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes. J. Appl. Phycol. 2008, 20:1001-1011.
59. Schlüter L., Mohlenberg F., Havskum H., Larsen S. The use of phytoplankton pigments for identifying and quantifying phytoplankton groups in coastal areas: testing the influence of light and nutrients on pigment/chlorophyll a ratios. Mar. Ecol. Prog. Ser. 2000, 192:49-63.
60. Seoane S., Laza A., Urrutxurtu I., Orive E. Phytoplankton assemblages and their dominant pigments in the Nervion River estuary. Hydrobiologia 2005, 549:1-13.
61. Seoane S., Laza A., Orive E. Monitoring phytoplankton assemblages in estuarine waters: the application of pigment analysis and microscopy to size-fractionated samples. Estuar. Coast. Shelf Sci. 2006, 67:343-354.
62. Seoane S., Zapata M., Orive E. Growth rates and pigment patterns of haptophytes isolated from estuarine waters. J. Plankton Res. 2009, 62:286-294.
63. Sherrard N.J., Nimmo M., Llewellyn C.A. Combining HPLC pigment markers and ecological similarity indices to assess phytoplankton community structure: an environmental tool for eutrophication?. Sci. Total Environ. 2006, 361:97-110.
64. Smayda T.J. Patterns of variability characterizing marine phytoplankton, with examples from Narragansett Bay. ICES J. Mar. Sci. 1998, 55:562-573. 10.1006/jmsc.1998.0385.
65. Smayda T.J., Reynolds C.S. Strategies of marine dinoflagellate survival and some rules of assembly. J. Sea Res. 2003, 49:95-106.
66. Smetacek V., Cloern J.E. On phytoplankton trends. Science 2008, 319:1346-1348. 10.1126/science.1151330.
67. Spatharis S., Tsirtsis G., Danielidis D.B., Chi T.D., Mouillot D. Effects of pulsed nutrient inputs on phytoplankton assemblage structure and blooms in an enclosed coastal area. Estuar. Coast. Shelf Sci. 2007, 73:807-815.
68. Ter Braak C.J.F., Smilauer P. CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (Version 4.5) 2002, Microcomputer Power, Ithaca, New York.
69. Tett P., Carreira C., Mills D.K., Van Leeuwen S., Foden J., Bresnan E., Gowen R.J. Use of a Phytoplankton Community Index to assess the health of coastal waters. ICES J. Mar. Sci. 2008, 65:1475-1482.
70. Trigueros J.M., Orive E. Seasonal variations of diatoms and dinoflagellates in a shallow, temperate estuary, with emphasis on neritic assemblages. Hydrobiologia 2001, 444:119-133.
71. Trigueros J.M., Ansotegui A., Orive E., Nó M.L. Morphology and distribution of two brackish diatoms, (Bacillariophyceae): Cyclotella atomus Hustedt and Thalassiosira guillardii Hasle in the estuary of Urdaibai (Northern Spain). Nove Hedwigia 2000, 70:431-450.
72. Utermöhl H. Zur Vervollkommung der quantitativen phytoplankton-methodik. Mitt. Internat. Verein. Limnol. 1958, 9:1-38.
73. Valencia V., Franco J. Main characteristics of the water masses. Oceanography and Marine Environment of the Basque Country. Elsevier Oceanography Series 2004, vol. 70:198-232. Elsevier, Amsterdam.
74. Van Lenning K., Latasa M., Estrada M., Saéz A.G., Medlin L., Probert I., Véron B., Young J. Pigments signatures phylogenetic relationships of the Pavlophyceae (Haptophyta). J. Phycol. 2003, 39:379-389.
75. Venables W.N., Ripley B.D. Modern Applied Statistics with S 2002, Springer-Verlag, Berlin. fourth ed.
76. Zapata M., Garrido J.L. Influence of injection conditions in reversed-phase high performance liquid chromatography of chlorophylls and carotenoids. Chromatographia 1991, 31:589-594.
77. Zapata M., Rodríguez F., Garrido J.L. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C-8 column and pyridine-containing mobile phases. Mar. Ecol. Prog. Ser. 2000, 195:29-45.
78. 2-MGDG). A novel marker pigment for Chrysochromulina species (Haptophyta). Mar. Ecol. Prog. Ser. 2001, 219:85-98.
79. Zapata M., Jeffrey S.W., Wright S.W., Rodríguez F., Garrido J.L., Clementson L. Photosynthetic pigments in 37 species (65 strains) of Haptophyta: implications for oceanography and chemotaxonomy. Mar. Ecol. Prog. Ser. 2004, 270:83-102.
80. Zapata M., Garrido J.L., Jeffrey S.W. Chlorophyll c pigments: current status. Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications 2006, 39-53. Springer, Dordrecht. B. Grimm, R.J. Porra, W. Rüdiger, U. Scheer (Eds.).