Recommendations for obtaining unbiased chlorophyll estimates from in situ chlorophyll fluorometers: A global analysis of WET Labs ECO sensors

Limnology and Oceanography: Methods

Volumn 15, Issue 6, 2017, Pages 572-585

  Roesler, Collin ^a   Uitz, Julia ^b   Claustre, Hervé ^b   Boss, Emmanuel ^c   Xing, Xiaogang ^d   Organelli, Emanuele ^b,e   Briggs, Nathan ^b   Bricaud, Annick ^b   Schmechtig, Catherine ^b   Poteau, Antoine ^b   D'Ortenzio, Fabrizio ^b   Ras, Josephine ^b   Drapeau, Susan ^a   Haëntjens, Nils ^c   Barbieux, Marie ^b  

^a BOWDOIN COLLEGE   (United States)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITY OF MAINE   (United States)

^d Chongqing Institute of Geology and Mineral Resources   (China)

^e PLYMOUTH MARINE LABORATORY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85018757217     PISSN: None     EISSN: 15415856     Source Type: Journal    
DOI: 10.1002/lom3.10185     Document Type: Article

References (82)

1. Antoine, D., F. d'Ortenzio, S. B. Hooker, G. Bécu, B. Gentili, D. Tailliez, and A. J. Scott. 2008. Assessment of uncertainty in the ocean reflectance determined by three satellite ocean color sensors (MERIS, SeaWiFS and MODIS-A) at an offshore site in the Mediterranean Sea (BOUSSOLE project). J. Geophys. Res. Oceans 113: 22. doi:10.1029/2007JC004472
2. Babin, M., A. Morel, and B. Gentili. 1996. Remote sensing of sea surface sun-induced chlorophyll fluorescence: Consequences of natural variations in the optical characteristics of phytoplankton and the quantum yield of chlorophyll a fluorescence. Int. J. Remote Sens. 17: 2417–2448. doi:10.1080/01431169608948781
3. Banse, K. 1977. Determining the carbon-to-chlorophyll ratio of natural phytoplankton. Mar. Biol. 41: 199–212. doi:10.1007/BF00394907
4. Banse, K., and D. C. English. 2000. Geographical differences in seasonality of CZCS-derived phytoplankton pigment in the Arabian Sea for 1978–1986. Deep-Sea Res. Part II Top. Stud. Oceanogr. 47: 1623–1677. doi:10.1016/S0967-0645(99)00157-5
5. Behrenfeld, M. J., and Z. S. Kolber. 1999. Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283: 840–843. doi:10.1126/science.283.5403.840
6. Behrenfeld, M. J., and E. Boss. 2006. Beam attenuation and chlorophyll concentration as alternative optical indices of phytoplankton biomass. J. Mar. Res. 64: 431–451. doi:10.1357/002224006778189563
7. Behrenfeld, M. J., K. Worthington, R. M. Sherrell, F. P. Chavez, P. Strutton, M. McPhaden, and D. M. Shea. 2006. Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics. Nature 442: 1025–1028. doi:10.1038/nature05083
8. Biogeochemical-Argo Planning Group. 2016. The scientific rationale, design and implementation plan for a Biogeochemical-Argo float array. In K. Johnson and H. Claustre [eds.]. doi:10.13155/46601
9. Booth, B. C. 1993. Estimating cell concentration and biomass of autotrophic plankton using microscopy, p. 199–205. In P. F. Kemp, B. F. Sherr, E. B. Sherr, and J. J. Cole [eds.] Handbook of methods in aquatic microbial ecology. Lewis Publishers.
10. Boss, E., D. Swift, L. Taylor, P. Brickley, R. Zaneveld, S. Riser, M. J. Perry, and P. G. Strutton. 2008. Observations of pigment and particle distributions in the western North Atlantic from an autonomous float and ocean color satellite. Limnol. Oceanogr. 53: 2112. doi:10.4319/lo.2008.53.5_part_2.2112
11. Boss, E., M. Picheral, T. Leeuw, A. Chase, E. Karsenti, G. Gorsky, L. Taylor, W. Slade, J. Ras, H. Claustre. 2013. The characteristics of particulate absorption, scattering and attenuation coefficients in the surface ocean; Contribution of the Tara Oceans expedition. Methods Oceanogr. 7: 52–62. doi:10.1016/j.mio.2013.11.002
12. Boss, E. B., and N. Haëntjens. 2016. Primer regarding measurements of chlorophyll fluorescence and the backscattering coefficient with WETLabs FLBB on profiling floats. SOCCOM Tech. Rep.
13. Bricaud, A., A. Morel, and L. Prieur. 1983. Optical efficiency factors of some phytoplankters. Limnol. Oceanogr. 28: 17. doi:10.4319/lo.1983.28.5.0816
14. Briggs, N., M. J. Perry, I. Cetinić, C. Lee, E. D'Asaro, A. M. Gray, and E. Rehm. 2011. High-resolution observations of aggregate flux during a sub-polar North Atlantic spring bloom. Deep-Sea Res. Part I Oceanogr. Res. Pap. 58: 1031–1039. doi:10.1016/j.dsr.2011.07.007
15. Cetinić, I., M. J. Perry, E. D'Asaro, N. Briggs, N. Poulton, M. E. Sieracki, and C. M. Lee. 2015. A simple optical index shows spatial and temporal heterogeneity in phytoplankton community composition during the 2008 North Atlantic Bloom Experiment. Biogeosciences 12: 2179–2194. doi:10.5194/bg-12-2179-2015
16. Claustre, H., A. Morel, M. Babin, C. Cailliau, D. Marie, J. C. Marty, D. Tailliez, and D. Vaulot. 1999. Variability in particle attenuation and chlorophyll fluorescence in the tropical Pacific: Scales, patterns, and biogeochemical implications. J. Geophys. Res. Oceans 104: 3401–3422. doi:10.1029/98JC01334
17. Claustre, H., and others. 2004. An intercomparison of HPLC phytoplankton pigment methods using in situ samples: Application to remote sensing and database activities. Mar. Chem. 85: 41–61. doi:10.1016/j.marchem.2003.09.002
18. Cloern, J. E., C. Grenz, and L. Vidergar-Lucas. 1995. An empirical model of the phytoplankton chlorophyll: Carbon ratio-the conversion factor between productivity and growth rate. Limnol. Oceanogr. 40: 1313–1321. doi:10.4319/lo.1995.40.7.1313
19. Coupel, P., D. Ruiz-Pino, M. A. Sicre, J. F. Chen, S. H. Lee, N. Schiffrine, H. L. Li, and J. C. Gascard. 2015. The impact of freshening on phytoplankton production in the Pacific Arctic Ocean. Prog. Oceanogr. 131: 113–125. doi:10.1016/j.pocean.2014.12.003
20. Crombet, Y., and others. 2011. Deep silicon maxima in the stratified oligotrophic Mediterranean Sea. Biogeosciences 8: 459–475. doi:10.5194/bg-8-459-2011
21. Cullen, J. C. 1982. The deep chlorophyll maximum: Comparing profiles of chlorophyll a. Can. J. Fish. Aquat. Sci. 39: 12. doi:10.1139/f82-108
22. Davis, R. F., C. C. Moore, J. R. V. Zaneveld, and J. M. Napp. 1997. Reducing the effects of fouling on chlorophyll estimates derived from long-term deployments of optical instruments. J. Geophys. Res. 102: 5. doi:10.1029/96JC02430
23. Do Rosário Gomes, H., J. I. Goes, S. G. P. Matondkar, E. J. Buskey, S. Basu, S. Parab, and P. Thoppil. 2014. Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia. Nat. Commun. 5:4862. doi:10.1038/ncomms5862
24. D'Ortenzio, F., and M. Ribera D'alcalà. 2009. On the trophic regimes of the Mediterranean Sea: A satellite analysis. Biogeosciences 6: 139–148. doi:10.5194/bg-6-139-2009
25. D'Ortenzio, F., V. Thierry, G. Eldin, H. Claustre, P. Testor, C. Coatanoan, M. Tedetti, C. Guinet, A. Poteau, L. Prieur, D. Lefevre, F. Bourrin, T. Carval, M. Coutx, V. Garcon, D. Thouron, M. Lacombe, P. Lherminier, H. Loisel, L. Mortier, and D. Antoine, 2010. White book on oceanic autonomous platforms for biogeochemical studies: Instrumentation and measure (PABIM). Version.
26. 3 profiling floats experiment. Geophys. Res. Lett. 41: 6443–6451. doi:10.1002/2014GL061020
27. Dos Santos, A. C. A., M. C. Calijuri, E. M. Moraes, M. A. T. Adorno, P. B. Falco, D. P. Carvalho, G. L. B. Deberdt, and S. F. Benassi. 2003. Comparison of three methods for chlorophyll determination: Spectrophotometry and fluorimetry in samples containing pigment mixtures and spectrophotometry in samples with separate pigments through high performance liquid chromatography. Acta Limnol. Bras. 15: 7–18. http://www.ablimno.org.br/publiActa.php?issue=v15n3
28. Falkowski, P., and D. A. Kiefer. 1985. Chlorophyll a fluorescence in phytoplankton: Relationship to photosynthesis and biomass. J. Plankton Res. 7: 715–731. doi:10.1093/plankt/7.5.715
29. Falkowski, P., and Z. Kolber. 1995. Variations in chlorophyll fluorescence yields in phytoplankton in the world oceans. Funct. Plant Biol. 22: 341–355. doi:10.1071/PP9950341
30. Geider, R. J. 1987. Light and temperature dependence of the carbon to chlorophyll a ration in microalgae and cyanobacteria: Implications for physiology and growth of phytoplankton. New Phytol. 106: 1–34. doi:10.1111/j.1469-8137.1987.tb04788.x
31. Geider, R. J., H. L. M acintyre, and T. M. Kana. 1997. Dynamic model of phytoplankton growth and acclimation: Responses of the balanced growth rate and the chlorophyll a: Carbon ratio to light, nutrient-limitation and temperature. Oceanogr. Lit. Rev. 148: 187–200.
32. Greene, R. M., Z. S. Kolber, D. G. Swift, N. W. Tindale, and P. G. Falkowski. 1994. Physiological limitation of phytoplankton photosynthesis in the eastern equatorial Pacific determined from variability in the quantum yield of fluorescence. Limnol. Oceanogr. 39: 1061–1074. doi:10.4319/lo.1994.39.5.1061
33. Guinet, C., and others. 2013. Calibration procedures and first dataset of Southern Ocean chlorophyll a profiles collected by elephant seals equipped with a newly developed CTD-fluorescence tags. Earth Syst. Sci. Data 5: 15–29. doi:10.5194/essd-5-15-2013
34. Holm-Hansen, O., C. J. Lorenzen, R. W. Holmes, and J. D. H. Strickland. 1965. Fluorometric determination of chlorophyll. J. Cons. Int. Explor. Mer. 30: 12. doi:10.1093/icesjms/30.1.3
35. Huot, Y., and M. Babin. 2011. Overview of fluorescence protocols: Theory, basic concepts, and practice, p. 31–74. In D. J. Suggett, O. Prášil, and M. A. Borowitzka [eds.], Chlorophyll fluorescence in aquatic sciences: Methods and applications. Developments in applied phycology. Springer.
36. IOCCG. 2011. Bio-optical sensors on Argo floats. In H. Claustre [ed.], Reports of the International Ocean-Colour Coordinating Group. IOCCG, No. 11, IOCCG, Dartmouth, Canada.
37. JCGM. 2008. Evaluation of measurement data - guide to the expression of uncertainty in measurement. GUM: Guide to the expression of uncertainty in measurement, p. 134. International Organization for Standardization.
38. Jeffrey, S., and G. Humphrey. 1975. New spectrophotometry equations for determining chlorophyll a, chlorophyll b, chlorophyll c-1 and chlorophyll c-2 in higher plants, algae and natural phytoplankton. Biochimie Physiol. Pflanzen 167: 191–194. doi:10.1016/S0015-3796(17)30778-3
39. Johnson, K., and H. Claustre. 2016. Bringing biogeochemistry into the Argo age. EOS 97. doi:10.1029/2016EO051467
40. Kruskopf, M., and K. J. Flynn. 2006. Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol. 169: 525–536. doi:10.1111/j.1469-8137.2005.01601.x
41. Lavigne, H., F. D'Ortenzio, H. Claustre, and A. Poteau. 2012. Towards a merged satellite and in situ fluorescence ocean chlorophyll product. Biogeosciences 9: 2111–2125. doi:10.5194/bg-9-2111-2012
42. Lavigne, H., F. D'ortenzio, M. R. D'Alcalà, H. Claustre, R. Sauzède, and M. Gacic. 2015. On the vertical distribution of the chlorophyll a concentration in the Mediterranean Sea: A basin-scale and seasonal approach. Biogeosciences 12: 5021–5039. doi:10.5194/bg-12-5021-2015
43. Longhurst, A. 1998. Ecological biogeography of the sea, p. 398. Academic Press.
44. Longhurst, A. R. 2006. Ecological geography of the sea, 2nd ed. Academic Press.
45. Lorenzen, C. J. 1966. A method for the continuous measurement of in vivo chlorophyll concentration. Deep-Sea Res. Oceanogr. Abstr. 13: 223–227. doi:10.1016/0011-7471(66)91102-8
46. Lorenzen, C. J. 1967. Determination of chlorophyll and pheo-pigments: Spectrophotometric equations. Limnol. Oceanogr. 12: 343–346. doi:10.4319/lo.1967.12.2.0343
47. Lorenzen, C. J., and J. Newton Downs. 1986. The specific absorption coefficients of chlorophyllide a and pheophorbide a in 90% acetone, and comments on the fluorometric determination of chlorophyll and pheopigments. Limnol. Oceanogr. 31: 4. doi:10.4319/lo.1986.31.2.0449
48. Marra, J., and C. Langdon. 1993. An evaluation of an in situ fluorometer for the estimation of chlorophyll a, p. 41. Palisades NY, DTIC Document.
49. Mitchell, B. G., and D. A. Kiefer. 1988. Chlorophyll a specific absorption and fluorescence excitation spectra for light-limited phytoplankton. Deep-Sea Res. Part A Oceanogr. Res. Pap. 35: 639–663.
50. Morel, A., and L. Prieur. 1977. Analysis of variations in ocean color. Limnol. Oceanogr. 22: 14. doi:10.4319/lo.1977.22.4.0709
51. Morel, A., and A. Bricaud. 1981. Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep-Sea Res. Part A Oceanogr. Res. Pap. 28: 1375–1393. doi:10.1016/0198-0149(81)90039-X
52. Morel, A., Y. Huot, B. Gentili, P. J. Werdell, S. B. Hooker, and B. A. Franz. 2007. Examining the consistency of products derived from various ocean color sensors in open ocean (case 1) waters in the perspective of a multi-sensor approach. Remote Sens. Environ. 111: 69–88. doi:10.1016/j.rse.2007.03.012
53. Morrison, J. R. 2003. In situ determination of the quantum yield of phytoplankton chlorophyll a fluorescence: A simple algorithm, observations, and a model. Limnol. Oceanogr. 48: 618–631. doi:10.4319/lo.2003.48.2.0618
54. Morrison, J. R., and D. S. Goodwin. 2010. Phytoplankton photocompensation from space-based fluorescence measurements. Geophys. Res. Lett. 37: L06603. doi:10.1029/2009GL041799
55. Neale, P. J., J. C. Cullen, and C. M. Yentsch. 1989. Bio-optical inferences from chlorophyll a fluorescence: What kind of fluorescence is measured in flow cytometry? Limnol. Oceanogr. 34: 9. doi:10.4319/lo.1989.34.8.1739
56. Oliver, M. J., and A. J. Irwin. 2008. Objective global ocean biogeographic provinces. Geophys. Res. Lett. 35: L15601. doi:10.1029/2008GL034238
57. Organelli, E., and others. 2016. A novel near-real-time quality-control procedure for radiometric profiles measured by Bio-Argo floats: Protocols and performances. J. Atmos. Oceanic Technol. 33: 937–951. doi:10.1175/JTECH-D-15-0193.1
58. Parkhill, J. P., G. Maillet, and J. J. Cullen. 2001. Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J. Phycol. 37: 517–529. doi:10.1046/j.1529-8817.2001.037004517.x
59. Pettigrew, N. R., and C. Roesler. 2005. Implementing the Gulf of Maine ocean observing system (GoMOOS), p. 1362–1369. Oceans 2005-Europe. IEEE. doi:10.1109/OCEANSE.2005.1513259
60. Proctor, C. W., and C. S. Roesler. 2010. New insights on obtaining phytoplankton concentration and composition from in situ multispectral chlorophyll fluorescence. Limnol. Oceanogr.: Methods 8: 695–708. doi:10.4319/lom.2010.8.695
61. Ras, J., H. Claustre, and J. Uitz. 2008. Spatial variability of phytoplankton pigment distributions in the Subtropical South Pacific Ocean: Comparison between in situ and predicted data. Biogeosciences 5: 353–369. doi:10.5194/bg-5-353-2008
62. ®. Water Res. 44: 2461–2472. doi:10.1016/j.watres.2010.01.012
63. Riemann, B., P. Simonsen, and L. Stensgaard. 1989. The carbon and chlorophyll content of phytoplankton from various nutrient regimes. J. Plankton Res. 11: 1037–1045. doi:10.1093/plankt/11.5.1037
64. Roesler, C. S. 2014. Calibration, correction and flagging of data from the chlorophyll fluorometer on GoMOOS Buoy A01: Nov 2005-Jun 2014. Boston: Massachusetts Water Resources Authority. Report 2014–14. 11 p.
65. Roesler, C. S., and A. H. Barnard. 2013. Optical proxy for phytoplankton biomass in the absence of photophysiology: Rethinking the absorption line height. Methods Oceanogr. 7: 79–94. doi:10.1016/j.mio.2013.12.003
66. Sackmann, B., M. Perry, and C. Eriksen. 2008. Seaglider observations of variability in daytime fluorescence quenching of chlorophyll-a in Northeastern Pacific coastal waters. Biogeosci. Discuss. 5: 2839–2865. doi:10.5194/bgd-5-2839-2008
67. Sauzède R., H. Claustre, C. Jamet, J. Uitz, J. Ras, A. Mignot, and F. D'Ortenzio. 2015. Retrieving the vertical distribution of chlorophyll a concentration and phytoplankton community composition from in situ fluorescence profiles: A method based on a neural network with potential for global-scale applications. J. Geophys. Res. Oceans 120: 451–470. doi:10.1002/2014JC010355
68. Schmechtig, C., A. Poteau, H. Claustre, F. D'Ortenzio, and E. Boss. 2015. Processing bio-Argo chlorophyll-a concentration at the DAC level. doi:10.13155/39468
69. Schuller, D., and others. 2015. SOCCOM float deployments from Polarstern ANTXXX_2 PS89.
70. Serôdio, J., and J. Lavaud. 2011. A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth. Res. 108: 15. doi:10.1007/s11120-011-9654-0
71. Sosik, H. M., and B. G. Mitchell. 1991. Absorption, fluorescence and quantum yield for growth in nitrogen-limited Dunaliella tertiolecta. Limnol. Oceanogr. 36: 910. doi:10.4319/lo.1991.36.5.0910
72. Strickland, J. D. H. 1968. Continuous measurement of in vivo chlorophyll; a precautionary note. Deep-Sea Res. Oceanogr. Abstr. 15: 225–227. doi:10.1016/0011-7471(68)90043-0
73. Swart, S., S. Thomalla, and P. Monteiro. 2015. The seasonal cycle of mixed layer dynamics and phytoplankton biomass in the Sub-Antarctic Zone: A high-resolution glider experiment. J. Mar. Syst. 147: 103–115. doi:10.1016/j.jmarsys.2014.06.002
74. Szeto, M., P. Werdell, T. Moore, and J. Campbell. 2011. Are the world's oceans optically different? J. Geophys. Res. Oceans 116. doi:10.1029/2011JC007230
75. Thibodeau, P. S., C. S. R oesler, S. L. Drapeau, S. Prabhu Matondkar, J. I. Goes, and P. J. Werdell. 2014. Locating Noctiluca miliaris in the Arabian Sea: An optical proxy approach. Limnol. Oceanogr. 59: 2042–2056. doi:10.4319/lo.2014.59.6.2042
76. Trees C. C., M. C. Kennicutt, and J. M. Brooks. 1985. Errors associated with the standard fluorimetric determination of chlorophylls and phaeopigments. Mar. Chem. 17: 1–12. doi:10.1016/0304-4203(85)90032-5
77. Vassiliev, I. R., Z. Kolber, K. D. Wyman, D. Mauzerall, V. K. Shukla, and P. G. Falkowski. 1995. Effects of iron limitation on photosystem II composition and light utilization in Dunaliella tertiolecta. Plant Physiol. 109: 963–972. doi:10.1104/pp.109.3.963
78. Welschmeyer, N. A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr. 39: 1985–1992. doi:10.4319/lo.1994.39.8.1985
79. Wernand, M. R., and H. J. Van Der Woerd. 2010. Spectral analysis of the Forel-Ule Ocean colour comparator scale. J. Eur. Opt. Soc. Rapid Publ. 5: 7. doi:10.2971/jeos.2010.10014s
80. Xing, X., A. Morel, H. Claustre, D. Antoine, F. D'Ortenzio, A. Poteau, and A. Mignot. 2011. Combined processing and mutual interpretation of radiometry and fluorimetry from autonomous profiling Bio-Argo floats: Chlorophyll a retrieval. J. Geophys. Res. Oceans 116. doi:10.1029/2010JC006899
81. Xing, X., H. Claustre, S. Blain, F. D'Ortenzio, D. Antoine, J. Ras, and C. Guinet. 2012. Quenching correction for in vivo chlorophyll fluorescence acquired by autonomous platforms: A case study with instrumented elephant seals in the Kerguelen region (Southern Ocean). Limnol. Oceanogr.: Methods 10: 483–495. doi:10.4319/lom.2012.10.483
82. Xing, X., H. Claustre, E. Boss, C. Roesler, E. Organelli, A. Poteau, M. Barbieux, and F. D'Ortenzio. 2017. Correction of profiles of in-situ chlorophyll fluorometry for the contribution of fluorescence originating from non-algal matter. Limnol. Oceanogr.: Methods 15: 80–93. doi:10.1002/lom3.10144