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Prasinophyceae)1 J. Phycol. 38, 1132–1142 (2002) DIEL VARIATIONS IN OPTICAL PROPERTIES OF MICROMONAS PUSILLA (PRASINOPHYCEAE)1 Michele D. DuRand,2 Rebecca E. Green, Heidi M. Sosik,3 and Robert J. Olson Woods Hole Oceanographic Institution, Biology Department, MS #32, Woods Hole, Massachusetts 02543, USA Micromonas pusilla (Butcher) Manton et Parke, a nitrogen ratio; Chli, intracellular chlorophyll concen- marine prasinophyte, was used to investigate how tration; CV, coefficient of variation; D, the diameter cell growth and division affect optical properties of of the mean cell; FLS, forward light scattering; G, phytoplankton over the light:dark cycle. Measurements geometric projected area of the mean cell; ␥, spectral were made of cell size and concentration, attenua- slope; ␮, growth rate; n, real refractive index; nЈ, imag- ␴ tion and absorption coefficients, flow cytometric inary refractive index; a, absorption cross-section; ␴ ␴ forward and side light scattering and chl fluores- b, scattering cross-section; c, attenuation cross-sec- cence, and chl and carbon content. The refractive in- tion; Qa, efficiency factor for absorption; Qb, effi- dex was derived from observations and Mie scattering ciency factor for scattering; Qc, efficiency factor for theory. Diel variations occurred, with cells increasing attenuation; V , volume of the mean cell in size, light scattering, and carbon content during daytime photosynthesis and decreasing during night- time division. Cells averaged 1.6 ␮m in diameter and exhibited phased division, with 1.3 divisions per day. Scattering changes resulted primarily from changes introduction in cell size and not refractive index; absorption Diel variations in bulk optical properties such as changes were consistent with a negligible package ef- beam attenuation (Siegel et al. 1989, Hamilton et al. fect. Measurements over the diel cycle suggest that 1990, Cullen et al. 1992, Stramska and Dickey 1992, in M. pusilla carbon-specific attenuation varies with Gardner et al. 1993, 1995) and in single cell optical cell size, and this relationship appears to extend to properties such as phytoplankton forward light scat- other phytoplankton species. Because M. pusilla is tering (FLS) (Olson et al. 1990, DuRand and Olson one of the smallest eukaryotic phytoplankton and be- 1996, Vaulot and Marie 1999) have been observed in longs to a common marine genus, these results will numerous field studies in many of the world’s oceans. be useful for interpreting in situ light scattering vari- A number of researchers have documented diel varia- ation. The relationship between forward light scat- tions in cell light scattering during laboratory studies tering (FLS) and volume over the diel cycle for M. of various phytoplankton cultures (Stramski and Rey- pusilla was similar to that determined for a variety of nolds 1993, Stramski et al. 1995, DuRand and Olson phytoplankton species over a large size range. We 1998). The typical pattern exhibited is scattering min- propose a method to estimate cellular carbon con- ima at dawn and maxima near dusk. Diel variations in tent directly from FLS, which will improve our esti- beam attenuation have been related to primary pro- mates of the contribution of different phytoplank- duction (Siegel et al. 1989, Cullen et al. 1992, Walsh ton groups to productivity and total carbon content et al. 1995) and have been proportioned among in the oceans. groups of organisms in the ocean (DuRand 1995, Du- Key index words: absorption; attenuation; diel varia- Rand and Olson 1996, Chung et al. 1998, Binder and tion; flow cytometry; Micromonas pusilla; optical DuRand 2002). properties; phytoplankton; Prasinophyceae; refractive Light scattering by particles such as phytoplankton index; scattering is determined by their size and refractive index and, to a lesser extent, by their shape and internal struc- Abbreviations: a, absorption coefficient; a*chl, chl- tures ( Jerlov 1976). If diel changes in scattering cross- specific absorption coefficient; ac-9, absorption and sections can be related to changes in cell size and attenuation meter; b, scattering coefficient; b*chl, chl- carbon content, then phytoplankton productivity specific scattering coefficient; c, attenuation coeffi- (Cullen et al. 1992) and growth rates (DuRand 1995, cient; c*c , carbon-specific attenuation coefficient; Ci, Binder et al. 1996) can be estimated from measure- intracellular carbon concentration; C:N, carbon to ments over the diel cycle in the field. In laboratory studies, contrasting data have been obtained on the relative contributions of variations in particle size and in refractive index to diel changes in optical cross- 1Received 24 January 2002. Accepted 22 June 2002. sections. Changes in refractive index have been found 2Present address: Ocean Sciences Centre, Memorial University of Newfoundland, St. John’s, NL A1C 5S7, Canada. E-mail mdurand@ to be equal to or more important than changes in cell mun.ca. size for determining the attenuation cross-section of a 3Author for correspondence: e-mail [email protected]. diatom (Stramski and Reynolds 1993) and a prokary- 1132 M. PUSILLA DIEL OPTICAL PROPERTIES 1133 otic picoplankter (Stramski et al. 1995). In contrast, materials and methods DuRand and Olson (1998) reported that changes in cell size were more important than those in refractive Laboratory measurements. Micromonas pusilla (CCMP 489), a strain isolated from the Sargasso Sea, was grown in f/2 medium index in determining diel variations in beam attenua- without silica (Guillard 1975) in replicate batch cultures at 25Њ C. tion for a small chlorophyte. The filtered (0.22 ␮m) seawater and nutrient solutions were au- Estimates of primary production in the ocean have toclaved separately and then added together after the seawater had cooled. To ensure particle-free medium, the solution was been made from diel variations in beam attenuation by ␮ converting changes in beam attenuation to carbon pro- then sterile filtered through a 0.22- m filter. The cultures were grown in 10-L carboys (containing 2 L of culture at the start of duction using a constant factor (Siegel et al. 1989, sampling) in an incubator on a 12:12-h light:dark cycle at 120 Cullen et al. 1992, Walsh et al. 1995). Ackleson et al. ␮mol photonsؒmϪ2ؒsϪ1 (cool-white fluorescent lights, measured (1993), however, reported carbon-independent changes with a QSL-100 4␲ quantum scalar irradiance sensor, Biospher- in cell scattering. In addition, several other laboratory ical Instruments, San Diego, CA, USA). The carboys were bub- bled with moisturized filtered air. Samples were forced out by studies on cultures have found that the carbon-specific air pressure through a sterile sampling port. The cultures were beam attenuation varies by 25%–30% over the diel cycle acclimated to the growth conditions for 7 days and diluted daily (usually increasing during the day) and mean values for 5 days before the day of sampling (with the last dilution 24 among the species studied vary by Ϯ21% (Stramski and h before the start of the sampling) to maintain the cells in ex- Reynolds 1993, Stramski et al. 1995, DuRand and Olson ponential growth. Samples were withdrawn every 2 h (starting at dawn, until 1998). It may be necessary to know the composition of the following dawn) and measurements made of cellular and the phytoplankton community to best interpret diel bulk properties (individual cell measurements of concentra- variations in beam attenuation as production (DuRand tion, forward and side light scattering, chl fluorescence, and and Olson 1996, Binder and DuRand 2002). cell size, and bulk measurements of absorption, attenuation, extracted chl content, and carbon content). Samples were pro- Stramski (1999) suggested that the strong correla- cessed in dim light during the nighttime sampling points. tion between intracellular carbon concentration and A modified Epics V flow cytometer (Beckman Coulter, Mi- real refractive index and between intracellular chl con- ami, FL, USA) with a Cicero acquisition interface (Cytomation, Fort Collins, CO, USA) was used to measure FLS (3–19Њ at 488 Њ ف -centration and the imaginary refractive index, ob served for phytoplankton cultures, could be used to es- nm), side angle light scattering ( 54–126 at 488 nm), and chl fluorescence (660–700 nm) of the M. pusilla cells in undiluted timate carbon and chl content of individual cells in duplicate samples. Polystyrene microspheres of two sizes (0.66 natural water samples. Despite the fact that the deriva- ␮m and 2.14 ␮m, YG calibration-grade beads from Poly- tion of refractive index from single-particle analysis is sciences, Warrington, PA, USA) were added as internal stan- not currently routine, the results of such an approach dards and differentiated from cells by their orange fluores- cence (555–595 nm). The samples were introduced into the are appealing because knowledge of the carbon-based flow cytometer using a peristaltic pump (Harvard Apparatus, size distribution of the plankton is crucial to an under- Holliston, MA, USA), and cell concentration was determined standing of upper ocean carbon cycling and knowl- from the pump flow rate and sample run time. Mean values of the measured parameters normalized to reference beads (2.14 edge of chl per cell is important for studies of phy- ␮ toplankton productivity and for bio-optical modeling. m) were calculated using “CYTOWIN” software (D. Vaulot, www.sb-roscoff.fr/Phyto/cyto.html). Flow cytometric analyses of natural samples have The size distribution of the M. pusilla cells was determined us- shown that eukaryotic picophytoplankton are ubiqui- ing a Coulter Multisizer (Beckman Coulter, Miami, FL, USA) tous (e.g. DuRand and Olson 1996, Campbell et al. equipped with a 30-␮m aperture. The culture was diluted with fil- 1997, Zubkov et al. 1998, Shalapyonok et al. 2001), tered seawater (9- to 14-fold dilutions) to obtain coincidence rates of 6% or less. The size distributions of replicate samples were av- but detailed laboratory studies of diel variations in phy- eraged and normalized to the cell concentration from flow cyto- toplankton optical properties have focused on smaller metric analysis.
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