Parting the Red Seas: The Optics of Red Tides H.M. Dierssen 1*, Kudela, R.M. 2, Ryan, J.P. 3 1 University of Connecticut, Department of Marine Science, Groton, CT 06340. 2 University of California, Ocean Sciences Department, Santa Cruz, CA 95064. 3 Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039. *To whom correspondence should be addressed. E-mail: heidi.dierssen@uconn.edu The first of the ten plagues of Egypt may be one of the earliest recorded instances of a red tide: "... and all the waters that were in the river turned to blood. And the fish that were in the river died, and the water stank..." 1. Much attention has been focused on understanding the association between red tides and harmful algal blooms 2, but misconceptions about the ruddy discoloration of marine surface water during intense algal blooms are prevalent. Optical measurements of sea surface reflectance during red tides show peak reflectance at a wavelength of 570 nm - a part of the visible spectrum not characterized by red, but by a yellowish hue. Moreover, red tides are commonly believed to originate from only a select group of phytoplankton containing specific reddish pigments 3. Here, we demonstrate that the color of red or red/brown tides is a function not only of the phytoplankton accessory pigments, but also the physiology of the human eye and can be produced at high concentrations of nearly all of the major phytoplankton taxa.
When observed under magnification, individual phytoplankton generally appear green, yellow/green or golden brown in color due to the pigments that absorb light for photosynthesis and photoprotection (Fig. 1). Chlorophyll a, found in nearly all oxygenic photosynthetic organisms, absorbs light in the blue and red portion of the spectrum (Fig. 2A). However, other pigments such as chlorophylls b and c, phycobiliproteins and carotenoids are also found in phytoplankton and harvest more of the incident blue and green light 4. Phytoplankton absorption spectra show spectral differences that can be attributed to the type and amount of pigment within the cells (Fig. 2A) 5. Larger phytoplankton have lower absorption per mass of chlorophyll than smaller phytoplankton due to packaging of the pigments within chloroplasts 6. Red algae (Rhodophyceae) are the reddest in color and contain pigments that absorb light in the middle or green region of the visible spectrum (~550 nm), while green algae (Chlorophyceae) absorb the least amount of green light. Diatoms (Bacillariophyceae) and dinoflagellates (Dinophyceae), responsible for over three quarters of the known red tide species 2, have similarly shaped absorption spectra that fall between these two extremes. Measured radiance spectra leaving the sea surface of a dinoflagellate red tide typically have a peak at a visible wavelength of 570 nm (Fig. 2B) a part of the visible spectrum characterized by a yellowish hue. Modeled radiance spectra for dense accumulations of phytoplankton known to cause red tides, including dinoflagellates and diatoms, exhibit the same spectral shape. The color red, however, is typically expressed at longer wavelengths from 600 to 700 nm (Fig. 2C). In addition, a lesser peak in the spectrum is centered at 683 nm due to solar-stimulated chlorophyll fluorescence 7, but the human eye
is not very sensitive at detecting light in this far-red region of the spectrum. Clearly, perceived color is a function of the physiology of the human eye and not just the dominant reflected wavelength of light. Most humans have three different kinds of cones in their eye, referred to as long-, middle-, and short-wavelength cones that collectively are responsible for our color vision (Fig. 2C). Each cone contains unique pigments that respond to a different range of visible wavelengths. These cones are sometimes called red, green, and blue cones, although the "red" wavelength cone response is actually in the yellow region of the spectrum. The red cone pigment evolved most recently (30-40 million years ago) by a minor mutation in the green cone pigment that shifted peak absorption only 30 nm towards the red. Even though much of the green and red cone absorption spectra overlap, the spectral difference is enough to distinguish ripe red fruit from green foliage 8. The color perceived by our visual system depends on the total light incident upon each type of cone and the comparative response between the three types. As phytoplankton concentrations increase at the sea surface, the apparent color goes from blue, to green, and finally to red or red/brown for the majority of phytoplankton taxa (Fig. 2D). The color brown is a mixture of light that stimulates all three cones, but with the maximum signal in the red. Of the taxa considered, only Prochlorococcus and Chlorophyceae do not produce a red or red/brown tide at high concentrations. However, not all of these taxa will actually produce a red tide in nature. Creation of dense aggregations of phytoplankton at the sea surface requires complex interactions
between cell growth and motility and physical mechanisms such as horizontal convergence, vertical stratification 9,10 and environmental perturbation 11. Satellite remote sensing can be a useful tool for identifying the temporal and spatial extent of red tides. Unfortunately, the current space-borne ocean color sensors have limited spectral capabilities 12 and provide no information in the region of the spectrum where red tides peak (570 nm) and where most of the taxon-specific differences occur in water-leaving radiance (555-660 nm) (Fig. 2B). Ocean color sensors with more spectral information (i.e., hyperspectral) will be critical for monitoring red tide formation 13. However, the spectral information from red tides has led to confusion because the color at the peak reflectance is not the color perceived by the human eye. A red tide is perceived by the human eye when phytoplankton become concentrated at the sea surface and absorb enough green light to shift the dominant signal only 20 nm from the eye's middle- to long-wavelength cones. There really isn't more light than meets the eye.
References 1. (7: 20-21). 2. Sournia, A. in Harmful Algal Algal Blooms, Proceedings of the Sixth International Conference on Toxic Marine Phytoplankton, October 1993, Nantes, France 103-112 (Lavoisier Publishing Inc., Paris, 1995). 3. Anderson, D. M. Red Tides. Scientific American 271, 52-58 (1994). 4. Falkowski, P. G. & Raven, J. Aquatic Photosynthesis (Blackwell, Oxford, 1997). 5. Stramski, D., Bricaud, A. & Morel, A. Modeling the inherent optical propreties of the ocean based on the detailed composition of the planktonic community. App. Opt. 40, 2929-2945 (2001). 6. Ciotti, A. M., Cullen, J. J. & Lewis, M. R. Assessment of the relationships between dominant cell size in natural phytoplankton communities and the spectral shape of the absorption coefficient. Limnol. Oceangr. 47, 404-417 (2002). 7. Smith, R. C. & Baker, K. S. Optical classification of natural waters. Limnol. Oceangr. 23, 260-267 (1978). 8. Livingstone, M. Vision and art: the biology of seeing (Harry N. Abrams, New York, 2002). 9. Ryther, J. H. in The Luminescence of Biological Systems (AAAS, Washington, DC, 1955). 10. Smayda, T. J. Turbulence, watermass stratification and harmful algal blooms: an alternative view and frontal zones as "pelagic seed banks". Harmful Algae 1, 95-112 (2002). 11. Ryan, J. et al. A red tide borne of rapid change. Nature (submitted).
12. Yoder, J. A. Terra's view of the sea. Science 288, 1978-1980 (2000). 13. Chang, G. et al. The new age of hyperspectral oceanography. Oceanogr. 17, 16-23 (2004). 14. Bigelow Laboratory for Ocean Sciences, University of New England, Jet Propulsion Laboratory/California Institute of Technology. Phytopia: Discovery of the Marine Ecosystem. CD: Version 01. (NASA, 2003). 15. Mobley, C. D. Light and water: Radiative transfer in natural waters (Academic Press, San Diego, 1994). Acknowledgements: We acknowledge D. Stramski for graciously providing us with absorption and scattering spectra. Funding was provided by NOAA's Center for Integrative Coastal Observation, Research, and Education (HMD), NOAA's Center for Integrated Marine Technology (RMK), and NASA (JPR).
Fig. 1. Color of individual phytoplankton cells under magnification compared to the color of a red tide. While the color of individual cells is dependent on the illumination source, microscopic examination of species known to cause red tides, including A) the diatom Chaetoceros socialis 14, B) the dinoflagellate Prorocentrum micans 14 or C) the dinoflagellate Ceratium sp. reveals colors ranging from green, golden brown, and reddish golden compared to D) photo of a red tide off the Monterey coast consisting of the dinoflagellate Ceratium sp. Fig. 2. Sea surface color modeled for increasing phytoplankton concentrations. A) Mean absorption spectra normalized to chlorophyll a concentration (m 2 mg Chl -1 ) for different phytoplankton communities (legend in panel D) [Kudela and 5 ]. Black dashed line is an absorption spectrum for chlorophyll a (Chl) pigment alone (scaled for figure) to illustrate the absorption due to accessory pigments in the different phytoplankton taxa. B) Upwelling radiance heading straight upward from the sea surface (L w, W m -2 nm -1 sr -1 ) during intense phytoplankton bloom conditions (50 mg Chl m -3 ). Results were modeled with the Hydrolight radiative transfer model using taxon-specific absorption (panel A) and scattering coefficients 5, a particle phase function corresponding to a backscattering ratio of 0.012, and including chlorophyll fluorescence 15. Black dashed line is a measured spectrum from a dinoflagellate red tide in Monterey Bay, 11 Oct. 2002. C) Response of the three cone types (short, middle, and long) in the human eye to different wavelengths of light (scaled to the same range) 8. The bottom color spectrum indicates the color associated with each wavelength of light. D) Color of the sea surface as a function of biomass concentration (chlorophyll a used as a proxy) for different
phytoplankton taxa. Color was modeled from water-leaving radiance (Panel B) using the Commission Internationale de l'êclairage color matching function for the 10º field size (C.I.E. 1964, tristimulus function) and transforming the color values to the Red-Green- Blue (RGB) colors of a standard computer monitor. Under various sun and observation angles, the reflected skylight off the sea surface would influence the observed color.
A B C D Figure 1: Dierssen et al.
A) Absorption, a * p(λ) B) Radiance, L w (λ) C) Photoreceptor Response 0.06 short middle long 0.01 0.04 0.02 0.005 400 500 600 700 400 500 600 700 400 500 600 700 Wavelength (nm) D) Sea Surface Color Prochlorococcus Synechococcus Haptophyceae Bacillariophyceae Rhodophyceae Dinophyceae Raphidophyceae Chlorophyceae 2 5 10 15 20 30 40 50 Chlorophyll (mg m -3 ) Figure 2: Dierssen et al.