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Chlorophyll fluorescence effects in the red part of reflectance spectra of natural waters
ContinentalShelfResearch, Vol. 6 No. 3, pp 385 to 395, 1986.
0278-4343/86$3Jg) + 0.00 PergamonJournals Ltd.
Printed in Great Britain.
Chlorophyll fluorescence effects in the red part of reflectance spectra of natural waters D. SPITZER* and R. W. J. DIRKS* (Received 3 July 1984; in revised form 13 February 1985; accepted 26 June 1985) Abstract--Solar-induced fluorescence of algal pigments can be (remotely) measured in productive water masses. Detection of the peak related to this fluorescence in the red part of the reflectance spectra can then be used for the (remote) assessment of the biomass, particularly in the waters where other optical determination methods fail. To study the chlorophyll fluorescence effects in natural waters a two-flow radiative transfer model was developed and m e a s u r e m e n t s were performed in turbid coastal waters. Several p h e n o m e n a , including the influence of the suspended and dissolved materials on the height and the position (shift) of the peak, and the effects of the vertical stratification of the water column, are described. The observed shift of the reflectance m a x i m u m to the longer wavelength appears to be inherent to the presence of the particular material in the water. Reflectance values near the sea surface in the red part of the spectrum are only little influenced by the stratification.
INTRODUCTION
A MAXIMUMin the irradiance reflectance (further referred to as 'reflectance' only) spectra has been frequently observed between 680 and 700 nm in various natural water types (MOREL and PRIEUR, 1977; NEVILLEand GOWER, 1977; DOERFFER, 1981; SelTZERet al., 1982). This maximum was originally ascribed to the anomalous dispersion due to the Chl a molecules, later it was explained as a fluorescence band of this pigment (MORELand PRIEUR, 1977; GORDON, 1979a). The height of the chlorophyll fluorescence maximum at 685 nm is considered as a possible phytoplankton concentration index, although several influential uncertainties, like the impact of the variability of the ambient physico-chemical conditions and the intracellular effects, hinder general application of this method (SATHYENDRANATHet al., 1982; SATHYENDRANATHand M O R E L , 1983). VASILKOVand KOPELEVICH(1982) ascribed the spectral variations, i.e. the maximum around 690 nm and the associated minimum around 675 nm, solely to the pure seawater and chlorophyll absorption effects, contrary to the fluorescence hypotheses. During our investigations in west European waters, systematic shift of the reflectance peak to the longer wavelengths (695 nm) in the red part of the spectrum has been noticed in the areas rich in organic particulate and dissolved materials. Obviously, the shape of the reflectance spectra around the flourescence wavelength is affected by the absorption and scattering effects of all the natural suspended and dissolved materials. Our calculations based on a two-flow model developed previously (SPITZER and WERNAND, 1983) concern both oceanic and coastal water types. The maximum appears to be * Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB D e n Burg, Texel, The Netherlands. 385
386
D. SP1TZER and R. W. J. DIRKS
caused chiefly by the chlorophyll fluorescence, but its magnitude and position is ruled by the characteristic seawater parameters like the specific absorption and scattering coefficients and by the concentration of the dissolved organic matter. EXPERIMENTS
Measurements of the upwelling radiance L,, downwelling irradiance Ed and the downwelling radiance Ld were performed between 400 and 720 nm from a platform approximately 2 m above the sea surface. Employing the CORSAIR (Coastal Opical Remote Sensing Airborne Radiometer) system described previously (SPITZERet al., 1982), a single spectral 500 channels scan (spectral resolution 2 nm) can be performed within 32 ms. The irradiance was detected by means of a flat (cosine) collector, the radiance was measured using an objective lens with a field of view 12°. The L, was measured at 30° from the nadir at the azimuth 'away from the sun' to prevent the detection of the direct sun radiation reflected on the water surface (sun glitter). The Ld was always measured in the L,,-zenith plane at 30° from the zenith, to enable correction of the detected upwelling signal for the sky radiation reflected on the sea surface (sky glitter). The experiments including simultaneous seawater sampling were performed in the western part of the Dutch Wadden Sea during seasons and tidal periods with very variable seawater load on suspended organic and inorganic and dissolved organic materials. Generally, these concentrations characteristic for the turbid coastal waters were relatively high. The concentrations of the total suspended matter (dry seston) varied between 2 and 70 g m-3, the concentration of Chl a plus pheophytin a pigments varied between 5 and 50 mg m 3. The absorption coefficient of the filtered seawater at 380 nm characterizing the yellow substance concentration varied between 0.1 and 3 m ~. It should be mentioned that these high concentrations of suspended and dissolved materials, characteristic for the Wadden area, represent an extreme case even for the coastal areas. Immediately after sampling the emission spectra of the seawater were measured at the excitation wavelength 436 nm employing the Perkin-Elmer 2000 fluorometer. Figure 1 shows an example of the recorded emission together with the uncorrected and corrected irradiance reflectance R* = QLJ0.54 Ed, R = Q(L. - pLd)/0.54 Ed spectra. respectively, where Q = E,,/L., E. is the upwelling irradiance, p is the reflection coefficient for the air-water interface and the factor 0.54 describes the ratio of reflectance just above the water surface to the reflectance just under the surface (AusTIN. 1974). Q was determined from the simultaneous subsurface irradiance measurements resulting in 1.2 < Q < 3.5, dQ/d)~ ,~ O. The relatively low Q values (AUSTIN, 1980) are probably due to the large viewing angle from the nadir of the radiance measurements, in accordance with observations performed previously by SMm~(1974), demonstrating an increase of L, towards the larger angles. The reflectance spectra exhibit shape typical for the coastal region concerned, with low values in the blue part due to the absorption of the yellow substance and of the chlorophyllous pigments, increasing reflectance up to about 550 nm and then again decreasing due to the increase of absorption of the water itself and of the algal pigments. Three minima can occur between 550 and 700 nm, corresponding with the absorption maxima of the chlorophyll, phycoerythrin and phycocyanin pigments present in the algal species (YENTSCH, 1980). The wavelength of the maximum of the chlorophyll fluorescence emission of the seawater (around 685 nm) does not coincide with the position of the reflectance peak (around 692 nm).
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Chlorophyll fluorescence effects
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.03
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, .........
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500
600
I
,,
700
Fig. 1. Irradiance reflectance as measured in the turbid Wadden Sea. Spectra corrected (full line) and uncorrected (dashed line) for the sky glitter are displayed. The fluorescence emission peak measured in the laboratory on the water sample taken simultaneously with the reflectance measurements, is also presented (lower dashed line). The maximum emission wavelength is indicated. The determined concentrations were: C = 23 mg m 3 a,. (380) = 1.2 m 1.
MODEL
Two-flow radiative transfer model outlined previously (SPwzER and WERNAND, 1983) was applied for the calculations of the chlorophyll fluorescence effects. The variations along the depth z of the downwelling and upwelling irradiance Ed and E., respectively, including fluorescence are expressed as dE,,(z) dz - - ( a . ( z ) + b . ( z ) ) E . ( z ) + bd(Z)Ed(Z) + ~F(z) (1)
dEd(Z) dz - --(ad(z) + bd(Z))Ed(Z) + b . ( z ) E . ( z ) + ½F(z), where a. is the absorption coefficient for the upweiling irradiance, b,, is the backscattering coefficient for the upwelling irradiance, a,. is the absorption coefficient of the chlorophyllous material, F(X) = ( .ZEqbe x p ( - ( Z - Zm)2/2¢~2) Ja~.~ X (21r~2)"
o
(~d(~'E)ac(~'E) + E"(XE)a"(XE))dXE
is the source function of the chlorophyllous material fluorescence described by a Gaussian emission around the m a x i m u m wavelength ~..... with a width constant c and wavelength independent quantum yield dO (GORDON, 1979a; SPITZER and WERNAND 1983), ~ , is the upwelling scalar irradiance and AXE is the excitation wavelength interval.
388
D. SPITZERand R. W. J. DIRKS
Analogous definitions and relationships hold also for the quantities referring to the downwelling radiation (index d). Introducing the distribution functions D,, = ~ . / E . , Dd = ~£d/Ed, the apparent optical coefficients can be expressed (PREISENDORFER,1976) by means of the inherent absorption and backscattering coefficients a and bb, respectively, as a. ad b,, bd
= = "~ "~
O.a Oda D,,bt, Ddbt,.
Generally all coefficients are depth (z) and wavelength (K) dependent, the distribution functions D . . Dd can be approximated as independent of both, depth and wavelength (PREISENDORFER, 1976). For exact definitions see PREISENDORFER(1976) and GORDON (1979a). To solve system (1) the boundary conditions are E,(0) = Eao = the incident solar irradianee at zero depth, neglecting the contribution due to the reflection of E.(0) at the water-air interface, E . ( h ) l E d ( h ) = r = the reflection coefficient of the bottom (or a layer) at the depth h. For homogeneous deep waters E . ( z --~ oo) = O. The solution (PREISENDORFER, 1976) of system (1) in terms of the remotely observable reflectance at zero depth R(0) = E.(O)IEa(O) in case of deep homogeneous medium is then 1 + /} f keqbexp(-(X- K,n)2/20"2) R(O) = /} + ~ ~a~,,: k (2n62) ~ a,,0vE).
E,Io(XD
(D,,/}(kE) + O,t P£---P~--~E)dKE
(2)
p,, = l(ct, - Cd) -I'- I((C u "]- Cd) 2 - 4b,,bd)" Pd = l(cu -- Cd) -- I((Cu q- Cd) 2 -- 4b,,bd)"
c,, = a., + b,, Cd = a d + bd,
where/~ = bal(c. + Pa) is the reflectance term without fluorescence. In the case where absorption dominates the backscattering (i.e. a,, > b,,, a, > bd) the solution reduces to b. R(0) - - - -
ad + a.
1 c + -
2Edo
J
E.o(XE) a;~,
S4~()vE)Dd
a. + ad(kF)
dkE
keqb exp(-(k - km)2/2Gz) S,(KE) = a,.(kE)
X
(2rco'2)"-'
INPUT P A R A M E T E R S
To evaluate the fluorescence effects, absorption and scattering coefficients representative for natural seawater must be introduced into the model. The property of additivity
389
Chlorophyll fluorescence cffects
allows splitting up the coefficients into the contributions by the characteristic components of the seawater. According to widely accepted classification a = aw + ac + ap 4- ay b = bhw + bhc + bt,p,
where the index w refers to the pure seawater, c to the particulate chlorophyllous material, p to the particulate nonchlorophyllous material and y to the colored component of the dissolved organic matter (yellow substance). Specific absorption and backscattering coefficients are introduced ac = Ca*, ap = Pa~, bhc
= C ° 6 3 b ~ c , bbp =
Pb?,p,
where C is the pigment concentration in mg m -3 as determined by standard methods and P is the concentration of nonchlorophyllous particles in terms of the total scattering coefficient in m -I (PmEuR and SATHVENDRANATH,1981). For the calculations the following data were used in the model: 0.6 0.4 D, = 2.5, Da - c o s j + 0.85----9 = 1.1 for the sun zenith angle/ = 30 ° (PRIEURand SATHYENDRANATU,1981); a,,, bbw as tabulated by SMITH and BAKER (1981); ac()Q = (0.058 + 0.018 C)a*'(L); a*'(X) as tabulated by PRIEUR and SATHYENDRANATH(1981); bt,,(~-) = 0.005 x O.12C°~'3a*(550)/a~(k) ( P R I E U R , 1981); ay(~,) = ay(380) exp (-0.014(L- 380)) ( B R I C A U D et al., 1981); al,(~,) = 0.042Pap*'(k); ap' as tabulated by PRIEUR and SATHYENDRANATH(1981); b h n ( L ) =
• 07
R
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C
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• 03 0
• 02-
.01,
0 40(
d wovelength (nm) . . . .
'r
. . . .
l
. . . .
500
?
. . . .
i
.
600
.
.
.
i
. . . .
I
700
Fig. 2. Examples of computed reflectance spectra for various concentrations of suspended and dissolved materials. Line a: C = 1 mg m -3, P = 0.5 m ~, a,. = 0.1 m ~; line b: C = 10 mg m 3 P-0.5m -~.ay=0.1 m ~;linec:C= 1 mgm3 P=7m ~,a,.=0. l m ~;lined:C= 1 mgm 3 P = 0.5 m l,a,. = 3 m i.
390
D. SP1TZERand R. W. J. DIRKS
0.015 P 550/k (PRmuR, 1981), k,, = 685 rim; qb = 0.01, ~ = 11 as evaluated analogously to GORDON(1979a); and Ejo as tabulated by TYLERand SMI'm (1970). Representative calculated spectra for various water types, as displayed in Fig. 2, exhibit coincidence with experimental data collected elsewhere (SATHYENDRANATItand MOREL, 1983). APPLICATIONS
Results of the model computations are presented. Results of experiments performed in very turbid waters, generally supporting the hypotheses, are shown as well.
Reflectance ratio The (blue-green) ratio between the reflectance at 440 nm and at 560 nm is frequently used in the algorithms for remote sensing of the aquatic biomass through its pigment concentration ( G O R D O N and MOREL, 1983). Figure 3 shows this ratio as a function of the pigment concentration C in double log scales for different yellow substance concentrations. For limited intervals of the pigment concentration this relationship can be approximated by a linear function (in the log-log scales), though the increasing yellow substance concentration decreases the sensitivity of such an algorithm. Curves calculated by GORDON and MOREL(1983) from a simplified model for seawater containing exclusively particulate chlorophyllous material ('Case 1') and an empirical relationship are presented in Fig. 3, together with values found in the Wadden Sea, where the concentrations of the suspended and dissolved matter varied ~vithin the limits used in the computations. It can be noticed that the blue-green ratio is rather unsuitable for the assessment of the pigment concentrations in the region where our measurements were taken.
Chlorophyll fluorescence effects in various water types To evaluateothe magnitude of the fluorscence effects, the height of the peak, defined as R ( O ) - R at the maximum emission wavelength has been investigated.
R E =
lit t ,
lO-~
C(mg Ira3) . . . . . . .
. . . . . . .
. . . . . . .
Fig. 3. Reflectance ratio as a function of the pigment concentrations. Full lines represent the ratio as computed according to the model presented in this paper. The used values of a,. (380) in m t are indicated. T h e dashed line ( . . . . ) shows the ratio computed by GORDON and MOREL (1983) applying a simplified ('Case 1') model, and an experimental algorithm (straight dashed line . . . . ). Results of our m e a s u r e m e n t s (cluster of the points) in the turbid W a d d e n Sea are also displayed.
391
Chlorophyll fluorescence effects
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20
30
40
50
60
70
80
90
Fig. 4. Height of the fluorescence peak as a function of the pigment concentration. Full lines represent the computations with a,. (380) = 0.1 m ~ and variable P as indicated in m ], dashed lines represent the computations with P = 1 m ~ and variable a,. (380) as indicated in m ~. The experimental data collected in the Wadden Sea are shown.
Figure 4 shows the R F a s function of the pigment concentration C for several yellow substance and nonchlorophyllous particulate material concentrations typical for some coastal waters. The computations indicate that the origin of the peak around 685 nm can be ascribed to the fluorescence effects, as the R F increases with C. For a limited interval of the pigment concentration, these curves can be approximated by linear functions in accordance with the experimental data (NEVILLEand GOWER, 1977; DOERFER, 1981; SelTZERet al., 1982). However, the presence of other than chlorophyllous materials have a substantial influence on the R F - C relationship. This explains also the scatter of the measured values displayed in Fig. 4. The cluster of the points cannot be matched by a single (regression) line, though, like in the previous case, the corresponding concentrations of the suspended and dissolved matter varied within the limits used in computations. Position of the maximum reflectance in the red The shift of the reflectance maximum is determined by the spectral behaviour of the absorption and backscattering coefficients. The pure water contribution tends to shift the maximum to the shorter wavelengths due to the increasing absorption and decreasing backscattering as function of the wavelength. The effects of the chlorophyllous particles, on the contrary, will cause a shift to the longer wavelengths due to their decreasing absorption and increasing backscattering as function of the wavelength. Also yellow substance and the nonchlorochyllous particles affect the position of the maximum. Again, the increasing C causes the reflectance at 685 nm to be lower than the reflectance at 690 nm, this effect being more pronounced at higher P and Yconcentration. The reversion of the relationship from R(685) > R(690) to R(685) < R(690), which is the indication of the shift to the longer wavelengths, appears even at low C values, when a>. (380) and/or P are high.
392
D. SPITZER and R. W. J. DIRKS
•012t R
/
~
•o"t ,
°'°t
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.oo 1 •008 -
~
\
.007-
5
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I
wavelength(nm) .00540'
I
' 660 "
i
' 6E}O '
I
' ?00
Fig. 5. C o m p u t e d shapes of the m a x i m u m in the red part of the spectrum, demonstrating the shift to the longer wavelengths due to the increase of the pigment concentration as indicated at each line i n m g m ~. Values of a,. (380) = 0.1 m i p = 1 m i were applied.
The dominant influence of the increasing pigment concentration on the shift of the peak in the red is shown in Fig. 5. Even for low a v and P values the maximum shifts from 685 nm to about 690 nm when C > 5 mg m 3. The form and the shifts of the computed spectra are in agreement with our observations. The reflectance spectra taken above the eutrophic turbid Wadden Sea exhibit the maximum located around 695 nm (Fig. 1), while above the less turbid southern part of the North Sea (SPrl ZER and WERNAND,1983) this maximum was detected around 68? nm.
Effects of stratification of the water column The vertical distribution of the particulate (algal) material can, under certain conditions, exhibit a subsurface maximum. As the remotely detected upwelling signal originates from about 1/Kd deep water column, where K~t = - d(ln Ed)/dz (GORDON and M c C L U N E Y , 1975), the influence of the stratification should be considered• The numerical method of invariant imbedding (MEYER, 1973) was chosen for solving system (l) in the case of the depth-dependent function F(X, z). The vertical pigment distribution and analogously the variations of the absorption coefficient a< (ks.., z) were chosen in the Gaussian form
t li - ,,AM where zm is the depth of the maximum pigment concentration. Since it can be expected that the near-surface reflectance R(0) is only little influenced by the pigment content below the maximum layer, the fact that C(z --+ oo) q: 0 does not play any important role in further calculations. Dependently on the choice of the constants C,, C~, ey,, (pigment depth profile) the contribution of the pigment-rich layer to the R(0) can be calculated. An example is shown in Fig. 6. Generally, the fluorescence of the layer located at the depths
393
Chlorophyll fluorescence effects
•005-
R
•004
.oo~
.oo25
;
~,
~,
~
~
Zm(m)
~,
Fig. 6. Reflectance at 685 n m as a function of the depth where the m a x i m u m of the (Gaussian) pigment distribution occurs. The parameters used: a,• (380) = 0.1 m ~, P = 1 m ~, m i n i m u m concentration Co = 1 mg m 3, m a x i m u m concentration C~ = 5 mg m 3 width of the pigment layer 2.35 ~,. = 3 m (lower line) and 5 m (upper line).
where the pigment maximum currently occurs (Zm > 10 m) ( P L A T T and H E R M A N , 1983) contributes to the R(0) negligibly. As can be expected, this contribution is less than the contribution at the shorter (blue-green) wavelengths (GORDON, 1979b; GORDON and CLARK, 1980). DISCUSSION
AND CONCLUSION
In accordance with the previous experimental studies, the model calculations indicate the applicability of the pigment fluorescence (remote) measurements for the surface phytoplankton distribution assessment. In addition to the intracellular and environmental effects extensively discussed by SATHYENDRANATItet al. (1982) the variation of the fluorescence-concentration relationship due to the load of all the particulate and dissolved materials, abundant in some water types, must be taken into account as described above, when dealing with the development and application of the fluorescence-method detection instruments and retrieval algorithms. The range of the concentration variations of the particulate nonchlorophyllous and dissolved organic materials within the coastal area, where the chlorophyll concentration is to be mapped through its fluorescence, should be known in order to estimate the errors of determination. In most cases, when the P varies within two decades and ay < 3 m-~ these errors do not exceed 40% and are comparable with the influence of the qb variations (GORDON et a l . , 1984). Support of the remote measurements by the sea truth collection including the P and a v (if relevant) allowing local adjustment of the algorithms, would be most advantageous. Our measurements described above allow the estimation of the sky glitter. It appears that this contribution to the measured upwelling radiance can exceed in the blue part of the spectrum 60% while in the red part it is <10% under most of the atmospheric conditions. This fact contributes to the advantages of the application of the fluorescence method
394
D. SPITZERand R. W. J. DmKS
(lower atmospheric influences, specificity with respect to chlorophyll, relative simplicity of algorithms) as compared to the blue-green ratio method by SAT|IYENDRANATHet al. (1982). It must be mentioned that the comparisons between the calculations and experiments (Figs 3 and 4) have only a demonstrative character since no appropriate absorption and scattering coefficients (input parameters) for the extreme conditions of the Wadden Sea are available yet. These input parameters can differ from those determined by PRmVRand SATtlYENDRANATH(1981). Abundancy of particulate and dissolved material causes systematic shifts of the observed fluorescence maximum to the longer wavelengths. The occurrence of these shifts is inherent to the presence of algal material. A question arises whether for the application of the optical remote sensing above the turbid coastal waters a scanner channel centred around 690 nm (maximum signal) would be more suitable than a channel at the orignal maximum fluorescence wavelength of 685 nm, though the influence of atmospheric absorption should also be considered. The calculations confirm (GORDON,1979b) that the vertical pigment stratification of the water column occurring at depths more than several metres generally cannot be recognized in the fluorescence signal detected above the sea surface. Acknowledgernents--The
authors wish to thank M. R. Wernand, R. Manuels, E. van lerland, W. M. L. Lambrechts and J. Regtien for their contributions during the experimental procedures and the manuscript preparation.
REFERENCES AUSTIN R. W. (1974) The remote sensing of spectral radiance from below the ocean surface. In: Optical aspects of oceanography, N. G. JERLOV and E. STEEMANN NIEt,S[LN, editors, Academic Press, New York, pp. 317-344. AUSTIN R. W. (1980) Gulf of Mexico, ocean-color surface-truth measurements. Boundary-Layer Meteorology, 18, 269-285. BmCAUD A., A. MOREL and L. PRIEUR (1981) Absorption by dissolved organic matter of the sea (yellow substance) in the UV and visible domains. Lirnnology and Oceanography, 26.43-53. DOERFEER R. (1981) Factor analysis in ocean colour interpretation. In: Oceanography from space, J. F. R. GOWER, editor, Plenum Press, New York, pp. 339-345. GORDON H. R. (1979a) Diffuse reflectance of the ocean: the theory of its augmentation by chlorophyll a fluorescence at 685 rim. Applied Optics, 18, 1161-1166. GORDON H. R. (1979b) Estimation of depth of sunlight penetration in natural waters for the remote sensing of chlorophyll a via in vivo fluorescence. Applied Optics, 18, 1883-1884. GORDON H. R. and W. R. MCCLUNEY (1975) Estimation of the depth of sunlight penetration in the sea for remote sensing. Applied Optics, |4,413-416. GORDON H. R. and D. K. CLARK(1980) Remote sensing optical properties of a stratified ocean: an improved interpretation. Applied Optics, 19, 3428-3430. GORDON H. R. and A, Y. MOREL(1983) Remote assessment of ocean color for interpretation of satellite visible imagery. Lecture notes on coastal and estuarine studies, Springer-Verlag, New York. GORDON H. R., D. K, CLARKand W. W. BROENKOW(1984) The relationship between sunlight-induced in vivo fluorescence and the chlorophyll a concentrations IAPSO. IUGG Proces-Verbaux No. 16, XVIII General Assembly, Hamburg, August 1983, p, 144. MEYER G. H. {1973) Initial value methods for boundary value problems theory and application of invariant imbedding. Academic Press, New York, pp. 17-70. MOREL A. and L. PRIEUR (1977) Analysis of variations in ocean color. Lirnnology and Oceanography, 22, 709-722. NEVlLLE R. A. and J. F. R. GOWER (1977) Passive remote sensing of phytoplankton via chlorophyll a fluorescence. Journal of Geophysical Research, 82, 3487-3493.
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PI,ATTT. and A. W. HERMAN(1983) Remote sensing of phytoplankton in the sea: surface-layer chlorophyll as an estimate of water-column chlorophyll and primary production. International Journal of Remote Sensing, 4, 34_3-351. PRHSENDOREER R. V. (1976) Hydrologic optics, Vol. 5, U.S. Department of Commerce, NOAA, pp. 8-51. PRXEUR L. (1981) Influence of dissolved and suspended matter on inherent properties considered as input parameters in optical ocean modelling. In: A collection of extended Abstracts presented at the Symposium on the Radiation Transfer in the Oceans and Remote Sensing of Ocean Properties, Hamburg, pp. 68-72. PRIEUR L. and S. SATIIYENDRANATH(1981) An optical classification of coastal and oceanic water based on the specific spectral absorption curves of phytoplankton pigments, dissolved organic matter, and other particulate materials. Limnology and Oceanography, 26, 671-689. SATttYENDRANATHS., L. PRIEURand A. MOREL(1982) Interpretation of ocean colour data with special rclerence to OCM. Midterm report Contract ESA 4726-81-F-DD-SC. SATIIYENDRANATH S. and A. MOREL (1983) Light emerging from the sea--interpretation and uses in remote sensing. In: Remote sensing applications in marine science and technology, A. P. CRACRNH,I., editor, D. Reidel Publishing Co., Dordrecht, U.K. pp. 32,3-357. SMITI] R. C. (1974) Structure of solar radiation in the upper layers of the sea. In: Opticalaspects r~[oceanography, N. G. JERI,OVand E. STEEMANNIELSEN, editors, Academic Press, New York, pp. 95-119. SMrrlt R. C. and K. S. BAKER(1981) Optical properties of the clearest natural waters (200-800 nm). Al?plied Optics, 20, 177-184. SPITZER D. and M. R. WERNAND (1983) Multi-spectral remote sensing of fluorescent tracers: theory and experiments. Oceanologica Acta, 6, 201-210. SPITZER D., C. RAPPOLDTand L. NYKJAER(1982) Optical remote sensing of tidal regions. In: Digest, Vol. 1, International (;eoscience and Remote Sensing Symposium, Munich 1982, IEEE Catalog No. 82 CH 14723-6, pp. 2.1-2.3. TYLER J. E. and R. C. SMITH (1970) Measurements" of spectral irradiance underwater. Gordon & Breach, New York, p. 46. VASILKOVA. P. and D. V. KOPELEVlCH(1982) Reasons of the appearance of the maximum near 700 nm in the radiance spectrum emitted by the ocean layer. Oceanology, 22,697-701. YENTSCH C. S. (1980) Light attenuation and phytoplankton photosynthesis. In: The physiological ecology of phytoplankton, I. MORRIS, editor, Blackwell Scientific, London, pp. 99-127.
0278-4343/86$3Jg) + 0.00 PergamonJournals Ltd.
Printed in Great Britain.
Chlorophyll fluorescence effects in the red part of reflectance spectra of natural waters D. SPITZER* and R. W. J. DIRKS* (Received 3 July 1984; in revised form 13 February 1985; accepted 26 June 1985) Abstract--Solar-induced fluorescence of algal pigments can be (remotely) measured in productive water masses. Detection of the peak related to this fluorescence in the red part of the reflectance spectra can then be used for the (remote) assessment of the biomass, particularly in the waters where other optical determination methods fail. To study the chlorophyll fluorescence effects in natural waters a two-flow radiative transfer model was developed and m e a s u r e m e n t s were performed in turbid coastal waters. Several p h e n o m e n a , including the influence of the suspended and dissolved materials on the height and the position (shift) of the peak, and the effects of the vertical stratification of the water column, are described. The observed shift of the reflectance m a x i m u m to the longer wavelength appears to be inherent to the presence of the particular material in the water. Reflectance values near the sea surface in the red part of the spectrum are only little influenced by the stratification.
INTRODUCTION
A MAXIMUMin the irradiance reflectance (further referred to as 'reflectance' only) spectra has been frequently observed between 680 and 700 nm in various natural water types (MOREL and PRIEUR, 1977; NEVILLEand GOWER, 1977; DOERFFER, 1981; SelTZERet al., 1982). This maximum was originally ascribed to the anomalous dispersion due to the Chl a molecules, later it was explained as a fluorescence band of this pigment (MORELand PRIEUR, 1977; GORDON, 1979a). The height of the chlorophyll fluorescence maximum at 685 nm is considered as a possible phytoplankton concentration index, although several influential uncertainties, like the impact of the variability of the ambient physico-chemical conditions and the intracellular effects, hinder general application of this method (SATHYENDRANATHet al., 1982; SATHYENDRANATHand M O R E L , 1983). VASILKOVand KOPELEVICH(1982) ascribed the spectral variations, i.e. the maximum around 690 nm and the associated minimum around 675 nm, solely to the pure seawater and chlorophyll absorption effects, contrary to the fluorescence hypotheses. During our investigations in west European waters, systematic shift of the reflectance peak to the longer wavelengths (695 nm) in the red part of the spectrum has been noticed in the areas rich in organic particulate and dissolved materials. Obviously, the shape of the reflectance spectra around the flourescence wavelength is affected by the absorption and scattering effects of all the natural suspended and dissolved materials. Our calculations based on a two-flow model developed previously (SPITZER and WERNAND, 1983) concern both oceanic and coastal water types. The maximum appears to be * Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB D e n Burg, Texel, The Netherlands. 385
386
D. SP1TZER and R. W. J. DIRKS
caused chiefly by the chlorophyll fluorescence, but its magnitude and position is ruled by the characteristic seawater parameters like the specific absorption and scattering coefficients and by the concentration of the dissolved organic matter. EXPERIMENTS
Measurements of the upwelling radiance L,, downwelling irradiance Ed and the downwelling radiance Ld were performed between 400 and 720 nm from a platform approximately 2 m above the sea surface. Employing the CORSAIR (Coastal Opical Remote Sensing Airborne Radiometer) system described previously (SPITZERet al., 1982), a single spectral 500 channels scan (spectral resolution 2 nm) can be performed within 32 ms. The irradiance was detected by means of a flat (cosine) collector, the radiance was measured using an objective lens with a field of view 12°. The L, was measured at 30° from the nadir at the azimuth 'away from the sun' to prevent the detection of the direct sun radiation reflected on the water surface (sun glitter). The Ld was always measured in the L,,-zenith plane at 30° from the zenith, to enable correction of the detected upwelling signal for the sky radiation reflected on the sea surface (sky glitter). The experiments including simultaneous seawater sampling were performed in the western part of the Dutch Wadden Sea during seasons and tidal periods with very variable seawater load on suspended organic and inorganic and dissolved organic materials. Generally, these concentrations characteristic for the turbid coastal waters were relatively high. The concentrations of the total suspended matter (dry seston) varied between 2 and 70 g m-3, the concentration of Chl a plus pheophytin a pigments varied between 5 and 50 mg m 3. The absorption coefficient of the filtered seawater at 380 nm characterizing the yellow substance concentration varied between 0.1 and 3 m ~. It should be mentioned that these high concentrations of suspended and dissolved materials, characteristic for the Wadden area, represent an extreme case even for the coastal areas. Immediately after sampling the emission spectra of the seawater were measured at the excitation wavelength 436 nm employing the Perkin-Elmer 2000 fluorometer. Figure 1 shows an example of the recorded emission together with the uncorrected and corrected irradiance reflectance R* = QLJ0.54 Ed, R = Q(L. - pLd)/0.54 Ed spectra. respectively, where Q = E,,/L., E. is the upwelling irradiance, p is the reflection coefficient for the air-water interface and the factor 0.54 describes the ratio of reflectance just above the water surface to the reflectance just under the surface (AusTIN. 1974). Q was determined from the simultaneous subsurface irradiance measurements resulting in 1.2 < Q < 3.5, dQ/d)~ ,~ O. The relatively low Q values (AUSTIN, 1980) are probably due to the large viewing angle from the nadir of the radiance measurements, in accordance with observations performed previously by SMm~(1974), demonstrating an increase of L, towards the larger angles. The reflectance spectra exhibit shape typical for the coastal region concerned, with low values in the blue part due to the absorption of the yellow substance and of the chlorophyllous pigments, increasing reflectance up to about 550 nm and then again decreasing due to the increase of absorption of the water itself and of the algal pigments. Three minima can occur between 550 and 700 nm, corresponding with the absorption maxima of the chlorophyll, phycoerythrin and phycocyanin pigments present in the algal species (YENTSCH, 1980). The wavelength of the maximum of the chlorophyll fluorescence emission of the seawater (around 685 nm) does not coincide with the position of the reflectance peak (around 692 nm).
o,]
Chlorophyll fluorescence effects
.06
/
\
/
k\-
ii I / f - ~ \ \ .05
l
/ / / /
.04 ¸
387
_,
"--',,', \',,.-,
.03
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/
i~ ,/ i / ',,
•
.01-
.........
0 , 4OO
--/
, .........
,;,o:e,,e,,,?,,h f°,"!,,
500
600
I
,,
700
Fig. 1. Irradiance reflectance as measured in the turbid Wadden Sea. Spectra corrected (full line) and uncorrected (dashed line) for the sky glitter are displayed. The fluorescence emission peak measured in the laboratory on the water sample taken simultaneously with the reflectance measurements, is also presented (lower dashed line). The maximum emission wavelength is indicated. The determined concentrations were: C = 23 mg m 3 a,. (380) = 1.2 m 1.
MODEL
Two-flow radiative transfer model outlined previously (SPwzER and WERNAND, 1983) was applied for the calculations of the chlorophyll fluorescence effects. The variations along the depth z of the downwelling and upwelling irradiance Ed and E., respectively, including fluorescence are expressed as dE,,(z) dz - - ( a . ( z ) + b . ( z ) ) E . ( z ) + bd(Z)Ed(Z) + ~F(z) (1)
dEd(Z) dz - --(ad(z) + bd(Z))Ed(Z) + b . ( z ) E . ( z ) + ½F(z), where a. is the absorption coefficient for the upweiling irradiance, b,, is the backscattering coefficient for the upwelling irradiance, a,. is the absorption coefficient of the chlorophyllous material, F(X) = ( .ZEqbe x p ( - ( Z - Zm)2/2¢~2) Ja~.~ X (21r~2)"
o
(~d(~'E)ac(~'E) + E"(XE)a"(XE))dXE
is the source function of the chlorophyllous material fluorescence described by a Gaussian emission around the m a x i m u m wavelength ~..... with a width constant c and wavelength independent quantum yield dO (GORDON, 1979a; SPITZER and WERNAND 1983), ~ , is the upwelling scalar irradiance and AXE is the excitation wavelength interval.
388
D. SPITZERand R. W. J. DIRKS
Analogous definitions and relationships hold also for the quantities referring to the downwelling radiation (index d). Introducing the distribution functions D,, = ~ . / E . , Dd = ~£d/Ed, the apparent optical coefficients can be expressed (PREISENDORFER,1976) by means of the inherent absorption and backscattering coefficients a and bb, respectively, as a. ad b,, bd
= = "~ "~
O.a Oda D,,bt, Ddbt,.
Generally all coefficients are depth (z) and wavelength (K) dependent, the distribution functions D . . Dd can be approximated as independent of both, depth and wavelength (PREISENDORFER, 1976). For exact definitions see PREISENDORFER(1976) and GORDON (1979a). To solve system (1) the boundary conditions are E,(0) = Eao = the incident solar irradianee at zero depth, neglecting the contribution due to the reflection of E.(0) at the water-air interface, E . ( h ) l E d ( h ) = r = the reflection coefficient of the bottom (or a layer) at the depth h. For homogeneous deep waters E . ( z --~ oo) = O. The solution (PREISENDORFER, 1976) of system (1) in terms of the remotely observable reflectance at zero depth R(0) = E.(O)IEa(O) in case of deep homogeneous medium is then 1 + /} f keqbexp(-(X- K,n)2/20"2) R(O) = /} + ~ ~a~,,: k (2n62) ~ a,,0vE).
E,Io(XD
(D,,/}(kE) + O,t P£---P~--~E)dKE
(2)
p,, = l(ct, - Cd) -I'- I((C u "]- Cd) 2 - 4b,,bd)" Pd = l(cu -- Cd) -- I((Cu q- Cd) 2 -- 4b,,bd)"
c,, = a., + b,, Cd = a d + bd,
where/~ = bal(c. + Pa) is the reflectance term without fluorescence. In the case where absorption dominates the backscattering (i.e. a,, > b,,, a, > bd) the solution reduces to b. R(0) - - - -
ad + a.
1 c + -
2Edo
J
E.o(XE) a;~,
S4~()vE)Dd
a. + ad(kF)
dkE
keqb exp(-(k - km)2/2Gz) S,(KE) = a,.(kE)
X
(2rco'2)"-'
INPUT P A R A M E T E R S
To evaluate the fluorescence effects, absorption and scattering coefficients representative for natural seawater must be introduced into the model. The property of additivity
389
Chlorophyll fluorescence cffects
allows splitting up the coefficients into the contributions by the characteristic components of the seawater. According to widely accepted classification a = aw + ac + ap 4- ay b = bhw + bhc + bt,p,
where the index w refers to the pure seawater, c to the particulate chlorophyllous material, p to the particulate nonchlorophyllous material and y to the colored component of the dissolved organic matter (yellow substance). Specific absorption and backscattering coefficients are introduced ac = Ca*, ap = Pa~, bhc
= C ° 6 3 b ~ c , bbp =
Pb?,p,
where C is the pigment concentration in mg m -3 as determined by standard methods and P is the concentration of nonchlorophyllous particles in terms of the total scattering coefficient in m -I (PmEuR and SATHVENDRANATH,1981). For the calculations the following data were used in the model: 0.6 0.4 D, = 2.5, Da - c o s j + 0.85----9 = 1.1 for the sun zenith angle/ = 30 ° (PRIEURand SATHYENDRANATU,1981); a,,, bbw as tabulated by SMITH and BAKER (1981); ac()Q = (0.058 + 0.018 C)a*'(L); a*'(X) as tabulated by PRIEUR and SATHYENDRANATH(1981); bt,,(~-) = 0.005 x O.12C°~'3a*(550)/a~(k) ( P R I E U R , 1981); ay(~,) = ay(380) exp (-0.014(L- 380)) ( B R I C A U D et al., 1981); al,(~,) = 0.042Pap*'(k); ap' as tabulated by PRIEUR and SATHYENDRANATH(1981); b h n ( L ) =
• 07
R
.06.
C
• 05
.04"
• 03 0
• 02-
.01,
0 40(
d wovelength (nm) . . . .
'r
. . . .
l
. . . .
500
?
. . . .
i
.
600
.
.
.
i
. . . .
I
700
Fig. 2. Examples of computed reflectance spectra for various concentrations of suspended and dissolved materials. Line a: C = 1 mg m -3, P = 0.5 m ~, a,. = 0.1 m ~; line b: C = 10 mg m 3 P-0.5m -~.ay=0.1 m ~;linec:C= 1 mgm3 P=7m ~,a,.=0. l m ~;lined:C= 1 mgm 3 P = 0.5 m l,a,. = 3 m i.
390
D. SP1TZERand R. W. J. DIRKS
0.015 P 550/k (PRmuR, 1981), k,, = 685 rim; qb = 0.01, ~ = 11 as evaluated analogously to GORDON(1979a); and Ejo as tabulated by TYLERand SMI'm (1970). Representative calculated spectra for various water types, as displayed in Fig. 2, exhibit coincidence with experimental data collected elsewhere (SATHYENDRANATItand MOREL, 1983). APPLICATIONS
Results of the model computations are presented. Results of experiments performed in very turbid waters, generally supporting the hypotheses, are shown as well.
Reflectance ratio The (blue-green) ratio between the reflectance at 440 nm and at 560 nm is frequently used in the algorithms for remote sensing of the aquatic biomass through its pigment concentration ( G O R D O N and MOREL, 1983). Figure 3 shows this ratio as a function of the pigment concentration C in double log scales for different yellow substance concentrations. For limited intervals of the pigment concentration this relationship can be approximated by a linear function (in the log-log scales), though the increasing yellow substance concentration decreases the sensitivity of such an algorithm. Curves calculated by GORDON and MOREL(1983) from a simplified model for seawater containing exclusively particulate chlorophyllous material ('Case 1') and an empirical relationship are presented in Fig. 3, together with values found in the Wadden Sea, where the concentrations of the suspended and dissolved matter varied ~vithin the limits used in the computations. It can be noticed that the blue-green ratio is rather unsuitable for the assessment of the pigment concentrations in the region where our measurements were taken.
Chlorophyll fluorescence effects in various water types To evaluateothe magnitude of the fluorscence effects, the height of the peak, defined as R ( O ) - R at the maximum emission wavelength has been investigated.
R E =
lit t ,
lO-~
C(mg Ira3) . . . . . . .
. . . . . . .
. . . . . . .
Fig. 3. Reflectance ratio as a function of the pigment concentrations. Full lines represent the ratio as computed according to the model presented in this paper. The used values of a,. (380) in m t are indicated. T h e dashed line ( . . . . ) shows the ratio computed by GORDON and MOREL (1983) applying a simplified ('Case 1') model, and an experimental algorithm (straight dashed line . . . . ). Results of our m e a s u r e m e n t s (cluster of the points) in the turbid W a d d e n Sea are also displayed.
391
Chlorophyll fluorescence effects
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./~
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• C °'~,, ,
/
t
"
.0020
I0
20
30
40
50
60
70
80
90
Fig. 4. Height of the fluorescence peak as a function of the pigment concentration. Full lines represent the computations with a,. (380) = 0.1 m ~ and variable P as indicated in m ], dashed lines represent the computations with P = 1 m ~ and variable a,. (380) as indicated in m ~. The experimental data collected in the Wadden Sea are shown.
Figure 4 shows the R F a s function of the pigment concentration C for several yellow substance and nonchlorophyllous particulate material concentrations typical for some coastal waters. The computations indicate that the origin of the peak around 685 nm can be ascribed to the fluorescence effects, as the R F increases with C. For a limited interval of the pigment concentration, these curves can be approximated by linear functions in accordance with the experimental data (NEVILLEand GOWER, 1977; DOERFER, 1981; SelTZERet al., 1982). However, the presence of other than chlorophyllous materials have a substantial influence on the R F - C relationship. This explains also the scatter of the measured values displayed in Fig. 4. The cluster of the points cannot be matched by a single (regression) line, though, like in the previous case, the corresponding concentrations of the suspended and dissolved matter varied within the limits used in computations. Position of the maximum reflectance in the red The shift of the reflectance maximum is determined by the spectral behaviour of the absorption and backscattering coefficients. The pure water contribution tends to shift the maximum to the shorter wavelengths due to the increasing absorption and decreasing backscattering as function of the wavelength. The effects of the chlorophyllous particles, on the contrary, will cause a shift to the longer wavelengths due to their decreasing absorption and increasing backscattering as function of the wavelength. Also yellow substance and the nonchlorochyllous particles affect the position of the maximum. Again, the increasing C causes the reflectance at 685 nm to be lower than the reflectance at 690 nm, this effect being more pronounced at higher P and Yconcentration. The reversion of the relationship from R(685) > R(690) to R(685) < R(690), which is the indication of the shift to the longer wavelengths, appears even at low C values, when a>. (380) and/or P are high.
392
D. SPITZER and R. W. J. DIRKS
•012t R
/
~
•o"t ,
°'°t
//: t7!
.oo 1 •008 -
~
\
.007-
5
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I
wavelength(nm) .00540'
I
' 660 "
i
' 6E}O '
I
' ?00
Fig. 5. C o m p u t e d shapes of the m a x i m u m in the red part of the spectrum, demonstrating the shift to the longer wavelengths due to the increase of the pigment concentration as indicated at each line i n m g m ~. Values of a,. (380) = 0.1 m i p = 1 m i were applied.
The dominant influence of the increasing pigment concentration on the shift of the peak in the red is shown in Fig. 5. Even for low a v and P values the maximum shifts from 685 nm to about 690 nm when C > 5 mg m 3. The form and the shifts of the computed spectra are in agreement with our observations. The reflectance spectra taken above the eutrophic turbid Wadden Sea exhibit the maximum located around 695 nm (Fig. 1), while above the less turbid southern part of the North Sea (SPrl ZER and WERNAND,1983) this maximum was detected around 68? nm.
Effects of stratification of the water column The vertical distribution of the particulate (algal) material can, under certain conditions, exhibit a subsurface maximum. As the remotely detected upwelling signal originates from about 1/Kd deep water column, where K~t = - d(ln Ed)/dz (GORDON and M c C L U N E Y , 1975), the influence of the stratification should be considered• The numerical method of invariant imbedding (MEYER, 1973) was chosen for solving system (l) in the case of the depth-dependent function F(X, z). The vertical pigment distribution and analogously the variations of the absorption coefficient a< (ks.., z) were chosen in the Gaussian form
t li - ,,AM where zm is the depth of the maximum pigment concentration. Since it can be expected that the near-surface reflectance R(0) is only little influenced by the pigment content below the maximum layer, the fact that C(z --+ oo) q: 0 does not play any important role in further calculations. Dependently on the choice of the constants C,, C~, ey,, (pigment depth profile) the contribution of the pigment-rich layer to the R(0) can be calculated. An example is shown in Fig. 6. Generally, the fluorescence of the layer located at the depths
393
Chlorophyll fluorescence effects
•005-
R
•004
.oo~
.oo25
;
~,
~,
~
~
Zm(m)
~,
Fig. 6. Reflectance at 685 n m as a function of the depth where the m a x i m u m of the (Gaussian) pigment distribution occurs. The parameters used: a,• (380) = 0.1 m ~, P = 1 m ~, m i n i m u m concentration Co = 1 mg m 3, m a x i m u m concentration C~ = 5 mg m 3 width of the pigment layer 2.35 ~,. = 3 m (lower line) and 5 m (upper line).
where the pigment maximum currently occurs (Zm > 10 m) ( P L A T T and H E R M A N , 1983) contributes to the R(0) negligibly. As can be expected, this contribution is less than the contribution at the shorter (blue-green) wavelengths (GORDON, 1979b; GORDON and CLARK, 1980). DISCUSSION
AND CONCLUSION
In accordance with the previous experimental studies, the model calculations indicate the applicability of the pigment fluorescence (remote) measurements for the surface phytoplankton distribution assessment. In addition to the intracellular and environmental effects extensively discussed by SATHYENDRANATItet al. (1982) the variation of the fluorescence-concentration relationship due to the load of all the particulate and dissolved materials, abundant in some water types, must be taken into account as described above, when dealing with the development and application of the fluorescence-method detection instruments and retrieval algorithms. The range of the concentration variations of the particulate nonchlorophyllous and dissolved organic materials within the coastal area, where the chlorophyll concentration is to be mapped through its fluorescence, should be known in order to estimate the errors of determination. In most cases, when the P varies within two decades and ay < 3 m-~ these errors do not exceed 40% and are comparable with the influence of the qb variations (GORDON et a l . , 1984). Support of the remote measurements by the sea truth collection including the P and a v (if relevant) allowing local adjustment of the algorithms, would be most advantageous. Our measurements described above allow the estimation of the sky glitter. It appears that this contribution to the measured upwelling radiance can exceed in the blue part of the spectrum 60% while in the red part it is <10% under most of the atmospheric conditions. This fact contributes to the advantages of the application of the fluorescence method
394
D. SPITZERand R. W. J. DmKS
(lower atmospheric influences, specificity with respect to chlorophyll, relative simplicity of algorithms) as compared to the blue-green ratio method by SAT|IYENDRANATHet al. (1982). It must be mentioned that the comparisons between the calculations and experiments (Figs 3 and 4) have only a demonstrative character since no appropriate absorption and scattering coefficients (input parameters) for the extreme conditions of the Wadden Sea are available yet. These input parameters can differ from those determined by PRmVRand SATtlYENDRANATH(1981). Abundancy of particulate and dissolved material causes systematic shifts of the observed fluorescence maximum to the longer wavelengths. The occurrence of these shifts is inherent to the presence of algal material. A question arises whether for the application of the optical remote sensing above the turbid coastal waters a scanner channel centred around 690 nm (maximum signal) would be more suitable than a channel at the orignal maximum fluorescence wavelength of 685 nm, though the influence of atmospheric absorption should also be considered. The calculations confirm (GORDON,1979b) that the vertical pigment stratification of the water column occurring at depths more than several metres generally cannot be recognized in the fluorescence signal detected above the sea surface. Acknowledgernents--The
authors wish to thank M. R. Wernand, R. Manuels, E. van lerland, W. M. L. Lambrechts and J. Regtien for their contributions during the experimental procedures and the manuscript preparation.
REFERENCES AUSTIN R. W. (1974) The remote sensing of spectral radiance from below the ocean surface. In: Optical aspects of oceanography, N. G. JERLOV and E. STEEMANN NIEt,S[LN, editors, Academic Press, New York, pp. 317-344. AUSTIN R. W. (1980) Gulf of Mexico, ocean-color surface-truth measurements. Boundary-Layer Meteorology, 18, 269-285. BmCAUD A., A. MOREL and L. PRIEUR (1981) Absorption by dissolved organic matter of the sea (yellow substance) in the UV and visible domains. Lirnnology and Oceanography, 26.43-53. DOERFEER R. (1981) Factor analysis in ocean colour interpretation. In: Oceanography from space, J. F. R. GOWER, editor, Plenum Press, New York, pp. 339-345. GORDON H. R. (1979a) Diffuse reflectance of the ocean: the theory of its augmentation by chlorophyll a fluorescence at 685 rim. Applied Optics, 18, 1161-1166. GORDON H. R. (1979b) Estimation of depth of sunlight penetration in natural waters for the remote sensing of chlorophyll a via in vivo fluorescence. Applied Optics, 18, 1883-1884. GORDON H. R. and W. R. MCCLUNEY (1975) Estimation of the depth of sunlight penetration in the sea for remote sensing. Applied Optics, |4,413-416. GORDON H. R. and D. K. CLARK(1980) Remote sensing optical properties of a stratified ocean: an improved interpretation. Applied Optics, 19, 3428-3430. GORDON H. R. and A, Y. MOREL(1983) Remote assessment of ocean color for interpretation of satellite visible imagery. Lecture notes on coastal and estuarine studies, Springer-Verlag, New York. GORDON H. R., D. K, CLARKand W. W. BROENKOW(1984) The relationship between sunlight-induced in vivo fluorescence and the chlorophyll a concentrations IAPSO. IUGG Proces-Verbaux No. 16, XVIII General Assembly, Hamburg, August 1983, p, 144. MEYER G. H. {1973) Initial value methods for boundary value problems theory and application of invariant imbedding. Academic Press, New York, pp. 17-70. MOREL A. and L. PRIEUR (1977) Analysis of variations in ocean color. Lirnnology and Oceanography, 22, 709-722. NEVlLLE R. A. and J. F. R. GOWER (1977) Passive remote sensing of phytoplankton via chlorophyll a fluorescence. Journal of Geophysical Research, 82, 3487-3493.
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PI,ATTT. and A. W. HERMAN(1983) Remote sensing of phytoplankton in the sea: surface-layer chlorophyll as an estimate of water-column chlorophyll and primary production. International Journal of Remote Sensing, 4, 34_3-351. PRHSENDOREER R. V. (1976) Hydrologic optics, Vol. 5, U.S. Department of Commerce, NOAA, pp. 8-51. PRXEUR L. (1981) Influence of dissolved and suspended matter on inherent properties considered as input parameters in optical ocean modelling. In: A collection of extended Abstracts presented at the Symposium on the Radiation Transfer in the Oceans and Remote Sensing of Ocean Properties, Hamburg, pp. 68-72. PRIEUR L. and S. SATIIYENDRANATH(1981) An optical classification of coastal and oceanic water based on the specific spectral absorption curves of phytoplankton pigments, dissolved organic matter, and other particulate materials. Limnology and Oceanography, 26, 671-689. SATttYENDRANATHS., L. PRIEURand A. MOREL(1982) Interpretation of ocean colour data with special rclerence to OCM. Midterm report Contract ESA 4726-81-F-DD-SC. SATIIYENDRANATH S. and A. MOREL (1983) Light emerging from the sea--interpretation and uses in remote sensing. In: Remote sensing applications in marine science and technology, A. P. CRACRNH,I., editor, D. Reidel Publishing Co., Dordrecht, U.K. pp. 32,3-357. SMITI] R. C. (1974) Structure of solar radiation in the upper layers of the sea. In: Opticalaspects r~[oceanography, N. G. JERI,OVand E. STEEMANNIELSEN, editors, Academic Press, New York, pp. 95-119. SMrrlt R. C. and K. S. BAKER(1981) Optical properties of the clearest natural waters (200-800 nm). Al?plied Optics, 20, 177-184. SPITZER D. and M. R. WERNAND (1983) Multi-spectral remote sensing of fluorescent tracers: theory and experiments. Oceanologica Acta, 6, 201-210. SPITZER D., C. RAPPOLDTand L. NYKJAER(1982) Optical remote sensing of tidal regions. In: Digest, Vol. 1, International (;eoscience and Remote Sensing Symposium, Munich 1982, IEEE Catalog No. 82 CH 14723-6, pp. 2.1-2.3. TYLER J. E. and R. C. SMITH (1970) Measurements" of spectral irradiance underwater. Gordon & Breach, New York, p. 46. VASILKOVA. P. and D. V. KOPELEVlCH(1982) Reasons of the appearance of the maximum near 700 nm in the radiance spectrum emitted by the ocean layer. Oceanology, 22,697-701. YENTSCH C. S. (1980) Light attenuation and phytoplankton photosynthesis. In: The physiological ecology of phytoplankton, I. MORRIS, editor, Blackwell Scientific, London, pp. 99-127.