Variability of Photosynthetic Parameters of the Surface Phytoplankton in the Black Sea Z

Home , Sargasso Sea

Oceanology, Vol. 42, No. 1, 2002, pp. 53Ð67. Translated from Okeanologiya, Vol. 42, No. 1, 2002, pp. 60Ð75. Original Russian Text Copyright © 2002 by Finenko, Churilova, Sosik, Basturk. English Translation Copyright © 2002 by MAIK “Nauka /Interperiodica” (Russia). MARINE BIOLOGY

Variability of Photosynthetic Parameters of the Surface Phytoplankton in the Black Sea Z. Z. Finenko1, T. Ya. Churilova1, H. M. Sosik2, and O. Basturk3 1 Institute of Biology of the Southern Seas, National Academy of Sciences, Sevastopol, Ukraine 2 Institute of Oceanography, Woods Hole, United States 3 Middle Eastern University, Institute of Marine Research, Erdemli, Turkey Received August 17, 2000; in ﬁnal form, February 8, 2001

Abstract—The effect of physical, chemical, and biological variables on the spatial and temporal variability of B αB the maximum photosynthesis intensity (Pmax ) and the initial slope of light curves were studied. Throughout B the year, the values of the photosynthetic parameters varied within one order of magnitude, i.e., Pmax from 1 to 11 mgC mgChl–1 h–1 and αβ from 0.04 to 0.20 mgC mgChl–1 h–1/(W m–2). The spatial and temporal variability B αB B of Pmax and were lower than that of the chlorophyll concentration. The seasonal dynamics of the Pmax values is characterized by their growth from winter to summer and their decrease by the end of the year. The annual B changes in Pmax are controlled by temperature, and they have a weak dependence on the phytoplankton adap- B tation to incident solar radiation. The share of the temperature in the overall variability of Pmax and Ik is 56−70%, and the temperature dependencies of these parameters are described by exponential functions. The temporal dynamics of αB are nitrate- and chlorophyll a-dependent. The temporal changes in the maximum φ αB quantum yield of phytoplankton photosynthesis ( max) calculated by and the average speciﬁc light absorp- φ tion by algae in the photosynthetically active radiation range (aph* ) were analyzed. It was shown that max and

aph* were chlorophyll concentration-dependent parameters, but their changes are in the opposite direction. The φ max values increase with a rise in the chlorophyll concentration, whereas the aph* values decrease. Over a wide range of chlorophyll concentration values (from 0.1 to 20 mg/m3), the relationship between the αB values and the chlorophyll concentration can be approximated by a dome-shaped curve with a maximum at about 3 mg/m3.

INTRODUCTION the temperature and light adaptation [1, 7, 11, 20]. The The key parameters determining the relationship results of the studies showed that, in the World Ocean, between the photosynthesis rate (P) and the light (I) are the photosynthetic parameter values vary over a wide α ∆ ∆ B Ð1 Ð1 the initial slope of the light curve ( P/ I) and the range, namely, Pmax from 1 to 24 mgC mgChl h and maximum photosynthesis rate (Pmax). These parameters αB from 0.03 to 0.40 mgC mgChlÐ1 hÐ1/(W mÐ2). The normalized with respect to the chlorophyll a concentra- minimum values are characteristic of high latitudes, αB B tion ( and Pmax ) are usually used in models for the while the maximums are related to the coastal commu- estimation of the primary production values from the nities of subtropical and tropical waters. These values satellite-based chlorophyll measurements and determi- do not conﬁrm the hypothesis on the constancy of the αB nation of the effect of the environmental factors on the values, which was derived from the fact that the ini- speciﬁc phytoplankton production. tial slope of the light curves was dependent only on photochemical reactions. During the past few years, active efforts were aimed at the extension of our understanding of the character of The most important factors determining the values variations of photosynthetic phytoplankton parameters. of the photosynthetic parameters in natural phytoplank- In many publications, the αB and PB variabilities are ton populations are the light, temperature, nutrient con- max centration, and pigment content in algae. One of the considered in connection with seasonal [21, 47, 48] and methods of the study of the effect of a combination of regional [19, 26, 28, 29, 34, 38, 49] features, as well as αB B with the daily periodicity [23, 25], taxonomic and size the factors on the variations of the and Pmax values composition diversity of phytoplankton [9, 17, 52], and may help the comparison of their values in the areas

54 FINENKO et al. with different environmental conditions. The generali- bution, reliable quantitative data for the interrelation of zation of a great amount of evidence allowed us to dis- the photosynthetic parameters with the environmental tinguish four vast areas in the World Ocean, namely, the features, changes in the pigment composition, and Polar area, the areas of the western and trade winds, and physiological and morphological characteristics of the coastal zone, within which provinces were recog- phytoplankton are required. nized [36, 48]. The classification of provinces is based The shortage of data on the variability in the photo- on the differences between some physical factors influ- synthetic parameters of phytoplankton in the Black Sea encing the dynamics of the phytoplankton community, makes it difficult to use remote sensing observations for photosynthetic parameters, and the parameters deter- calculation of the primary production values to the mining the vertical chlorophyll distribution. As a result, scale of the entire sea, because the previous studies provinces were recognized where, during certain sea- were restricted in space and time [1, 8, 9]. sons, the photosynthetic parameters change within relatively narrow limits [47, 48]. The use of these data, in The aim of this paper is to examine the effect of the combination with the results of the satellite-based mea- key physical, chemical, and biological factors on the surements of chlorophyll concentration, gave us the annual and spatial variability of the photosynthetic possibility to calculate the primary production values parameters of the Black Sea phytoplankton, which are for specific areas and for the World Ocean as a whole. considered as a ground for development of algorithms for calculation of the satellite-based primary produc- So far, such estimates have had poor precision. For the tion values. open oceanic waters, the error is 60%, while for the coastal waters it increases up to 100% [26]. As a rule, one of the reasons is related to the limited number of MATERIALS AND METHODS P−I experiments used for the calculations of the primary production values. Based on them, it is difficult to The studies were carried out over twelve oceano- graphic cruises in the Black Sea, at stations located estimate the spatial and temporal variability of the ′ ′ parameters studied in all the identified provinces. In between 41°30 Ð45°30 N in different months and years addition, in the pelagic zone of the ocean, no well- (Fig. 1). The greatest number of measurements was defined boundaries of the areas varying from season to performed in the deep-water areas of the sea from season and from year to year are available. For extrap- December to January (1988 and 1992), from March to April (1988 and 1995), from June to July (1996 and αB B olation of the and Pmax values measured at selected 1990), and from August to September (1980 and 1992). stations to the scales correlated with the inhomoge- At every station, the chlorophyll concentration, temper- neous character of the satellite-based chlorophyll distri- ature, and incident solar radiation at the sea surface

N 47° 1 44.6 46° 2 3 4 45° 44.2 33.2 33.6

44°

43°

42°

41°

28° 30° 32° 34° 36° 38° 40° E

Fig. 1. Layout of the stations where photosynthetic parameters of the surface phytoplankton were measured (200-m depth contour line is indicated): 1—winter (36 stations); 2—spring (52 stations); 3—summer (45 stations); and 4—fall (31 stations).

OCEANOLOGY Vol. 42 No. 1 2002

VARIABILITY OF PHOTOSYNTHETIC PARAMETERS 55 were measured, and the experiments estimating the active radiation (E350Ð700 nm), a coefficient of 0.45 was effect of light on phytoplankton photosynthesis were used. conducted. In total, 164 experiments were carried out, Measurement of the phytoplankton photosynthe- of them, 36 in winter, 52 in spring, 45 in summer, and sis rate. The rate of photosynthesis was measured by 31 in fall. the difference between the values of H14COÐ absorp- In June 1996, the spectral light absorption by the 3 surface phytoplankton was determined at 20 stations tion by phytoplankton in the light and dark flasks in two located off the southern coast of the Crimea (Fig. 1) and replicates. After completion of the experiment, the sam- at 2 stations in the deep-water (42°55′–43°00′ N and ples were filtrated under moderate vacuum (down to ′ ′ ′ ′ 0.25 atm) through a membrane filter with a mesh size 30°48 –31°08 E) and shelf (44°00 –44°10 N and µ 33°01′–33°13′ E) parts of the sea during the period of 0.45 m. The isotopes absorbed by filters were from 1998 to1999. In total, 73 measurements were car- washed with 5 ml of a 1% HCL solution and 10 ml of a ried out. sea water ultrafiltrate. The radioactivity of the filters was measured in a scintillating liquid by means of a Measurement of phytoplankton photosynthetic Rack Beta counter. The carbon content in all the forms parameters. For detection of the photosynthetic of carbon dioxide was calculated by standard formulas parameters of phytoplankton, water samples were [4]. For the photosynthetic zone, this value ranged from exposed to different light intensities for twoÐthree 33 to 36 mgC/l. hours at the temperature that was observed within the Measurement of chlorophyll a concentration. In surface layer. As a light source, white fluorescent lamps order to improve the data comparability, aliquots were with a spectral composition close to that of sunlight simultaneously taken from the 10-l bottle water sample. were used. In the studies performed before 1990, the These aliquots were used for determination of the chlo- photosynthesis rate was determined at eight light inten- rophyll a concentration and the rate photosynthesis. sities, namely, from 1 to 150 W mÐ2. Different levels of Samples 1Ð2 l in volume were filtrated through a mem- irradiance were produced by filters with a neutral spec- brane filter with a mesh size of 0.45 µm. Pigments were tral transmission characteristic. In the later studies, an extracted with 90% acetone over 18 h. After centrifuga- incubator, where the photosynthesis rate was measured tion of the extract, the chlorophyll a and phaeophytin at 16 light levels, from 1 to 200 W mÐ2, was used. A concentrations were measured by a standard fluoromet- halogen lamp served as a light source. In front of the ric method [28], according to the technique described lamp, a blue filter and a 5% solution of CuSO were 4 in [10]. placed to remove the light with wavelengths greater than 760 nm. Attenuation of the density of incident In the studies performed in June 1996, the chloro- light flux at the flask surface was provided by sequen- phyll concentration was measured by the light absorp- tial arrangement of the samples at different distances tion by phytoplankton at the wavelength of 680 nm. from the light source. To enhance the light attenuation The set of comparative measurements (n = 32) showed between the flasks, light filters with a neutral spectral that, in the range of concentrations from 0.2 to 3 Ð1 transmission characteristic (K = 50%) were used. The 1.1 mg/m , the light absorption values (aph, m ) at this spectral composition of the efficient radiation was close wavelength are directly proportional to the chlorophyll a to that of fluorescent lamps and sunlight in the PhAR content measured by the fluorometric method, namely, range. a ()680 ==0.0189 Chl r2 0.92. (1) Measurement of light. In the course of the labora- ph tory experiments, the light incident on a plane flask sur- Light absorption by phytoplankton. Water sam- face and inside it was studied. To measure the light ples 1Ð2 l in volume were filtrated through GF/F filters, inside the flasks, light pipes with a condensing sphere and prior to the measurements, they were kept in a (a bubble of opal glass) fixed at the pipe end were Dewar flask with liquefied nitrogen at a temperature of – employed. Another end of the light pipe was connected 70°C. The spectrum of light absorption by particulate mat- λ λ ≤ λ ≤ to a photocell. The incident light was measured by ter (ap( )), where is the wavelength, 400 750 nm), means of a quantometer and luxmeter calibrated was measured under laboratory conditions by means of against the readings of a quantometer in the photosyn- a spectrophotometer by the Yentsch method [53] in the thetically active radiation range. For transition from modification of Mitchell and Kiefer [40, 41]. The λ units of irradiance to energetic units, an empirically amount of light absorbed by phytoplankton (aph( )) found relationship, namely, 1000 lk ≈17.2 µE m–2 s–1 ≈ was measured following [33], i.e., by the difference 3.47 W m–2, was used. between the spectral characteristics of particulate mat- The intensity of the incident solar radiation was ter and those of the particles without pigments. For the measured using a nonselective thermoelectric pyra- transition from the values of the optical density of the nometer from sunrise to sunset in the days when the suspended matter on the filter to the values of its optical experiments were set up. The average value for a light density in suspension, the equation from [39] was used. day was calculated. For the transition from the absolute Maximum quantum yield of phytoplankton pho- energetic values (E350Ð3000 nm) to photosynthetically tosynthesis. In the experiments carried out in June

OCEANOLOGY Vol. 42 No. 1 2002 56 FINENKO et al.

PB, mgC mgChl–1 h–1 The spectral properties of the light energy in the experiment (Q(λ)) were determined as the product of the 6 energy spectrum of the light source (E(λ)), the spectrum (a) λ 2 of the light absorption by a 5% solution of CuSO4–S( ), and the blue filter spectrum (F(λ)): 4 Q()λ = E()λ F()λ S()λ . (4) 1 Mathematical description of the photosynthesisÐ light relationship. To describe the photosynthesisÐ 2 light dependence, the empiric equation offered by Platt et al. [45] was used: B B[]β()αB B ()B Ik(1) Ik(2) P = Ps 1 Ð exp I/Ps Ð exp I/Ps , (5) 04080 120 160 where PB is the photosynthetic intensity (mgC mgChlÐ1 hÐ1) I, W m–2 at the density of a light flux I (W mÐ2); PB is the scaling 6 s Ð1 Ð1 B (b) 1 factor (mgC mgChl h ); α is the initial slope of the light curve [(mgC mgChlÐ1 hÐ1)/(W mÐ2)]; and β is the photoinhibition parameter [(mgC mgChlÐ1 hÐ1)/(W mÐ2)]. 4 β 2 In the absence of photosynthesis inhibition ( = 0), B Ps is equal to the maximum intensity of photosynthe- B 2 sis (Pmax ). For calculation of the coefficients, a standard Sigma-Plot software package was used. The parameter Ik corresponds to the intersection of the Ik(1) Ik(2) extrapolated linear segment with the level of photosyn- 050100 150 200 thesis saturation, I = PB /αB. I, W m–2 k max

Fig. 2. Typical relationships between the light and intensity RESULTS of photosynthesis (PB) of the surface phytoplankton (a) in (1) the winter and (2) spring seasons and (b) in (1) the sum- Spatial variability of phytoplankton photosyn- mer and (2) fall seasons. Horizontal dashed lines corre- thetic parameters. Figure 2 shows typical curves for spond to the maximum values of photosynthesis intensity the relationship between the intensity of photosynthesis B B (Pmax ); vertical dashed lines correspond to the intersec- (P ) and light (I). Throughout the year, at variations of tions of the extrapolated linear segments with those of the the power of the light flux in the experiments from 0.5 levels of the photosynthesis saturation (Ik). to 150Ð200 W mÐ2, no photoinhibition of the light flux took place. The curves had a similar shape and varied only in the initial inclination and in the maximum 1996 (in the vicinity of Balaklava), the maximum quan- B φ value. During the winterÐspring period, the P values tum yield of photosynthesis ( max) was determined by measured reach their peak and flatten out. In the sum- the formula mer, the maximum PB values obtained in the experi- φ α ments differ from the calculated PB values by less max = /aph, (2) max than 10%. Despite a certain variability in the experi- where α is the initial slope of the lightÐphotosynthesis mental data, they are described well by the curve calcu- αB B rate curve; aph is the value equal to the quantity of lated by equation (5). When and the Pmax parame- absorbed quanta, which is normalized to the flux of the ters were estimated, the coefficient of variation ranged incident quanta in the range of the photosynthetically within 5Ð20% and was 10% on average. According to active radiation calculated by the formula the definition, Ik is a derivative from the calculated val- αB B 700 ues and Pmax and the accuracy of its estimate depends on that of the determination of these parameters. a ()λλ d Q()λ d() λ ∫ ph During the cold period of the year (from December 400 aph = ------. (3) to March), the water temperature within the surface 700 layer ranges in relatively narrow limits, namely, from 7 ∫ Q()λ d() λ to 11°C, while the photosynthetically active radiation inci- Ð2 400 dent at the sea surface (I0) varies from 28 to 130 W m .

OCEANOLOGY Vol. 42 No. 1 2002 VARIABILITY OF PHOTOSYNTHETIC PARAMETERS 57

αB B Table 1. Seasonal changes in the photosynthetic parameters ( , Pmax , and Ik) of phytoplankton, average intensity of incident solar radiation in the range of photosynthetically active radiation per light day (I0), temperature (T), and chlorophyll a concentration (Chl. a) within the surface layer of the Black Sea (0Ð2 m). The first line is the average value, the second line is the standard deviation, and the third line is the limits of variations

αB B Month, year Pmax Ik I0 I0/Ik T Chl. aN

January, 1989, 1992 0.11 2.80 25 68 2.80 8.0 0.89 20 (0.014) (0.53) (4) (19) (0.4) (0.9) (0.41) 0.07Ð0.13 1.82Ð3.75 17Ð30 35Ð90 1.6Ð3.5 6.5Ð10.0 0.30Ð4.80 February 1992 0.17 2.80 16 44 2.74 7.7 1.46 3 (0.01) (0.26) (3) (10) (0.5) (0.3) (0.12) 0.16Ð0.18 2.60Ð3.10 14Ð19 28Ð50 2.3Ð3.3 7.8Ð8.0 1.32Ð1.53 March 1989, 1995 0.13 4.82 39 107 2.72 9.19 2.14 22 (0.03) (1.05) (12) (20) (1.2) (1.0) (0.60) 0.07Ð0.13 2.00Ð6.00 28Ð85 60.0Ð130 0.3Ð4.3 7.0Ð11.0 0.37Ð3.54 April 1995 0.08 3.92 50 139 2.70 11.6 0.41 18 (0.016) (1.13) (18) (27) (0.6) (2.3) (0.30) 0.05Ð0.13 2.54Ð6.60 23Ð63 40Ð184 1.1Ð3.7 10.0Ð12.0 0.10Ð1.00 May 1990 0.07 4.64 66 165 2.50 15.0 0.33 5 (0.010) (0.56) (8) (24) (0.5) (1.0) (0.20) 0.05Ð0.08 3.85Ð5.20 55Ð70 130Ð200 2.0Ð3.0 14.0Ð16.0 0.15Ð0.60 June 1989, 1996 0.08 5.51 69 210 2.47 19.7 0.25 20 (0.011) (1.50) (7) (38) (0.34) (1.6) (0.10) 0.07Ð0.09 4.00Ð7.00 60Ð76 168Ð230 1.8Ð3.5 5.0Ð23.0 0.12Ð0.38 July 1990 0.08 5.94 74 193 2.76 20.0 0.36 25 (0.018) (2.1) (25) (25) (0.72) (2.0) (0.25) 0.05Ð0.12 3.00Ð11.10 45Ð108 150Ð229 1.2Ð4.2 18.0Ð22.5 0.13Ð1.67 August 1992 0.08 7.70 93 245 2.0 23.0 0.18 4 (0.006) (0.95) (41) (21) (0.20) (0.0) (0.05) 0.08Ð0.09 7.00Ð9.10 60Ð168 221Ð257 1.7Ð2.2 23.0 0.14Ð0.25 September 1980 0.07 4.14 58 172 2.0 20.0 0.16 23 (0.016) (1.10) (6) (32) (0.40) (1.3) (0.20) 0.04Ð0.12 2.00Ð7.80 50Ð65 140Ð215 1.8Ð3.6 18.0Ð22.0 0.03Ð1.10 October 1990 0.09 3.88 45 119 2.64 16.0 0.43 5 (0.017) (0.81) (15) (21) (0.30) (0.0) (0.10) 0.06Ð0.10 2.95Ð4.70 30Ð60 98Ð140 2.2Ð3.2 16.0 0.33Ð0.55 November 1989 0.10 2.71 28 78 2.36 13.0 0.71 3 (0.017) (0.53) (5) (15) (0.20) (0.0) (0.21) 0.08Ð0.12 2.20Ð3.30 22Ð38 60Ð93 2.4Ð3.0 13.0 0.51Ð0.89 December 1988 0.10 2.42 24 61 2.54 9.0 0.85 14 (0.021) (0.60) (5) (27) (0.42) (1.0) (0.15) 0.06Ð0.11 1.70Ð3.35 18Ð31 33Ð88 2.0Ð3.1 8.0Ð10.0 0.62Ð1.08

B Ð1 Ð1 αB Ð1 Ð2 –2 ° Note:Pmax —mgC mgChl h ; —mgC mgChl /(W m ); Ik and I0—W m ; T—temperature, C; Chl a—chlorophyll a concentration, mg/m3.

OCEANOLOGY Vol. 42 No. 1 2002 58 FINENKO et al.

Under these conditions, the αB values measured at period (from December to March), whereas in the some stations differ by a factor of three, i.e., from 0.06 period from April to October they are rather stable. B B to 0.18. In a similar way, the Pmax values changed from Depending on the environmental conditions, the Pmax 1.7 to 6.0 (Table 1). The values of the photosynthetic values range within wider limits than those of αB. The parameters measured in the deep part of the sea and in latter reliably differ between the cold and warm periods the areas of the continental slope were close. On aver- of the year at a level of significance equal to 0.01. αB age, the coefficient of variation for was 17% and for The average values of Ik regularly increased from the B Ð2 Ð2 Pmax it was somewhat greater—25%. winter (16Ð25 W m ) to the summer (69Ð93 W m ). During the summer period, the maximum values of The effect of light and temperature on the photo- αB were found in the area of the continental slope, in the synthetic parameters. The coefficients of simple cor- ± αB B northwestern and southern parts of the sea (0.11 relation of the , Pmax , and Ik parameters with temper- 0.015). In the deepwater part of the sea and on the shelf ature and light are given in Table 2. During either of the southern coast of the Crimea, they were lower period of the year, the coefficients of correlation B (0.07 ± 0.018). The P values varied in synchronism B αB B max between the Pmax and values and the Pmax and Ik val- with those of αB. Similar regional differences were ues are reasonably high and reflect the coupling of the found in September. In the northwestern part of the light and dark reactions of photosynthesis. During the αB B αB continental slope, the mean values of and Pmax were winter–spring period, a significant correlation of and αB equal to 0.11 ± 0.015 and 6.20 ± 1.51, respectively, T and of and Io (r = 0.48 and r = 0.35, respectively) whereas in the deepwater areas they were 0.06 ± 0.014 is observed, while during the summerÐfall period, it is and 3.92 ± 0.80, respectively. As we can see, during the B absent. The Pmax values correlate with T and Io during summer period, the values of the photosynthetic param- both periods of the year, but for the cold period, the eters of phytoplankton in the waters of the continental coefficients of correlation are 1.5 times higher than for slope, where greater chlorophyll concentrations were the warm period (Table 2). The I parameter correlates observed, were 1.5 times as great as in the deepwater k areas. Owing to the coupled action of the variations of with T and Io during the winterÐspring period (r = 0.65 and r = 0.50, respectively), but for the summerÐfall the αB and PB values, a relative stability of the mean max period only the correlation between Ik and T (r = 0.55) Ð2 values of the Ik parameter (56Ð65 W m ) was observed. is reliable. The coefficients of variation for photosynthetic param- The effect of solar radiation (Io) on the photosyn- eters were equal both under the conditions of a moder- thetic parameters of phytoplankton was estimated in the ately calm sea in the summer and under the intensive experiments carried out in the cold (from December to turbulent mixing in the winter (15Ð25%). March) and warm (from June to September) periods of Seasonal dynamics of the photosynthetic param- the year at different Io values and a relatively constant B ° eters. Throughout the year, the average monthly P temperature (8Ð10 and 19Ð21 C, respectively). When, max during the winterÐspring period of the year, the solar ra- values increase from 2.40 to 7.70 from December to diation values change by a factor of 2Ð5, no reliable August, and then they decrease (Table 1). The maxi- B B αB mum α values are characteristic of the winterÐspring correlation between Pmax, , Ik and Io was observed

Table 2. Correlation matrix for the data obtained for the surface layer. Coefficients of correlation (r) were calculated from 63 measurements carried out from December to March (gray background) and for 90 measurements carried out from April to October

αB B Pmax Ik I0 T

αB 1 0.57 0.17 0.35 0.48

B Pmax 0.55 1 0.79 0.76 0.86

Ik 0.28 0.61 1 0.50 0.65

I0 0.04 ns 0.46 0.15 ns 1 0.57 T 0.08 ns 0.57 0.55 0.39 1

Note: T—temperature at which the experiments were conducted; I0—average solar radiation per light day in the range of photosynthetically Ð2 αB B active radiation (W m ); Ik, , and Pmax —photosynthetic parameters; ns—not reliable value at signiﬁcance level p = 0.05.

OCEANOLOGY Vol. 42 No. 1 2002 VARIABILITY OF PHOTOSYNTHETIC PARAMETERS 59

() DecemberÐJanuary ( ) 10 5 (‡) (b) JuneÐSeptember () March –1 h

–1 –1 8 5

4 6 mgC mgChl , B max 4

P 3

T = 8Ð10°C T = 19Ð21°C 2 2 (c) (d) 60 100 –2 W m

, 40 80 k I

20 60

T = 8Ð10°C T = 19Ð21°C 0 40

) 0.12 –2 0.16 (e) (f) W m

/ ( 0.10 –1 h

–1 –1 0.12 0.08

0.06 mgC mgChl

, 0.08 B

α T = 8Ð10°C T = 19Ð21°C 0.04 04080 120 160 80 140 160 200 240 –2 –2 I0, W m I0, W m

B αB Fig. 3. Variability of the (a, b) Pmax , (c, d) Ik, and (e, f) values of the surface phytoplankton in the cold and warm periods of the year at different intensities of solar radiation (I0) incident at the sea surface.

(Fig. 3). During the summerÐfall period, a weak corre- of the year were used. From the data shown in Fig. 4a, lation of PB and I with I was found, because only we can see that within the biokinetic interval of temper- max k 0 atures, during the winterÐspring and the summerÐfall 25% of the points were described by a linear relation- B ship (r2 = 0.25 and r2 = 0.28, respectively). Since phy- periods, the ﬂuctuations of the Pmax values are related toplankton adaptation to different intensities of incident to the temperature and are described by the exponential radiation was not followed by the regular dynamics of function: photosynthetic parameters, one can assume that the B () 2 Pmax ===1.68exp 0.074T n 40, r 0.58, (6) B αB seasonal ﬂuctuations of the Pmax , , and Ik values are B () 2 controlled by temperature. To check this assumption, Pmax ===2.46exp 0.076T n 21, r 0.72, (7) the results of the measurements conducted throughout B () 2 the temperature interval in the cold and warm periods Pmax ===0.82exp 0.085T n 60, r 0.56. (8)

OCEANOLOGY Vol. 42 No. 1 2002 60 FINENKO et al.

12 perature of its dwelling (8 and 22°C, respectively) (a) shows that they are two times lower in the winterÐ spring phytoplankton than in the summer. However, after changing the maximum intensity of photosynthe- –1 ° h sis of the summer phytoplankton from 22 to 8 C –1 –1 8 according to equation (8), it becomes threeÐfour times lower than in phytoplankton during the winterÐspring period. These differences can either be accepted as a proof for the increase in the maximum photosynthesis

mgC mgChl intensity of phytoplankton, adapted to low tempera-

, tures, or be understood as a result of the different 4

B 1 max extents of phytoplankton supply by biogenic elements. P 2 Since most of the measurements, excluding those conducted in March, were carried out at relatively low 3 nitrate and phosphate concentrations within the surface layer (<0.15 µM), one can assume that they equally 0 B inﬂuenced Pmax at all the temperatures. In March, (b) 120 when diatoms featured mass vegetation at a relatively high nitrate concentration within the mixed layer, which reached 0.4Ð2.0 µM at individual stations, B greater Pmax values were observed at the same temper- –2 80 atures as compared to January.

W m The light intensity values at which the onset of the , k light saturation in terms of photosynthesis (I ) is I k observed also depend on the temperature (Fig. 4b), and, 40 for all the seasons, the Ik—temperature relationship is described by a common equation: () Ik ==17.4exp 0.066T , n 164, (9) 2 0 5 10 15 20 25 r = 0.70, at 6.5 ≤≤T 23°C. T, °C αB B B Because = Pmax /Ik from equations (6)Ð(9) it fol- Fig. 4. Effect of temperature on (a) variations of Pmax val- ° ues (1) at the beginning (December to January) and the end lows that at the temperature increase from 10 to 20 C, (April) of the winterÐspring phytoplankton vegetation, (2) αB can increase by 14% on average. As we can see, the at the maximum of the winterÐspring phytoplankton vege- share of temperature in the total αB variability is negli- tation (February to March), and (3) at the summer phase of gible. phytoplankton vegetation; (b) variations of the Ik values during all the seasons. Throughout the year, the averaged monthly ratio I0/Ik has small variations, because with the growth of Equation (6) was obtained for the beginning of the temperature, simultaneously, the intensity of incident winterÐspring phytoplankton vegetation period (from solar radiation increases, and on average, the Ik value is ± December to January) and for the time after its comple- 38% of I0, or Ik = (0.38 0.09)I0. tion (April); equation (7) was acquired for the winterÐ spring peak of phytoplankton vegetation period (from Ratio between the rate of phytoplankton photo- February to March); and equation (8) was obtained for synthesis and chlorophyll concentration. For four the summer period (from June to September). periods of the year, when the water temperature (T) within the surface layer ranged by not more than 3Ð5°C Attention is drawn to the fact that in the above equa- (the ﬁrst period lasted from December to February, the tions corresponding to Q10 = 2.1Ð2.3, the difference second was March, the third period lasted from April to between the exponents is very small. Therefore, the May, and the fourth lasted from June to October, phytoplankton adaptation to low and high temperatures Figs. 5a, 5b), the correlation between the rate of photo- does not cause variations in the temperature coefﬁcient synthesis and the chlorophyll concentration (Chl) was B B Pmax. A comparison of the Pmax values in the winterÐ found. At such an integration of the data obtained, the Ð3 Ð1 spring and summer phytoplankton at the average tem- maximum rate of photosynthesis Pmax (mgC m h ),

OCEANOLOGY Vol. 42 No. 1 2002 VARIABILITY OF PHOTOSYNTHETIC PARAMETERS 61 depending on the chlorophyll concentration (excluding (a) March), is described by a power function: 25 1.25 ≤≤ 2 Pmax = 2.87 Chl at 0.3 Chl 2.2,

(10) –1 20 ≤≤ 2 h 1

6.5 T 9.5, r ==0.93, n 36, –3 1.01 ≤≤ 15 Pmax = 4.73 Chl at 0.3 Chl 3.5,

(11) mgC m 7.0 ≤≤T 11.0, r2 ==0.96, n 23, , 10 max P P = 5.22 Chl1.27 at 0.1≤≤ Chl 1.0, max (12) 5 10.0 ≤≤T 14.0, r2 ==0.93, n 23, P = 5.91 Chl1.16 at 0.07≤≤ Chl 1.7, 012 3 4 5 max (13) 2 18.0 ≤≤T 23.0, r ==0.89, n 76. (b) Equations (10)Ð(13) are given for the first to the 12 fourth periods, respectively. For the first, third, and 2 –1 fourth periods of the year, the exponents are approxi- h mately the same, but the coefficient of proportionality –3 9 increases by a factor of 1.8 with the temperature growth. During all the periods of the year, excluding mgC m 6 March, the value of the power coefficient differs from , 1 unity (at p < 0.05) and Pmax shows a nonlinear increase max P as the chlorophyll concentration increases. In this case, 3 the growth in the chlorophyll concentration by a factor of 10 causes an increase in the maximum intensity of B photosynthesis (Pmax ) by a factor of 1.5Ð2.0. Thus, 0 0.3 0.6 0.9 1.2 1.5 phytoplankton responds to the variations in the environmental conditions, first of all, by rather great fluctua- (c) tions in its biomass and smaller changes in specific pro- 0.8 duction. ) –2 The relationship between the rate of photosynthesis on Ð3 Ð1 Ð2 0.6 the initial part of the light curve (α, mgC m h /(W m )) W m and the chlorophyll concentration is also described by / ( –1 a power-law function (Fig. 5c). However, unlike the h

–3 0.4 Pmax values, the values of the exponent and coefficient of proportionality are barely recognized during all the

periods of the year, namely, 1.17Ð1.31 and 0.10Ð0.12, mgC m

, 0.2 respectively. Therefore, the data obtained in all the sea- α sons can be integrated. Then, 1.28 α = 0.11 Chl at 0.07≤≤ Chl 5.0, 012 3 4 5 (14) –3 7 ≤≤T 23 r2 ==0.95, n 164. Chl ‡, mg m From equations (10)Ð(14) it follows that throughout Fig. 5. Relationship of (a, b) the maximum photosynthesis the year, excluding March, a linear relationship rate Pmax and (c) the initial slope of the photosynthesisÐ between P and α is observed. In March, the relation light curve to chlorophyll a concentration. (a) 1—March; max 2—December–January; (b) 1—April–May; 2—June–Octo- between these parameters is described by a power-law ber; and (c)—January–December. α0.80 function Pmax = 27.4 . Ratio between the aB values and chlorophyll con- values and the chlorophyll concentration adheres to a αB power-law function over the interval of the values mea- centration. Equation (14) shows that the parameter sured: also depends on the chlorophyll concentration. The data obtained for all the seasons are given in Fig. 6. αB = 0.11 Chl0.29 at 0.07≤≤ Chl 5.0, Despite a rather wide dispersion of the points, they (15) 2 show that the form of the relationship between the αB r ==0.68, n 164.

OCEANOLOGY Vol. 42 No. 1 2002 62 FINENKO et al.

αB, mgC mgChl–1 h–1 /(W m–2) the αB and nitrate concentration values. The parallel 0.20 measurements of the nitrate concentration values and the αB values were conducted at individual stations in the coastal area off the southern part of the Crimea in the summer and also during the winterÐspring period in 0.16 the southeastern and central parts of the sea. The nitrate concentration values within the 0- to 15-m layer varied from 0 to 2.0 µM, and the αB values ranged from 0.04 to 0.21 mgC mgChlÐ1 hÐ1/W mÐ2. The minimum values 0.12 of αB and the nitrate concentration were observed in the summer, while the maximum ones were confined to the period from February to March. Clearly, these differences are not occasional and reflect the αB variations in 0.08 the water with the nitrate concentration (Fig. 7). For description of this dependence, a modified equation of the MichaelisÐMenthen type was used:

αB ==0.055+() 0.17N/0.7 + N r2 0.75, (16) 1 2 3 4 5 Chl ‡, mg mÐ3 where N is the nitrate concentration, µM. At low nitrate concentrations (0.01Ð0.10), the αB Fig. 6. Relationship between the initial slope of the photo- synthesisÐlight curve (αB) and chlorophyll a concentration. values for the summer and spring phytoplankton are fairly close but they are trebled when, in the period from February to March, the concentration reaches αB, mgC mgChl–1 h–1 /(W m–2) 2 µM. 0.20 Quantum yield of photosynthesis. The measurements of the maximum rate of photosynthesis and light absorption by the surface phytoplankton carried out 0.16 simultaneously off the southern coast of the Crimea in φ June showed that the max values vary from 0.005 to 1 0.015 and make up 0.011 ± 0.003 mole C (mole quanta)Ð1 0.12 2 on average. For calculation of the quantum yield in other areas, where such simultaneous measurements of the rate of photosynthesis and light absorption by phy- 0.08 toplankton were not available, the results of 53 determi- nations of the spectral light absorption by the surface phytoplankton were used. They were carried out at two 0.04 fixed stations in the deepwater and coastal areas of the sea in different seasons of 1998Ð1999. The data analysis showed that in the Black Sea a power-law dependence between the coefficients of light absorption by Ð1 0 1 2 3 phytoplankton (aph, m ) at the wavelengths of 440 and –1 [NO3 ], µM 678 nm and the chlorophyll concentration in the range from 0.1 to 2.5 mg mÐ3 is valid: Fig. 7. Initial slope of the photosynthesisÐlight curve (αB) as a function of nitrate concentration. 1—June; 2—Febru- () 0.63 2 aph 440 ==0.040Chl r 0.63, (17) ary and March. () 0.81 2 aph 678 ==0.020Chl r 0.85. (18) From equation (15) it follows that the αB values The average (over the spectrum) specific coefficient of grow twofold as the chlorophyll concentration light absorption by phytoplankton in the range from increases from 0.07 to 3.0 mg mÐ3. 400 to 700 nm (aph* ) is B Relationship between the α values and nitrate Ð0.38 a* = 0.015 Chl . (19) concentration. As has been shown above, the light and ph temperature weakly control the αB fluctuations; there- Using equations (17)Ð(19) and the data on the chlo- fore, the data obtained in the different seasons were rophyll concentration within the surface layer obtained integrated for the analysis of the relationship between at 164 stations, we calculated the average ratios

OCEANOLOGY Vol. 42 No. 1 2002 VARIABILITY OF PHOTOSYNTHETIC PARAMETERS 63

φ –1 max, moleC (mole quanta) 0.08 (a) (b)

0.06

0.04

0.02

0 1 2 3 4 2.0 2.5 3.0 3.5 4.0 –3 Chl a, mg m aph* (440)/aph*(678)

φ Fig. 8. Maximum quantum yield of photosynthesis of the surface phytoplankton ( max) as a function of (a) the chlorophyll a concentration and (b) the ratio between the values of the speciﬁc coefﬁcient of light absorption by phytoplankton at 440 and 678 nm.

φ between the specific coefficients of light absorption by ( max aph* ) increases as the chlorophyll concentration Ð3 pigments at 440 and 678 nm, aph* (400Ð700 nm) for increases up to 3 mg m . every station, and the maximum quantum yield: DISCUSSION φ = k()αB/a* , (20) max ph During the early studies carried out in the Black Sea, where k is the coefficient of conversion from gram to the photosynthesis intensityÐlight dependence was mole, hour to second, and watt to mole quanta equal to determined in the in situ experiments [8]. In the deepwater areas of the sea, the PB value for the surface 0.005; aph* is the average specific light absorption by max phytoplankton normalized to chlorophyll a in the range phytoplankton increased from 3.50 ± 1.33 to 6.72 ± from 400 to 700 nm (m2 (mg Chl)Ð1). 1.77 mgC mgChlÐ1 hÐ1 from April to September. Close values were obtained in the studies conducted later, in φ Throughout the year, the max values estimated var- the summerÐfall period [1Ð3]. The seasonal dynamics ied within the limits of an order of magnitude, namely, B of P in the deepwater areas of the sea and in Sevas- from 0.005 to 0.06 mole C (mole quanta)Ð1. For the max winter, spring, and summer and fall, they were 0.032 ± topol Bay are similar [6, 8]. During the spring period, ± ± B 0.01, 0.034 0.02, and 0.013 0.006 on average, the Pmax values range from 1.8 to 4.2, in the summerÐ respectively. As we can see, for the summer period, the fall period they vary from 5 to 15, while in the winter estimated values were roughly similar to the measured Ð1 Ð1 φ they are not greater than 2.5 mgC mgChl h . ones. Using all the data, we obtained that the max val- B ues regularly increase as the chlorophyll concentration The average values of Pmax for the Black Sea and grows (Fig. 8a) and the kinetics of the process can be oceanic phytoplankton of the temperate latitudes are described by MichaelisÐMenthen equation: reasonably close. According to the results from many measurements performed in the winterÐspring period φ 2 ° ° max ==0.093 Chl/1.76+ Chl, r 0.90. (21) between 38 and 50 N in the coastal and deep-water regions of the Atlantic Ocean, the average PB values φ max At the same time, it was found that, between the max ranged from 2.7 ± 1.3 to 3.7 ± 1.3, while in the summer values and the specific ratio of the absorbed light at 440 they varied from 5 to 7 mgC mgChlÐ1 hÐ1 [47]. The mea- and 670 nm, an inverse relationship is observed surements carried out in the spring (from April to May) (Fig. 8b). A comparison of the character of variations in ° ° ° B φ at 20 W and from 35 to 50 N showed that the Pmax the max and aph* values with the chlorophyll concentra- values reach 6Ð10 mgC mgChlÐ1 hÐ1 at a temperature of tions shows that they go in opposite directions: with a ° rise in the chlorophyll concentration, the φ values 16 C [38]. In the subtropical Atlantic waters, the same max values were found from April to May [35]; they are * increase, while the aph values decrease. As a result, the approximately twofold greater than in the Black Sea in efficiency of photosynthesis (αB) equal to the product the spring period, but they are obtained at a higher tem-

OCEANOLOGY Vol. 42 No. 1 2002 64 FINENKO et al.

B B perature. The Pmax values for the winterÐspring phy- found in the period of our studies, the expected Pmax toplankton of the Black Sea, reduced to 16°C according values should be equal to 5.2 and 6.4, respectively. to equations (6)Ð(7), will be within the same limits Thus, at a constant temperature, the fourfold change in (6.1Ð9.5 mgC mgChlÐ1 hÐ1). In the fall (September to the average values of solar radiation from the winter to Ð2 October), the PB values ranged from 4 to the summer (from 60 to 250 W m ) may increase the max B 6 mgC mgChlÐ1 hÐ1 at a temperature of 20Ð22°C, which Pmax values only by a factor of 1.2. During this period, was close to the measured and calculated data for the the increase in the average value of PB was threefold summer Black Sea phytoplankton. max (Table 1). Therefore, the threefold growth of the PB In the Black Sea, in selected seasons, the spatial max values results from the change in the water temperature variability of PB and αB on the scale of a few hundred ° max from 7Ð9 to 20Ð23 C. The Q10 coefficient calculated for kilometers does not exceed 25% (the coefficient of vari- this temperature interval is equal to 2.1. In the phy- ation), whereas the variability of the chlorophyll con- toplankton living under conditions of low or elevated centration is greater (from 30 to 125%, Table 1). The temperatures, Q10 is equal to 2.0 and 2.3, respectively temporal variability of PB (40%) and αB (30%) is (Fig. 4). The generalization of a great amount of data max obtained practically over the whole range of tempera- similar being twoÐthree times lower than that of the ° chlorophyll concentration (106%). Thus, at the level of tures in the ocean (from Ð1 to 28 C) showed that the B the mesoscale variability, the rate of photosynthesis Pmax value increases as the temperature grows within ° normalized to the chlorophyll concentration is a more the interval from Ð1 to 20 C (Q10 = 2.35) and decreases stable parameter than the phytoplankton biomass. in the range from 20 to 28°C [12]. The same or close The studies carried out in the Atlantic Ocean (from values of Q10 were gained in the early studies carried 50°N to 50°S) point to the fact that the large-scale vari- out in the coastal waters off New York [34], Nova B Scotia [44], and in Tokyo Bay [30, 51]. ability of the P (84%) and chlorophyll concentra- max According to our studies, the share of temperature in tion (102%) values are about the same [38]. The mesos- the total variability of PB was 50Ð70%. In the sub- cale variability of PB and αB in the subtropical area max max tropical waters of the Atlantic Ocean, it ranged from 40 of the Atlantic Ocean ranged from 16 to 60% [35] and, to 60%, but when analyzing the combined effect of the on average, was two times lower than on the scale of temperature and nutrient concentration (nitrogen, phos- several thousands of kilometers. The high variability of phate, and silicates) on the variations in the PB val- the PB parameter in this area is related to the inclu- max max ues, the coefficient of determination increases to sion into the analysis of the data obtained at different 0.70−0.84 [35]. depths. Since in the tropical and subtropical waters the In the Black Sea, the temporal dynamics of the αB PB values decrease with depth [11, 38], one can max values differs from the seasonal changes in the PB believe that they reflect the variability within the water max column rather than within the surface layer. values. Comparatively high values were found from November to March (0.10Ð0.20); in the summer, they B are two times lower on average. Not much of the data By our data, a weak correlation between the Pmax 2 obtained before for the summer and fall periods is and I0 values (r = 0.25) was observed only in the sum- within the same limits [1, 8]. An analysis of the data merÐfall period, whereas for the winterÐspring period it showed that the αB parameter was not governed by was not observed. Previously, owing to the data of the light, and the temperature contribution to the total vari- in situ experiments in the Black Sea, it was shown that, αB in the summer period, a positive correlation between ability of the parameter was small (Table 2). At the same time, it was found that the αB values increase with incident radiation and light photosynthetic optimum is µ frequently found [5]. By the results of a great number the growth of nitrate concentration up to 2 M (Fig. 7). of experiments with different species of algae, which A similar character of the relationship was found dur- were carried out at a rather constant temperature (18Ð ing the spring phytoplankton vegetation in the Sargasso 22°C) and a sufficient nutrient supply, the relationship Sea, when the nitrate concentration in the water decreases [46]. The data obtained in the Indian Ocean between the density of the light flux (I0), to which the B [49] may be regarded as an argument in favor of the B algae were adapted, and Pmax can be described by the assumption that nitrates control the variations in the α function [22] PB = a + bIlog( ), where PB is values. Although the dispersion of the values is very max 0 max wide, the data in the Sargasso Sea and in the Indian Ð1 Ð1 expressed in mgC mgChl h , a = 1.58, and b = 0.88 Ocean are described by the same curve. The relations ≤ Ð2 ≤ at 1 I0, W m 250. Therefore, when the monthly between the αB values and nitrate concentration for the Ð2 average I0 values vary from 60 to 250 W m , which was oceanic and Black Sea phytoplankton have the same

OCEANOLOGY Vol. 42 No. 1 2002 VARIABILITY OF PHOTOSYNTHETIC PARAMETERS 65 form, but the coefficients entering into the equations tic, the chlorophyll concentration values ranged from 1 to Ð3 φ differ. At low concentrations of NO3 within the surface 5 mg m and the max values varied from 0.035 to layer (about 0.05 µM), the αB values for the Black Sea 0.05 mole C (mole quanta)Ð1; in the oligotrophic areas and oceanic phytoplankton [46, 49] coincide and equal with a chlorophyll concentration <0.1 mg mÐ3, it 0.06 mgC mgChlÐ1 hÐ1/W mÐ2 on average. At high con- decreased to 0.005 mole C (mole quanta)Ð1 [11]. µ αB centrations of NO3 (about 3 M), the values for the In the Black Sea, at low ratios Ð1 Ð1 Ð2 Black Sea reach 0.2 mgC mgChl h /W m , which is * * φ two times greater than in the Sargasso Sea. In the aph (440 nm)/aph (678 nm) (1.5Ð2.0), the max value spring, in the subtropical Atlantic and in the southern reaches 0.07 mole C (mole quanta)Ð1 and is close to that subtropical zone of convergence, the αB values are obtained in the period of the spring bloom and after it 0.18Ð0.40 mgC mgChlÐ1 hÐ1/W mÐ2 at the same nitrate in the Sargasso Sea [16]. In the Indian Ocean, at the concentrations (1Ð3 µM) [19, 35]. While it is difficult to same ratio of the absorbed light, i.e., φ attach particular significance to one of the nutrients, aph* (440 nm)/aph* (678 nm), the max values were lower nevertheless, we note that, in different areas, at equal than in the Black Sea by a factor of 1.5. These differ- αB NO3 concentrations, some differences in the values ences are determined by the prevalence of small algae are found. They can depend on the light absorption by having higher specific coefficients of light absorption phytoplankton and which are related to the changes in [49]. As the ratio aph* (440 nm)/aph* (678 nm) rises to the size and taxonomic algae composition. 3.0–3.5, the quantum yield decreases about five times It is well known that the algae with large intracellu- (Fig. 8b). It is conceivable that this is related to the dif- lar content of pigments and the cells of large size have ferent nutrient supply of phytoplankton at low and high lower specific coefficients of light quanta absorption chlorophyll concentrations. In the laboratory experi- than the algae with small cellular sizes or low content ments, at the nitrogen-limited rate of algae growth, the of pigments [31, 42]. An increase in the intracellular φ max values decrease [15]. The deficiency of nitrogen content of pigments is followed by the enlarging of decreases the activity of the reaction center of the pho- chloroplasts and increasing of the amount of tilackoids tosystem and the ratio of the reaction centers of photo- and the extent of their packaging, which results, by system II to pigments [33]. As a result, the light analogy with an optically dense system, in the self- absorbed by algae is transformed into chemical energy shading of pigments and in the drop in the specific with a lower efficiency. The high density of the light spectral coefficient of light absorption. The power coef- flux causes a decrease in the efficiency of photosynthe- αB ficients in the Ðchlorophyll concentration and aph* Ð sis due to the increase in the photoptotective pigmentsÐ chlorophyll concentration relationships are different photosynthetic pigments ratio [18]. The drop in the (equations (15) and (19)). As a result, with increases in quantum yield at low chlorophyll concentrations can be the chlorophyll concentration in a wide range of values determined by partial absorption of the light of limited (0.1Ð20 mg mÐ3), the αB values in the Black Sea calcu- photosynthetic utility by photoptotective pigments. φ Thus, the assessment of a sufficiently great amount lated as the product ( max aph* ), will first grow (up to Ð3 of experimental data, for the first time for the Black 3 mg m ) and then decrease. For oceanic phytoplank- Sea, allowed us to find temporal and regional variations αB ton, the maximum values are found at a concentra- in the photosynthetic parameters and to reveal the fea- Ð3 tion of 0.4Ð0.6 mg m , but in the field of low and high tures of their variability depending on the factors that concentrations, they decrease by a factor of 1.3Ð1.8 control their variability. The data analysis points to the [43]. Thus, we can assume that, in the range of the chlo- fact that the key factor determining the temporal varia- rophyll concentrations from 0.1 to 20 mg mÐ3, the pat- tions of the PB values is the temperature, while the αB tern of the variations of the αB values in the Black Sea max will take a dome-shaped form with a single maximum parameter depends on the nitrate and chlorophyll con- in the left-hand part of the curve. centrations and also on the specific light absorption by φ phytoplankton (a* ). A comparison between the average values of max ph for the Black Sea phytoplankton and the data measured For the first time, temporal variations of the maxi- in other areas of the ocean shows that they do not fall mum quantum yield of the Black Sea phytoplankton beyond the expected limits given in Fig. 8. For exam- φ photosynthesis ( max) were studied. The comparison ple, in the waters of the California Current with a chlo- φ * Ð3 φ between the pattern of variations of the max and aph rophyll concentration of 0.2Ð0.4 mg m , the max average for the surface phytoplankton was 0.027 ± values and that of the chlorophyll concentrations shows Ð1 that they proceed in opposite directions; namely, the 0.019 mole C (mole quanta) [50]. In the spring and φ φ max values grow with the increase in the chlorophyll fall, in the subtropical Atlantic, the max averages ranged from 0.017 to 0.034 at a variation of the chloro- concentration values, whereas the aph* values decrease. phyll concentration from 0.1 to 0.3 mg mÐ3 [35]. In the The results of calculations show that the relationship mesotrophic and eutrophic waters of the tropical Atlan- between the αB and chlorophyll concentration values

OCEANOLOGY Vol. 42 No. 1 2002 66 FINENKO et al.

(0.1Ð20 mg mÐ3) can be approximated by a one-peaked 8. Finenko, Z.Z., Phytoplankton Production, Osnovy curve with a maximum at 3 mg mÐ3. produktivnosti Chernogo morya (Productivity Basis in the Black Sea), Kiev: Naukova Dumka, 1979, pp. 88Ð97. The relationships found can form a basis for the jus- 9. Finenko, Z.Z. and Krupatkina, D.K., Primary Production tification of algorithms for the calculation of the pri- and Size Structure of Phytoplankton in the Black Sea in mary production in the Black Sea in terms of the chlo- the WinterÐSpring Period, Plankton Chernogo morya rophyll concentrations and densities of the light flux at (Plankton of the Black Sea), Kiev: Nauk. Dumka, 1993, different depths. They give a possibility to forecast the pp. 74Ð92. temporal and spatial variability of photosynthetic 10. Yunev, O.A. and Berseneva, G.P., Fluorimetric Method parameters within the surface layer of the Black Sea by for Determination of Chlorophyll a and Phaeophytine a remote sensing of the chlorophyll concentration and in Phytoplankton, Gidrobiol. Zh., 1986, pp. 89Ð95. temperature. For the estimation of phytoplankton pro- 11. Babin, M., Morel, A., Claustre, H., et al., Nitrogen- and duction within the water column, the αB parameter is of Irradiance-Dependent Variations of the Maximum Quan- greater importance. In the Black Sea, on the scale of tum Yield of Carbon Fixation in Eutrophic, Mesotrophic, several hundred kilometers, the αB values vary by a fac- and Oligotrophic Marine Systems, Deep-Sea Res. I, tor of 1.5Ð3. Taking these differences into account 1996, vol. 43, no. 8, pp. 1241Ð1272. improves the accuracy of the phytoplankton production 12. Behrenfeld, M.J. and Falkowski, P.G., Photosynthetic calculations from satellite-based data. For the correct Rates Derived from Satellite-Based Chlorophyll Concen- estimation of the primary production within the photo- tration, Limnol. Oceanog, 1997, vol. 42, no. 1, pp. 1Ð20. synthetic layer, we should also consider the vertical 13. Bricaud, A., Babin, M., Morel, A., et al., Variability in variability of the photosynthetic efficiency. the Chlorophyll-Specific Absorption Coefficients of Natural Phytoplankton: Analysis and Parameterization, J. Geophys. Res., 1995, vol. 100, no. C7, pp. 13 321Ð13 332. ACKNOWLEDGMENTS 14. Bricaud, A., Morel, A., Babin, M., et al., Variation of Light Absorption by Suspended Particles with Chloro- This study was supported by NASA, grant phyll a Concentration in Oceanic (Case 1) Waters: Anal- no. NAGW-4709, and NATO, Linkage grant ysis and Implications for Bio-Optical Models, J. Geo- no. LG 973350. phys. Res., 1998, vol. 103, no. C13, pp. 31033Ð31044. 15. 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