06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 687
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
Effect of Mesodinium rubrum (= Myrionecta rubra) on the action and absorption spectra of phytoplankton in a coastal marine inlet
MARGARETH KYEWALYANGA*, SHUBHA SATHYENDRANATH1,2 AND TREVOR PLATT2 INSTITUTE OF MARINE SCIENCES, UNIVERSITY OF DAR ES SALAAM, PO BOX , ZANZIBAR, TANZANIA, 1DEPARTMENT OF OCEANOGRAPHY, DALHOUSIE UNIVERSITY, HALIFAX, NOVA SCOTIA BH J AND 2BIOLOGICAL OCEANOGRAPHY DIVISION, BEDFORD INSTITUTE OF OCEANOGRAPHY, BOX , DARTMOUTH, NOVA SCOTIA BY A, CANADA
*CORRESPONDING AUTHOR: EMAIL: [email protected]
This study, carried out at a single station in the Bedford Basin (Nova Scotia, Canada), examined time-dependent changes in the physical and chemical conditions of the waters with associated changes in species composition and some photosynthesis properties of phytoplankton. The sampling period covered late summer months (August and September) and fall months (October to December). Changes in the water conditions were found to influence species composition, which in turn had an effect on the shapes and amplitudes of the action and absorption spectra of phytoplankton, and on the maximum quantum yield of photosynthesis. The most remarkable change was observed in October during a bloom of Mesodinium rubrum, a ciliate harbouring photosynthetic endosymbionts rich in phycobilins. The presence of M. rubrum yielded atypical shapes of the measured photosynthetic action spectra; furthermore, other photosynthesis properties changed significantly. These results demonstrate that the presence of certain pigments in the water column may be associated with a marked shift from what may be considered typical (representative) photosynthesis properties of phytoplankton.
INTRODUCTION Shapes of action and absorption spectra have been shown to vary both spatially and temporally. One of the Knowledge of the action and absorption spectra of major causes of variation in action and absorption spectra phytoplankton is important in the estimation of primary is changes in pigment composition, which could imply production using spectrally-resolved photosynthesis–light variation in the phytoplankton population structure models. If ignored, variation in the action spectrum B( ) (Lewis et al., 1986; Hoepffner and Sathyendranath, 1992; B and the phytoplankton absorption spectrum ap ( ) (where Lutz et al., 1996; Schofield et al., 1996). Other factors is the wavelength, and the superscript indicates normal- known to cause variations in the spectra are acclimation ization to phytoplankton biomass B) may cause errors in to light quality or levels (Sakshaug et al., 1991; Johnsen and the computed water-column primary production. For Sakshaug, 1993; Johnsen et al., 1994; Schofield et al., example, a 20% systematic error in B( ) could result in 1996); intracellular pigment concentration or cell size an error of up to 10% in the calculated water-column (Sathyendranath et al., 1987; Sosik and Mitchell, 1994; primary production (Kyewalyanga et al., 1997). The Stuart et al., 1998); and the presence of photosyntheti- action spectrum B( ) is proportional to the biomass- cally-inactive pigments (Sosik and Mitchell, 1995; B specific absorption coefficient of phytoplankton, ap ( ), Lazzara et al., 1996). However, changes in pigment com- with the proportionality factor being equal to the position and/or phytoplankton population structure are maximum quantum yield of photosynthesis m (Platt and influenced by short-term (e.g. days to weeks) or long-term B B Jassby, 1976): ( ) = m( ) ap ( ). That is to say, vari- (seasonal) variations in environmental conditions. B ation in ( ) may be caused by changes in m( ) or in Variations in environmental conditions induce changes B ap ( ), or in both. in phytoplankton populations. However, their effects on
© Oxford University Press 2002 06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 688
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
photosynthetic properties would depend on the type of with a maximum depth of 70 m and a surface area of phytoplankton group(s) present. Phycobiliprotein-con- ~17 km2. The basin is separated from the ocean by a 20 m taining phytoplankton such as cryptomonads and deep sill; the water inside the basin and open-ocean waters cyanobacteria, which have their maximum absorption in move across the sill in response to physical forcing by the green part of the spectrum, have absorption and winds, tides and freshwater runoffs (Platt and Conover, action spectra that differ significantly from what is con- 1971; Platt et al., 1972). sidered to be typical. An example of organisms that show Water samples were collected weekly from four depths unique characteristics is Mesodinium rubrum (= myrionecta (1, 5, 10 and 60 m) at a single station in the middle of the rubra), an autotrophic ciliate that contains endosymbionts Basin from 10 August to 21 December 1994, a total of 20 (cryptomonads) rich in phycoerythrin. Mesodinium rubrum weeks. The water taken from 60 m did not contain any live has been shown to occupy a wide range of environmental phytoplankton, and was therefore excluded from the conditions (Taylor et al., 1971; Crawford, 1989; Satoh and analysis. Data were collected every Wednesday at approxi- Watanabe, 1991; Perriss et al., 1993, 1995; Crawford et al., mately 9.00 a.m. For the determination of absorption 1997). Some of the conditions that have been known to spectra, chlorophyll-a (Chl-a) concentration (by Turner influence the occurrence and abundance of M. rubrum fluorometry), oxygen concentration, pigment composition include increase in temperature and water column (by high performance liquid chromatography, HPLC), stability,which could be caused by heavy precipitation and and concentrations of nutrients (nitrate plus nitrite, sili- run-off (Cloern et al., 1994; Perriss et al., 1995; Crawford cate and phosphate), water was collected at each of the et al., 1997). Another condition is the depletion of three depths using a Niskin bottle. Samples for the action dissolved nitrogen and phosphorus in the photic zone, spectrum and phytoplankton identification were collected since M. rubrum cells can migrate vertically to exploit the only at 5 m. Profiles of temperature, in situ fluorescence (as nutrient pool below the pycnocline (Cloern et al., 1994), a proxy for Chl-a), salinity and photosynthetically avail- and thus out-compete non-motile phytoplankton (such as able radiation (PAR) were determined using a CTD diatoms). probe. Meteorological observations of wind speed and Apart from causing red tides (Barber et al., 1969; Taylor direction, air temperature, rainfall and hours of bright et al., 1971; Crawford, 1989; Crawford et al., 1997) the sunshine were available from Shearwater Airport as daily occurrence of M. rubrum blooms also affects some proper- averages and were obtained from Atmospheric Environ- ties such as the concentration of the main algal pigment, ment Service, Bedford, Nova Scotia. Chlorophyll-a, and the rate of nutrient uptake (Wilkerson The photosynthetic action spectra were determined using and Grunseich, 1990) and primary production (Smith and a spectral incubator, as explained in Kyewalyanga et al. (Kye- Barber, 1979; Laybourn-Parry and Perriss, 1995). walyanga et al., 1997). Water samples were incubated for 3 However, the effect of the presence of M. rubrum on h, under a series of 12 narrow-band (10 nm bandwidth) photosynthesis properties used as inputs in primary pro- irradiances in the range from 400 to 700 nm. At each band, duction models, such as the phytoplankton action spec- 16 bottles (Corning, 70 ml polystyrene culture flasks) were trum, the absorption spectrum and quantum yield, has yet inoculated with 14C and incubated at different light intensi- to be investigated. ties. Another bottle, similarly inoculated, was incubated in In the present study, we examine the effect of changing the dark. To produce the narrow-band light, interference environmental factors and phytoplankton population colour filters (Corion) were used. After incubation, filtration structure on the shapes of action and absorption spectra and fuming to remove unincorporated 14C, counting was of phytoplankton, over a period of five months, in a done using a liquid scintillation counter, and the amount of coastal inlet. In particular, we report on the impact of a 14C fixed was calculated according to Strickland and Mesodinium bloom on the shapes of absorption and action Parsons (Strickland and Parsons, 1972). spectra. The work was carried out at a single station in the Absorption by total particulate materials was deter- Bedford Basin (Nova Scotia, Canada) during late summer mined by using the filter technique (Kishino et al., 1985). to fall 1994. Week-to-week variations in the action spectra, Correction for the pathlength amplification ( factor) was absorption spectra, quantum yield of carbon fixation, made using the method of Hoepffner and Sathyendranath pigment (species) composition and hydrographic con- (Hoepffner and Sathyendranath, 1992), and detrital ditions, are explored. absorption was estimated using the approach of Hoepffner and Sathyendranath (Hoepffner and Sathyendranath, 1993), which assumes an exponential function for the METHOD shape of the detrital absorption spectrum. Fourth deriva- The study was carried out in the Bedford Basin, Nova tive of the absorption spectra (Butler and Hopkins, 1970; Scotia, Canada. Bedford Basin is a small marine inlet, Owens et al., 1987; Bidigare et al., 1989; Millie et al., 1995)
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 689
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
was calculated to resolve absorption maxima of major pig- and September. During this period, the water-column was ments present in each sample. Concentrations of nutrients stratified, with a shallow mixed layer of about 3–5 m. The were determined by a standard automated method using depth of the chlorophyll maximum ranged from 5 to 9 m, an Alpkem autoanalyser, as in Irwin et al. (Irwin et al., 1989). but was frequently at 5 m, and the peak was relatively Pigment composition was determined by HPLC follow- narrow. Salinity was low at 1 m, but increased slightly with ing the method of Head and Horne (Head and Horne, depth below the mixed layer. An example from this group 1993). The samples were kept in a deep freezer (–70°C) and is given in Figures 1a and b, for profiles determined on 17 the analysis was made two years later. Fluorometric determi- August 1994. nation of Chl-a was made the day following sampling, using The second set of the sampling period could be cate- the method of Holm-Hansen et al. (Holm-Hansen et al., gorized as ‘mixed’, and this condition prevailed during the 1965). Both the action and absorption spectra were nor- months of October through December. During this malized to Chl-a determined fluorometrically because it was period, in the fall, the stratification at the surface was more reliable than that determined by HPLC. The com- eroded and the mixed layer extended to between 10 and parison between Chl-a determined by the Turner fluorom- 20 m. There was a layer of low salinity on the top 15 m or eter with that determined by HPLC revealed that the so, and a strong halocline developed between 15 and 25 HPLC-determined Chl-a was lower than that determined m. The Chlorophyll peak was broader than in the first fluorometrically by about a factor of two. This might be a group, and extended from the surface to 10 m or more. consequence of Chl-a degradation; Chl-a might have been Figures 1c and d show the hydrographic conditions for 19 gradually lost during the two-year storage (E. Head, per- October 1994, as an example from this period. In both sonal communication). Therefore, HPLC data were used periods, the photic zone was shallow and did not exceed only for qualitative determination of pigment types. 20 m. Oxygen concentration was measured using an auto- Nutrient concentrations (µg per l) for the entire sam- mated dissolved oxygen titration system (Jones et al., 1992). pling period are shown in Figures 1e to g. Nitrate (plus Samples for microscopic identification of dominant phyto- nitrite, referred to henceforth as nitrate) was very low at 1 plankton groups were collected in the last half of the sam- and 5 m during the stratified period, and then increased pling period (from 19 October to 21 December 1994), sharply during the mixed period (Figure 1e). A similar fixed in Lugol’s solution and identified the following day. trend was observed for silicate, although its concentration Identification of phytoplankton using a microscope was was relatively high in the stratified period (Figure 1f ). not made for samples collected in August, September and Phosphate concentration, on the other hand, was of the first half of October. No cell counting was undertaken. similar magnitude in both periods (Figure 1g), with a The spectrally-averaged maximum quantum yield of notable decrease around day 300 (in October). All nutri- photosynthesis m was estimated as the ratio of the spec- ents reached maximum concentration between late tral mean of the biomass-specific action spectrum, < B>, November and early December (day 327 to 341) then to the spectral mean of the biomass-specific absorption decreased by the second week of December, day 348. The B coefficient of phytoplankton,
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 690
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
Fig. 1. Profiles of temperature, salinity, photosynthetically available radiation (PAR) and Chl-a concentration for two sampling dates in the Bedford Basin: (a and b) 17 August 1994 and (c and d) 19 October 1994. Nutrient concentrations for the whole sampling period are presented as a func- tion of day of the year (1994): (e) nitrate plus nitrite, (f ) silicate and (g) phosphate; in all cases, circles indicate data collected at 1 m, squares joined by lines show data taken from 5 m and triangles indicate data sampled at 10 m.
spectra, but are featureless in the blue–green to yellow (Owens et al., 1987; Bidigare et al., 1989; Millie et al., 1995). region, reflecting the presence of diverse pigments. The fourth-derivative spectra were therefore calculated, Derivative analysis has been shown to be useful in and the results are summarized in Table I. The peaks due separating overlapping absorption bands, as the maxima to Chl-a absorption at around 416, 440, 618 and 676 nm of absorption bands of pigments present in each sample were detectable in all the spectra, although the centre are revealed as peaks in the fourth-derivative spectra wavelengths changed slightly between the sampling dates.
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 691
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
small differences. Silicate concentration was low in (e) 1m August, then it increased in September (Figure 1f), phos-
) 10 -1 5m 8 phate concentration did not differ much in August and 10m September (Figure 1g), although nitrate stayed low (Figure
(ug-at l 6 - 3 1e). Presumably, the change in the water conditions 4
+NO caused a slight change in species composition, which - 2 2 could correspond with changes in cell size and intracellu- NO 0 lar pigment concentration (Coté and Platt, 1983). This in 210 240 270 300 330 360 turn had an effect on the spectral shapes. In August, the Day of the Year (1994) peak in the action spectra in the region between 400 and 500 nm was narrow, with sharp blue peaks at 440 nm whereas the blue peaks in September were broader and
(f) 1m some spectra had shoulders at 460 or 490 nm (compare 5m Figures 2a and b). ) -1 15 10m Although pigment composition was determined by 10 HPLC, it was still difficult to infer the dominant species (ug-at l -4 4 5 from pigment data alone. Microscopic identification was
SiO 0 prompted by the appearance of a brick-red colour on the 210 240 270 300 330 360 filters, during the second week of October. The colour Day of the Year (1994) was caused by a bloom of ciliates identified as M. rubrum (formerly known as Cyclotrichium meunieri Powers, but now also called Myrionecta rubra), containing autotrophic endosymbionts rich in phycoerythrin (Barber et al., 1969; (g) 1m Taylor et al., 1971; White et al., 1977). The endosymbionts 5m ) -1 1.2 10m are cryptomonads that harbour an endosymbiont red alga 0.9 (Richard Pienaar, personal communication). The appear- 0.6 (ug-at l ance of M. rubrum marked a shift in phytoplankton -3 4 0.3 population, perhaps it was caused by a change in environ- PO 0 210 240 270 300 330 360 mental condition. The geographic distribution of Day of the Year (1994) M. rubrum is very wide. Most occurrences have been reported for extreme neritic locations such as inlets, fjords and bays, and also for upwelling systems (reviewed by Fig. 1. Continued. Taylor et al., 1971) and in Antarctica waters (Satoh and Watanabe, 1991; Perriss et al., 1993, 1995; Leakey et al., 1994; Laybourn-Parry and Perriss, 1995). Another common feature of all derivative spectra was the An examination of the meteorological data revealed maximum in the blue region around 465–472 nm, which changes in some of the conditions between the last week could be attributed to absorption by Chl-c, Chl-b and/or of September and the first week of October. Prior to the carotenoids (Bidigare et al., 1989, 1990; Johnsen et al., sampling day in the second week of October, there was an 1992, 1994; Johnsen and Sakshaug, 1993; Hoepffner and increase in wind speed. This could have been responsible Sathyendranath, 1993). The carotenoid peak around 497 for mixing the water column, and extending the mixed nm and the peak of Chl-c or Chl-b absorption in the red layer from 3 to ~15 m (Figures 1a and c), and probably the at about 646 nm (Owens et al., 1987; Bidigare et al., 1990; conditions became favourable for the initiation of the Johnsen et al., 1994) were present in all samples. However, M. rubrum bloom. The Mesodinium rubrum bloom continued the centres of these peaks varied between the sampling throughout October, peaking in the last two weeks. The days (up to 6 nm difference). Most of the differences in the ciliates could still be observed in the samples in November fourth-derivative spectra were found in the blue–green and December, although their concentration decreased region (Table I). with time. The month-to-month variation in the spectral shapes These phycoerythrin-containing cells were responsible was more pronounced in the action spectra (Figure 2) than for the occurrence of the peaks in the green part of the in the absorption spectra (Figure 3), with the most signifi- action spectra in October and November (Figures 2c–d). cant changes being observed in the months of October The presence of Mesodinium cells also affected the shapes and November. August and September showed only some of the absorption spectra, although to a lesser extent than
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 692
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
(a) August (b) September 2.7 2.1
1.8 1.4
0.9 0.7
0 0 400 500 600 700 400 500 600 700
(c) October 2.1
1.4
0.7
0 400 500 600 700
(d) November (e) December 2 2 1.5 1.5 1 1
0.5 0.5
0 0 400 500 600 700 400 500 600 700
WAVELENGTH (nm)
Fig. 2. Shapes of action spectra for five months: (a) August, (b) September, (c) October, (d) November and (e) December, sampled in 1994, in the Bedford Basin. Each spectrum is normalized to its mean value, averaged over the spectral range from 400 to 700 nm.
the shapes of the action spectra. In the absorption spectra, most pigments are present in two or more phytoplankton absorption by phycoerythrin appeared as shoulders in the groups. Since Chlorophyll-a is present in all phyto- green part of the spectra around 543 nm, and shoulders plankton, all pigments were normalized to Chl-a for a at ~497 nm became prominent (Figures 3c–e). Absorp- better comparison of the proportions of pigments tion spectra determined for samples collected at 1 and 10 present. The chlorophylls determined were Chl-a, Chl-b, m also showed features similar to their 5-m counterparts Chl-c3 and Chl-c1 + c2. The carotenoids which were (data not shown). present in significant amount included: fucoxanthin, alloxanthin, peridinin, diadinoxanthin, 19 -hexanoyloxy- Phytoplankton pigments fucoxanthin and zeaxanthin + lutein. The last two pig- The phytoplankton pigments will be discussed without ments co-elute and could not be separated. The ratios of reference to species or groups they represent, because Chlorophylls b, c1 + c2 and c3 to Chl-a are plotted as a
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 693
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
Table I: Centres (nm) of peaks of the fourth-derivative spectra calculated for each absorption spectrum for samples collected from 5 m
Date (1994) Blue peaks (nm) Blue–green peaks (nm) Red peaks (nm)
Aug. 10 416 440 466 495 – 591 618 641 676 Aug. 17 418 441 465 495 – 590 615 641 677 Aug. 24 415 440 467 494 – 593 618 641 677 Aug. 31 416 440 471 496 – 593 617 645 678 Sept. 7 416 441 467 498 548 594 618 646 679 Sept. 14 416 441 469 494 547 593 618 644 679 Sept. 21 416 440 467 494 545 592 618 644 680 Sept. 28 415 441 469 497 545 591 618 643 678 Oct. 5 414 441 469 497 545 589 617 640 676 Oct 12 417 441 472 495 547 587 617 643 676 Oct. 19 415 441 468 499 545 591 616 640 684 Oct. 26 417 441 471 496 542 591 616 645 681 Nov. 2 416 441 472 493 – – 617 647 680 Nov. 9 419 440 469 495 545 591 616 640 684 Nov. 16 416 439 471 495 – – 620 647 679 Nov. 23 417 441 470 500 546 589 – 642 680 Nov. 30 714 440 471 499 – – 621 640 681 Dec. 7 413 441 472 497 548 591 – 642 678 Dec. 14 414 441 469 499 – – 616 637 682 Dec. 21 414 441 469 499 567 588 618 642 680
function of sampling day of the year in Figures 4d–f. The succession. It is unfortunate that phycoerythrin, which is a ratios of carotenoids to Chl-a are also plotted as a func- marker for M. rubrum (and other red algae), was not tion of day of the year (Figures 5a–f ). Because the action detectable by the HPLC technique used; hence we do not spectra were measured only at 5 m, more emphasis is know the actual onset and termination of the M. rubrum given to data representing that depth. Therefore, they are bloom. The relative concentration of Chl-c1 + c2 fluctu- shown as squares and joined by lines to distinguish them ated more or less similarly to that of fucoxanthin and, from those taken at the other depths. interestingly, showed a pattern similar to that of dissolved There was a considerable weekly variation, and depth oxygen concentration (Figures 4b and e). The concen- variation in some cases, in the pigment ratios throughout tration of zeaxanthin + lutein relative to Chl-a remained the sampling period. Significant depth variation was low (ratio below 0.05; Figure 5f ), with an exception of the found in the proportions (relative to Chl-a) of alloxanthin, last weeks in November at 10 m, and 1 and 5 m in the first diadinoxanthin and 19 -hexanoyloxy-fucoxanthin, two weeks of December. notably during the stratified period (Figures 5b, d and e, respectively). The relative concentration of fucoxanthin Physiological parameters was inversely related to that of Chl-b (Figures 4d versus For the entire 20 weeks of data collection, the maximum 5a), while those of Chl-c3 and 19 -hexanoyloxy-fucoxan- quantum yield of photosynthesis, m, ranged from 0.014 thin showed similarity in their distribution patterns and to 0.052, with a mean (± SD) of 0.024 ± 0.008 mol C (mol –1 were present in significant amount only in August and photons) . The average m in the present study is lower September, the stratified period (Figures 4f and 5e). than that found by Taguchi (Taguchi, 1981), with a mean The highest concentrations in fucoxanthin, alloxanthin of 0.054 ± 0.025 mol C (mol photons)–1, during a bloom and peridinin occurred out of phase, two weeks apart: of Ceratium longipes Bailey (between 30 October and 20 fucoxanthin peaked first (at day 278), followed by alloxan- November 1974) in the Bedford Basin. Although the sam- thin (at day 292), and lastly peridinin (at day 306; Figures pling season for this and Taguchi’s study was the same 5a, b and c, respectively), which could imply species (fall), the difference in the values of m emphasizes the
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 694
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
2.7 (a) August (b) September 2.7
1.8 1.8
0.9 0.9
0 0 400 500 600 700 400 500 600 700
(c) October 2.7
1.8
0.9
0 400 500 600 700
(d) November (e) December 2.7 2.7 1.8 1.8 0.9 0.9 0 0 400 500 600 700 400 500 600 700
WAVELENGTH (nm)
Fig. 3. As in Figure 2, but for the corresponding absorption spectra.
effect of changing phytoplankton population (Ceratium (Equation 1), the pattern observed in Figures 6a–c B versus Mesodinium blooms) on the photosynthesis proper- suggests that changes in
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 695
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
Fig. 4. Time-series variation for data collected from the Bedford Basin between 10 August and 21 December 1994. (a) chlorophyll-a (Chl-a) concen- tration, (b) concentration of dissolved oxygen, (c) water temperature, (d) the ratio of chlorophyll-b (Chl-b) to Chl-a,(e) ratio of Chl-c1 + c2 to Chl- a and (f) the ratio of Chl-c3 to Chl-a. The symbols are as defined in Figure 1.
0.012 to 0.07, a factor of about six, with a mean value of showed variation with time, with the greatest change 2 –1 B 0.039 ± 0.016 m (mg Chl-a) ; the corresponding ap (676) being observed in October; both the maximum (2.2) and ranged from 0.007 to 0.034, averaging 0.019 ± 0.007 m2 the minimum (0.3) values occurred in this month (Figure (mg Chl-a)–1. 7c). Overall, the ratios were above 1.0 except for the two In general, the amplitudes of the spectra were higher weeks in October during the bloom of M. rubrum.The during the stratified period than in the mixed one. The values of B at 440 nm were lower than expected because pattern in the peak values at the blue and red wavelengths, of the imbalance in Chl-a distribution between photo- B B for both and ap , resembled that of the corresponding systems I and II, the effect of which became prominent in mean values of the spectra (compare Figures 6b and c the unenhanced action spectra measured here, in the pres- with 7a and b). The blue-to-red absorption ratio, ap(440): ence of M. rubrum. ap(676), did not change significantly over the sampling time, although it was slightly lower in October than in DISCUSSION AND CONCLUSION September and November (Figure 7c). It ranged from 1.7 to 2.3, which is within the range reported for healthy The changes in the shapes and amplitudes of the action and phytoplankton [1.1 to 2.5; reviewed by (Cleveland et al., absorption spectra from month to month could be related 1989)]. The ratio B(440): B(670), on the other hand, to changes in the water conditions and phytoplankton
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 696
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
Fig. 5. Time-series variation in the ratios of carotenoids to Chl-a for samples collected from 10 August to 21 December 1994 in the Bedford Basin. (a) fucoxanthin (fuco), (b) alloxanthin (allo), (c) peridinin (perid), (d) diadinoxanthin (diadi), (e) 19 -hexanoyloxy-fucoxanthin (19 hexa) and (f ) zeazanthin + lutein (ze+lut). The symbols are as defined in Figure 1.
species composition. In the months of August and Sep- size or low intracellular pigment concentration (Duysens, tember, the water-column was stratified. In general, the 1956; Morel and Bricaud, 1981; Sathyendranath et al., spectra showed a maximum in the blue part of the spec- 1987). trum, a minimum in the green part, and another peak in The phytoplankton assemblages were dominated by the red region around 676 nm (Figures 2a, 2b, 3a and 3b). cells with high proportions of Chl-c3 and 19 -hexanoy- During this period, the water temperature was high loxy-fucoxanthin (Figures 4f and 5e), but low alloxanthin (Figure 4c), nitrate concentration was low and Chl-a and peridinin (Figures 5b and c). Fucoxanthin and Chl-c1 concentration was moderate in the mixed layer (Figures 1e + c2 were relatively high in August when the wind was low and 4a). The samples in this stratified group were charac- and rainfall was high, but decreased in September with B B terized by high values of (440) and ap (440) (Figures 7a increasing winds (Figures 4e and 5a). The reverse situation and b), which could imply the presence of populations was seen for the proportion of Chl-b in the two months with low package effect, that is, a community of small cell (Figure 4d).
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 697
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
(a) (a) 440 nm 0.08 670 nm 0.06 0.06 0.04 0.04 0.02 Maximum 0.02
Quantum Yield 0 210 240 270 300 330 360 Initial Slopes 0 Day of the Year (1994) 210 240 270 300 330 360
(b) (b) 440 nm 670 nm 0.08 0.036 0.027 0.06 0.018 0.04 0.009 0.02 Mean Initial Slope 210 240 270 300 330 360 0 Day of the Year (1994) Specific Absorption 210 240 270 300 330 360
(c) (c) alpha 0.036 Absorption 3 0.027 2.5 0.018 2 1.5 0.009 Absorption 1 Mean Specific 0 0.5
210 240 270 300 330 360 Ratio (blue:red) 0 Day of the Year (1994) 210 240 270 300 330 360
Fig. 6. Time-series variation in data collected at 5 m from the Bedford Basin between 10 August and 21 December 1994. (a) The Maximum DAY OF THE YEAR (1994) –1 quantum yield of carbon fixation [mol C (mol photons) ], (b) the Fig. 7. Time-series variation in the amplitudes of the (a) action (b) B –1 –1 average value of the action spectra ( ) [mg C (mg Chl-a) h (µmol absorption spectra for values at the blue peaks (circles) and at the red –2 –1 –1 m s ) ] and (c) the mean value of the biomass-specific absorption peaks (squares), for data collected at 5 m in the Bedford Basin. (c) Ratios B 2 –1 coefficients, ap ( ) [m (mg Chl-a) ]. of blue-to-red values of the action spectra [ B(440): B(670); diamonds] and absorption spectra [ap(440):ap(676); squares].
The most distinct features in the absorption spectra for August and September were the blue and red peaks due (characteristic of M. rubrum when filtered), indicating that, primarily to Chl-a absorption, and the shoulders in the if present, then they were in low concentration. The blue region due to absorption by other chlorophylls and difference between the peaks in the blue–green region for carotenoids. The peaks of the fourth-derivative spectra August and September samples could be attributed to (Table I) for samples collected in August and September changes in species composition, given also that fucoxan- were similar, except that the samples from August lacked thin and Chl-b were inversely correlated. an absorption peak at about 545–548 nm in the For the months of October, November and December, blue–green region. This peak, presumably due to phyco- that is, during the mixed period, microscopic analysis erythrin absorption (Barber et al., 1969; White et al., 1977; showed that phytoplankton community was dominated by Bidigare et al., 1989, 1990), was present in the September big cells (autotrophic ciliates, diatoms and dinoflagellates), samples although the amplitude was low. The peak for although small cells were also present. Nitrate and silicate phycoerythrin absorption observed for September concentrations started to increase in October but the samples could suggest that M. rubrum cells (or other phy- concentration of phosphate was relatively low during this coerythrin-containing micro-algae) were present in the month. The most significant change in the shapes of the water. However, no red colouration of filters was seen spectra, especially the action spectra, was found in
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 698
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
October and was associated with the bloom of M. rubrum, measured here (Emerson, 1957; Schofield et al., 1990, a phycoerythrin-rich photosynthetic ciliate. The magni- 1996). tudes of the blue peaks (at 440 nm) for both the action and In phycobilin-rich algae like M. rubrum, almost all the absorption spectra were lower during this time than in any accessory pigments are associated with PSII whereas most other month (Figures 7a and b). This could be attributed of Chl-a is associated with PSI (Kirk, 1983; Neori et al., to the package effect since M. rubrum cells are relatively 1986; Prézelin and Boczar, 1986). Since PSI is unable to large (cell volume could reach 3.25 104 µm3, depending transfer its excess excitation energy to PSII, a decrease in on the season of the year) (Montagnes and Lynn, 1989) the photosynthetic efficiency at the wavelengths at which with numerous chloroplasts (Taylor et al., 1971; Lindholm, Chl-a absorb could have occurred, resulting in a deviation 1985; Lindholm et al., 1988). in the shape of the spectrum from that of a typical action Although the absorption peak due to phycoerythrin spectrum, as observed here. However, this type of bias started to appear in September (Table I, column six), it could be eliminated by estimating the photosynthetic became more prominent in October during the bloom of action spectrum from the shape of phytoplankton absorp- M. rubrum. Mixing brought deep nitrate-rich waters to the tion spectrum and the magnitude of the broad-band B surface, replenishing the surface waters depleted of nutri- (Kyewalyanga et al., 1997). ents due to summer stratification. During this period also, In the absorption spectra, shoulders were present in the the rainfall was heavy and the wind speed was high. In blue–green and green region, a consequence of absorp- contrast, for a temperate estuary during spring, Cloern et tion by phycoerythrin (Barber et al., 1969; Shimura and al. (Cloern et al., 1994) found that the prerequisite for a Fujita, 1975; Lewis et al., 1988). However, the shoulders bloom of M. rubrum to occur was heavy precipitation and were not as prominent as might have been expected from run-off that caused salinity stratification. Furthermore, the action spectra. A possible explanation for the reduced the photic-zone was depleted of inorganic nitrogen and amplitude of the peak due to phycoerythrin absorption phosphate. The authors also found other prerequisites to during the bloom period in October (Figure 8) is the possi- be the occurrence of a spring diatom bloom and several bility that some of the water-soluble pigment, phycoery- days of warming and stabilization in the upper surface thrin, was lost during the filtration process. Mesodinium layer. On the other hand, blooms of M. rubrum have been rubrum is extremely fragile and ruptures easily when sub- shown to occur under low temperatures (–1.6°C), low jected to pressure or exposure to preservatives like forma- salinity (7 ppt) and high nutrient concentrations (Satoh lin (Barber et al., 1969; White et al., 1977; Smith and and Watanabe, 1991). Because of its high swimming Barber, 1979). When cells burst during filtration, the red speed [2–7 m h–1 (Smith and Barber, 1979; Barber and pigment has been shown to move away from the centre to Smith, 1981)], the ciliate is capable of rapid vertical the edge of the filter (Smith and Barber, 1979). This migration to the nutrient-rich deep waters to satisfy its phenomenon was observed during filtration in the present nutrient requirements (Satoh and Watanabe, 1991). study, implying that there was some loss of phycoerythrin. These studies suggest that M. rubrum can adapt to a wide Barber et al. (Barber et al., 1969) compared absorption range of environmental conditions. spectra of M. rubrum before and after washing in distilled The presence of M. rubrum does not only cause dis- water (their Figure 1); they showed that a phycoerythrin colouration of the water (red tide, due to phycoerythrin) peak present in the spectrum of the unwashed sample was but could also result in a significant change in the photo- reduced to a shoulder in the spectrum of the washed one. synthetic properties. A typical action spectrum has a The authors thus demonstrated how easily phycoerythrin maximum (peak) in the blue part of the spectrum at could be lost during filtration. Indeed, the shapes of our around 440 nm, a minimum (valley) in the green to yellow absorption spectra for October (Figure 3c) resemble their region, and a minor peak in the red at ~675 nm. Contrary spectrum for the washed cells. to this, at the time of the M. rubrum bloom in the last two Another noticeable feature of the shapes of absorption weeks of October, the spectra had peaks in the green spectra was a shoulder between about 600 and 650 nm region, which were higher than the blue and red peaks (Figures 3c–e), which was not prominent in the first two (Figure 2c). The low values of B(440) and B(670) could months. The shoulders were well resolved in the fourth- be attributed to an imbalance in the distribution of Chl-a derivative spectra, and were present in all samples (Table between photosystem I (PSI) and photosystem II (PSII), I). They became prominent only in early October, which can be acute in biliprotein-containing algae such as perhaps due to the presence of M. rubrum, which is rich in cryptomonads and cyanobacteria (Lüning and Dring, Chl-c (Barber et al., 1969; White et al., 1977). However, 1985; Neori et al., 1986, 1988; Lewis et al., 1986, 1988; contribution to the shoulders by absorption from other Prézelin and Boczar, 1986). The effect of such an imbal- pigments, such as Chl-b, is also possible. Figure 8 shows, ance would be evident in the un-enhanced action spectra as an example, the fourth derivative of the absorption
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 699
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
different phytoplankton: the dominant ones included 684
1.00E-05 441 Chaetoceros, Nitzschia, Ceratium, Gonyaulax, silicoflagellates 468
499 and other small cells. Mesodinium rubrum was present, but
5.00E-06 415 669 640 545 591 616 in less abundance than in October and November. 0.00E+00 400 450 500 550 600 650 700 The associated pigment composition and hydrographic -5.00E-06 conditions showed that Chl-a concentration was high
-1.00E-05 during the Mesodinium bloom, but it decreased and stayed 4th derivative low, whereas dissolved oxygen concentration showed the -1.50E-05 opposite pattern (Figures 4a and b), and the water tem- -2.00E-05 perature progressively decreased slightly with time, but stayed uniform with depth (Figure 4c). The proportion of fucoxanthin was low during the October bloom, although 0.3 it increased as M. rubrum decreased (Figure 5a). Alloxan- thin increased during the bloom, then decreased slightly
) 0.25 -1 after it, but stayed high for the remaining time of the sam- 0.2 pling period (except on the last week; Figure 5b). Alloxan- 0.15 thin is a pigment marker for cryptophytes. Therefore, the
0.1 increase in alloxanthin could be related to the presence of cryptomonad endosymbionts in M. rubrum. Peridinin was Absorption (m 0.05 relatively low, but increased strongly in November when 0 dinoflagellates were dominant (Figure 5c). Unlike in the 400 450 500 550 600 650 700 stratified period, the proportions of Chl-c3 and 19 -hexa- noyloxy-fucoxanthin were undetectable during this period WAVELENGTH (nm) (Figures 4f and 5e). Fig. 8. Fourth-derivative spectrum (top panel) showing peaks of In summary, the study conducted here showed that absorption maxima for different pigments present in the sample col- between late summer and fall 1994, in the Bedford Basin, lected from 5 m on 19 October 1994 (bottom panel). The approxi- mate positions of the peaks and shoulders corresponding to the peaks the hydrographic conditions controlled species composi- in the fourth-derivative spectrum are indicated by arrows. The con- tion and, in turn, changes in pigment composition tributing pigments are discussed in the text, but note the peak for phy- affected the shapes and amplitudes of both the action and coerythrin absorption at ~545 nm. absorption spectra. For the first two months (August and September), the water column was stratified, temperature and salinity were high but nitrate concentration was low spectrum for the sample collected on 19 October 1994. (at 5 m). This period was associated with cells rich in Chl- The maxima in the spectra are associated with (top panel) c3 and 19 -hexanoyloxy-fucoxanthin but generally poor in the peaks and shoulders (corresponding to the arrows in Chl-c1 + c2, alloxanthin and peridinin. The spectral shapes the bottom panel) due to absorption by major pigments. had no particular features in the blue–green, green or The peak for phycoerythrin absorption is centred at yellow regions of the spectrum. The samples had rela- ~545 nm. tively high values of B( ) and specific absorption co- Major phytoplankton groups/species during the mixed efficients, which could imply that the phytoplankton com- period were as follows: in October, the dominant phyto- munity was dominated by small cells. plankters were M. rubrum, microflagellates, diatoms and In the following three months (October, November and silicoflagellates. In November, a month with the highest December), the water column in the top 15 m was well wind speed and nutrient concentrations, dinoflagellates mixed. This period was associated with relatively low (mostly Ceratium, Gonyaulax and Dinophysis) were the most salinity and temperature but high nutrient concentrations. abundant, followed by diatoms and photosynthetic cili- The samples were dominated by large phytoplankton ates. Taguchi (Taguchi, 1981) also found the dinoflagel- cells; thus the B( ) and specific absorption coefficients late, Ceratium longipes (Bailey) Gran, to bloom from late were lower than in the stratified period, probably due to October to November in the Bedford Basin. Diatoms, on the package effect. Likewise, pigment composition and the the other hand, are known to become dominant in spring. shapes of the action and absorption spectra were different In a study carried out during a spring bloom, in the from those of the stratified case. In general, the spectra Bedford Basin, it was dominated by diatoms (Smith et al., became relatively broad in the blue part of the spectrum, 1983). The bloom was preceded by that of dinoflagellates and peaks or shoulders were observed in the green and and other flagellates. In December, there was a mixture of yellow region, reflecting changes in pigment composition.
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 700
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
The samples from the mixed period were rich in phyco- Cloern, J. E., Cole, B. E. and Hager, S. W. (1994) Notes on Mesodinium rubrum red tides in San Francisco Bay (California, USA). J. Plankton erythrin, alloxanthin and peridinin, but poor in Chl-c3 and 19 -hexanoyloxy-fucoxanthin. Res., 16, 1269–1276. Overall, the results obtained here showed strong differ- Côté, B. and Platt, T.(1983) Day-to-day variations in the spring-summer photosynthetic parameters of coastal marine phytoplankton. Limnol ences in the shapes and magnitudes of the photosynthesis Oceanogr., 28, 320–344. properties between the two periods sampled. There was a Crawford, D. W.(1989) Mesodinium rubrum: the phytoplankter that wasn’t. clear distinction in the properties between the two seasons, Mar. Ecol. Pro. Ser., 58, 161–174. summer (the stratified period) and fall (the mixed period), Crawford, D. W., Purdie, D. A., Lockwood, A. P. M. and Weissman, P. which was attributable to changes in pigment (species) com- (1997) Recurrent red-tides in the Southampton water estuary caused position. The most significant change in the m values, and by the phototrophic ciliate Mesodinium rubrum. Estuarine, Coastal Shelf in the shapes and amplitudes of both the action and absorp- Sci. 45, 799–812. tion spectra was observed in October when the bloom of Duysens, L. N. M. (1956) The flattening of the absorption spectrum of sus- the phycoerythrin-rich M. rubrum occurred. These results pensions, as compared to that of solutions. Biochim Biophys Acta, 19, 1–12. suggest that the presence of M. rubrum, like that of any Emerson, R. (1957) Dependence of yield of photosynthesis in long-wave biliprotein-containing phytoplankton (such as cyanobac- red and on wavelength and intensity of supplementary light. Science, 123, 746. teria) could have a significant effect on the photosynthetic properties of phytoplankton, especially the unenhanced Head, E. J. H. and Horne, E. P. W. (1993) Pigment transformation and vertical flux in an area of convergence in the North Atlantic. Deep-Sea action spectrum. This is mainly caused by the imbalance of Res., 40, 329–346. Chl-a distribution between photosystems I and II. Hoepffner, N. and Sathyendranath, S. (1991) Effect of pigment compo- sition on absorption properties of phytoplankton. Mar. Ecol. Prog. Ser., 73, 11–23. ACKNOWLEDGEMENTS Hoepffner, N. and Sathyendranath, S. (1992) Bio-optical characteristics We thank Brian Irwin and Jeff Anning for helping with of coastal waters: Absorption spectra of phytoplankton and pigment distribution in the western North Atlantic. Limnol. Oceanogr., 37, the design and construction of the spectral incubator; 1660–1679. Gilberto Gaxiola and Paul Dickie for helping with field Hoepffner, N. and Sathyendranath, S. (1993) Determination of the sampling and nutrient measurements; and Heidi Maass major groups of phytoplankton pigments from the absorption spectra for help with the calculation of the fourth-derivatives. The of total particulate matter. J. Geophys Res., 98, 22789–22803. work presented here was supported by the Office of Naval Holm-Hansen, O., Lorenzen, C. J., Holmes, R. W. and Strickland, J. D. Research, the National Aeronautics and Space Adminis- H. (1965) Fluorometric determination of chlorophyll. J. cons. (cons) int. tration, the Department of Fisheries and Oceans, and the Explor. Mer., 30, 3–15. Natural Sciences and Engineering Research Council Irwin, B., Caverhill, C., Anning, J., Macdonald, A., Hodgson, M., through research grant to S.S and T.P. Horne, E. P. W. and Platt, T. (1989) Productivity localized around seamounts in the Atlantic (PLASMA) during June and July 1987. Can. Data Rep. Fish. Aquat. Sci., 732, iv + 227pp. Johnsen, G. and Sakshaug, E. (1993) Bio-optical characteristics and REFERENCES photoadaptive responses in the toxic and bloom-forming dinoflagel- Barber, R. T. and Smith, W. O. (1981) The role of circulation, sinking lates Gyrodinium aureolum, Gymnodinium galatheanum and two strains of and vertical migration in physical sorting of phytoplankton in the Prorocentrum minimum. J. Phycol., 29, 627–642. upwelling centre at 15C. In Richards, F. A. (ed.), Coastal Upwelling: Johnsen, G., Sakshaug, E. and Vernet, M. (1992) Pigment composition, Coastal and Estuarine Sciences 1. Geophysical Monography Bd, Washing- spectral characterization and photosynthetic parameters in Chrysochro- ton DC, pp. 366–371. mulina polylepsis. Mar. Ecol. Prog. Ser., 83, 241–249. Barber, R. T., White, A. W. and Siegelman, H. W. (1969) Evidence for a Johnsen, G., Nelson, N. B., Jovine, R. V. and Prézelin, B. B. (1994) cryptomonad symbiont in the ciliate, Cyclotrichium meunieri. J. Phycol., 5, Chromoprotein- and pigment-dependent modeling of spectral light 86–88. absorption in two dinoflagellates, Prorocentrum minimum and Heterocapsa Bidigare, R. R., Morrow, J. H. and Kiefer, D. A. (1989) Derivative analy- pygmaea. Mar. Ecol. Prog. Ser., 114, 245–258. sis of spectral absorption by photosynthetic pigments in the western Jones, E. P.,Zemlyak, F. and Steward, P.(1992) Dissolved Oxygen Titra- Sargasso Sea. J. Mar. Res., 47, 323–341. tion System. Can. Tech. Rep. of Hydrography and Ocean Sci. 138, iv + 51pp. Bidigare, R. R., Ondrusek, M. E., Morrow, J. H. and Kiefer, D. A. (1990) Kirk, J. T.O. (ed.) (1983) Light and Photosynthesis in Aquatic Ecosystems. Cam- In vivo absorption properties of algal pigments. Ocean Optics, 1302, bridge University Press, Cambridge. 290–302. Kishino, M., Takahashi, M., Okami, N. and Ichimura, S. (1985) Esti- Butler, W. L. and Hopkins, D. W. (1970) An analysis of fourth derivative mation of the spectral absorption coefficients of phytoplankton in the spectra. Photochem. Photobiol., 12, 451–456. sea. Bull. Mar. Sci., 37, 634–642. Cleveland, J. S., Perry, M. J., Kiefer, D. A. and Talbot, M. C. (1989) Kyewalyanga, M., Platt, T. and Sathyendranath, S. (1997) Estimation of Maximal quantum yield of photosynthesis in the northwestern Sar- the photosynthetic action spectrum: implication for primary produc- gasso Sea. J. Mar. Res., 47, 869–886. tion models. Mar. Ecol. Prog. Ser., 146, 207–223.
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 701
M. KYEWALYANGA, S. SATHYENDRANATH AND T. PLATT EFFECT OF M. RUBRUM ON PHYTOPLANKTON SPECTRA
Laybourn-Parry, J. and Periss, S. J. (1995) The role and distribution of Platt, T. and Jassby, A. D. (1976) The relationship between photosyn- the autotrophic ciliate Mesodinium rubrum (Myrionecta rubra) in three thesis and light for natural assemblages of coastal marine phyto- Antarctic saline lakes. Arch. Hydrobiol., 135, 179–194. plankton. J. Phycol., 12, 421–430. Lazzara, L., Bricaud, A. and Claustre, H. (1996) Spectral absorption and Platt, T., Prakash, A. and Irwin, B. (1972) Phytoplankton nutrients and fluorescence excitation properties of phytoplanktonic populations at a flushing of inlets on the coast of Nova Scotia. Naturaliste Can., 99, mesotrophic and an oligotrophic site in the tropical North Atlantic 253–261. (EUMELI program). Deep Sea Res., 43, 1215–1240. Prézelin, B. B. and Boczar, B. A. (1986) Molecular bases of cell absorp- Leakey, R. J. G., Fenton, N. and Clarke, A. (1994) The annual cycle of tion and fluorescence in phytoplankton: potential application to planktonic ciliates in nearshore waters at Signy Island, Antarctica. J. studies in optical oceanography. Prog. Phycol. Res., 4, 350–464. Plankton Res., 16, 841–856. Sakshaug, E., Johnsen, G., Andresen, K. and Vernet, M. (1991) Model- Lewis, M. R., Warnock, R. E. and Platt, T. (1986) Photosynthetic ing of light-dependent algal photosynthesis and growth: experiments response of marine picoplankton at low photon flux. In: Platt, T. and with the Barents Sea diatoms Thalassiosira nordenskioeldii and Chaetoceros Li, W. K. W. (eds) Photosynthetic Picoplankton. Can Bull Fish Aquat Sci, furcellatus. Deep Sea Res., 38, 415–430. Ottawa, pp. 235–250. Sathyendranath, S., Lazzara, L. and Prieur, L. (1987) Variations in the Lewis, M. R., Ulloa, O. and Platt, T. (1988) Photosynthetic action, spectral values of specific absorption of phytoplankton. Limnol. absorption, and quantum yield spectra for a natural population of Oceanogr., 32, 403–415. Oscillatoria in the North Atlantic. Limnol. Oceanogr., 33, 92–98. Satoh, H. and Watanabe, K. (1991) A red water-bloom caused by Lindholm, T.(1985) Mesodinium rubrum—a unique photosynthetic ciliate. autotrophic ciliate: Mesodinium rubrum, in the austral summer in the fast Ad. Aquat. Microbiol., 3, 1–48. ice area near Syowa station, Antarctica, with note on their photosyn- Lindholm, T., Lindroos, P.and Mörk, A.-C. (1988) Ultrastructure of the thetic rate. J. Tokyo Univ. Fish., 78, 11–17. photosynthetic ciliate Mesodinium rubrum. BioSystems, 21, 141–149. Schofield, O., Bidigare, R. R. and Prézelin, B. B. (1990) Spectral photo- Lüning, K. and Dring, M. J. (1985) Action spectra and spectral quantum synthesis, quantum yield and blue-green light enhancement of yield of photosynthesis in marine macroalgae with thin and thick productivity rates in the diatom Chaetoceros gracile and the prymnesio- thalli. Mar. Biol., 87, 119–129. phyte Emiliania huxleyi. Mar. Ecol. Prog. Ser., 64, 175–186. Lutz, V. A., Sathyendranath, S. and Head, E. J. H. (1996) Absorption Schofield, O., Prézelin, B. and Johnsen, G. (1996) Wavelength depen- coefficient of phytoplankton: regional variations in the North dency of the maximum quantum yield of carbon fixation for two red Atlantic. Mar. Ecol. Prog. Ser., 135, 197–213. tide dinoflagellates, Heterocapsa pygmea and Prorocentrum minimum (Pyrro- phyta): implications for measuring photosynthetic rates. J. Phycol., 32, Millie, D. F., Kirkpatrick, G. J. and Vinyard, B. T.(1995) Relating photo- 574–583. synthetic pigments and in vivo optical density spectra to irradiance for the Florida red-tide dinoflagellate Gymnodinium breve. Mar. Ecol. Prog. Shimura, S. and Fujita, Y. (1975) Changes in the activity of fucoxan- Ser., 120, 65–75. thin-excited photosynthesis in the marine diatom Phaeodactylum tricor- nutum grown under different culture conditions. Mar. Biol., 33, Montagnes, D. J. S. and Lynn, D. H. (1989) The annual cycle of Meso- 185–194. dinium rubrum in the waters surrounding the Isles of Shoals, Gulf of Maine. J. Plankton Res., 11, 193–201. Smith Jr., W. O. and Barber, R. T. (1979) A carbon budget for the autotrophic ciliate Mesodinium rubrum. J. Phycol., 15, 27–33. Morel, A. and Bricaud, A. (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorp- Smith, J. C., Platt, T. and Harrison, W. G. (1983) Photoadaptation of tion of phytoplankton. Deep Sea Res., 28A, 1375–1393. carboxylating enzymes and photosynthesis during a spring bloom. Prog. Oceanogr., 12, 425–459. Neori, A., Vernet, M., Holm-Hansen, O. and Haxo, F. T. (1986) Relationship between action spectra for chlorophyll a fluorescence Sosik, H. and Mitchell, B. G. (1994) Effect of temperature on growth, light absorption, and quantum yield in Dunaliella tertiolecta (Chloro- and photosynthetic O2 evolution in algae. J. Plankton Res., 8, 537–548. phyceae). J. Phycol., 30, 833–840. Neori, A., Vernet, M., Holm-Hansen, O. and Haxo, F. T. (1988) Com- Sosik, H. M. and Mitchell, B. G. (1995) Light absorption by phyto- parison of chlorophyll far-red and red fluorescence excitation spectra plankton, photosynthetic pigments and detritus in the California with photosynthetic oxygen action spectra for photosystem II in algae. Current System. Deep-Sea Res., 42, 1717–1748. Mar. Ecol. Prog. Ser., 44, 297–302. Strickland, J. D. H. and Parsons, T.J. (1972) A practical handbook of sea- Owens, T. G., Gallagher, J. C. and Alberte, R. S. (1987) Photosynthetic water analysis. Bull. Fish. Res. Board Can, 167 311p. light-harvesting function of violaxanthin in Nannochloropsis spp. Stuart, V., Sathyendranath, S., Platt, T., Maass, H. and Irwin, B. (1998) (Eustigmatophyceae). J. Phycol., 23, 79–85. Pigments and species composition of natural phytoplankton popu- Perriss, S. J., Laybourn-Parry, J. and Marchant, H. J. (1993) Mesodinium lations: effect on the absorption spectra. J. Plankton Res., 20, rubrum (Myrionecta rubra) in an Antactic brackish lake. Arch. Hydrobiol., 187–217. 128, 57–64. Taguchi, S. (1981) Seasonal studies of the dinoflagellate Ceratium longipes Perriss, S. J., Laybourn-Parry, J. and Marchant, H. J. (1995) Wide- (Bailey) Gran in the Bedford Basin, Canada. J. Exp. Mar. Biol. Ecol., 55, spread occurrence of populations of the unique autotrophic ciliate 115–131. Mesodinium rubrum (Ciliophora: Haptorida) in brackish and saline Taylor, F. J. R., Blackbourn, D. J. and Blackbourn, J. (1971) The red- lakes of the Vestfold Hills (eastern Antarctica). Polar Biol., 15, water ciliate Mesodinium rubrum and its ‘incomplete symbionts’: a 423–428. review including new ultrastructral observations. J. Fish. Res. Board Platt, T. and Conover, R. J. (1971) Variability and its effect on the 24h Can., 28, 391–407. chlorophyll budget of a small marine basin. Mar. Biol., 10, 52–65. White, A. W.,Sheath, R. G. and Hellebust, J. A. (1977) A red tide caused
06kyewalyanga 82W(ds) 2/7/02 8:50 am Page 702
JOURNAL OF PLANKTON RESEARCH VOLUME NUMBER PAGES ‒
by the marine ciliate Mesodinium rubrum in Passamaquoddy Bay,includ- symbiotic ciliate Mesodinium rubrum: the significance of nitrogen ing pigment and ultra-structure studies of the endosymbiont. J. Fish. uptake. J. Plankton Res., 12, 973–989. Res. Board Can., 34, 413–416. Wilkerson, F. P. and Grunseich, G. (1990) Formation of blooms by the Received on April 17, 2001; accepted on April 3, 2002