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Studies on phytoplankton distribution and primary production in the western English Channel in 1980 and 1981
ContinentalShelfResearch,Vol.3, No. 1, pp. 25 to 34, 1984. Printedin Great Britain.
0278--4343/84 $3.00 + 0.00 O 1984 PergamonPressLtd.
Studies on phytoplankton distribution and primary production in the western English Channel in 1980 and 1981 M. B. JORDAN* and I. R. JOINT* (Received 17 May 1983; in revisedform 16 August 1983; accepted 23 August 1983) Abstract--The distribution of chlorophyll on a transect of the English Channel was measured during 1980 and 1981. In both years, high concentrations of chlorophyll a were measured in midchannel in July and August and this was due to a bloom of Gyrodinium aureolum. At a near-shore station close to Plymouth, regular measurements of water transparency and primary production were made during 1981. Values of diffuse attenuation coefficient increased in the spring with increasing chlorophyll concentration; this was followed by a period o f low attenuation coefficients when chlorophyll maxima developed on the thermocline. The attenuation coefficient was greatly increased in late summer as the result o f a bloom of G. aureolum. The high cell density resulted in self-limitation and specific rates of photosynthetic carbon fixation were low during the bloom. The total water-column light utilization index (~) is calculated to be 0.48 g C g Chl a -~ E -mm -2 and the possible use of this index to calculate production from depth-integrated chlorophyll a concentrations is discussed.
INTRODUCTION
THE WESTERNEnglish Channel has been the subject of study since the turn of the century but it is relatively recently that the phytoplankton of the region has been studied. BOALCnet al. (1978) and MADDOCKet al. (1981) described the phytoplankton production of the region between 1964 and 1974 but an important development was the work of PINGREEet al. (1975, 1976, 1977), who related phytoplankton distribution to the differing physical stabilities encountered in the region and demonstrated the importance of frontal boundaries as sites of phytoplankton blooms. Hydrographic conditions across the English Channel in summer vary from stratified near the English coast, through a transitional region to the frontal boundary in the centre of the Channel and then to vertically well-mixed water near the French coast (PINGREE, 1978). The hydrographic conditions, and particularly the vertical stability of the water column, appear to play an important role in the development of dense blooms of dinoflagellates in this region (HOLLIGANand HARBOUR,1977; HOLLIGANet al., 1980). The western English Channel has also been sampled at monthly intervals since 1974 as a standard route of the Continuous Plankton Recorder Survey (CPR) (GLOVES, 1967) and in addition, since 1979, temperature, salinity, and chlorophyll fluorescence have been sampled by the Undulating Oceanographic Recorder (UOR), as described by AIKEN(1981). The UOR automatically records the measured parameters as the recorder undulates between the surface and a depth which depends on the towing cable length; information is therefore obtained in * Natural Environment Research Council, Institute for Marine Environmental Research, Prospect Place, The Hoe, Plymouth Pl I 3DH, U.K. 25
26
M.B. JORDANand I. R. JOINT
both horizontal and vertical planes. AIKEN (1981) showed the structure of temperature and chlorophyll measured by two UOR tows in a transect across the English Channel in August 1979. The purposes of this study were twofold; firstly to obtain data on the seasonal abundance of chlorophyll using standard sampling protocols which could be used as confirmation of the data obtained with the UOR and secondly to study the seasonal changes in water transparency and how this was related to phytoplankton production. METHODS The study area is shown in Fig. 1 ; 11 stations were placed equidistant on the line between Plymouth and Roscoff. This transect is the standard route samplcxl by the CPR and more recently by the U O R (G. A. ROSINSON, personal communication). Preliminary measurements began in 1980 and Stas 1 to 6 were sampled nine times between March and September. In 198 l, all 11 stations were sampled in March and July and an intensive study was made at Sta. l (50 ° 15.00'N, 04 o 09.00'W), which was sampled 13 times between March and August 1981. At each station, salinity and temperature were measured with a Braystoke inductive salinometer. Water samples were taken at 5 m depth intervals using N I O water bottles; subsamples of this water were used for primary production estimation and the remainder was
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Studies on phytoplanktondistributionand primaryproduction
27
filtered through glass-fibre GF/C filters, quickly frozen on dry-ice and analysed for photosynthetic pigment content on return to the laboratory. The filters were extracted with 90% v/v acetone and the extracted pigments were measured in a 4 cm path-length cell in a Pye-Unicam SP8000 recording spectrophotometer; the concentrations of chlorophyll a and phaeopigments were calculated using the equations of STRICKLAND and PARSONS (1972). During 1981, water samples were also preserved with 1% Lugol's Iodine for subsequent identification and enumeration of phytoplankton. In 1981, primary production was routinely measured by two methods. On each of 13 sampling visits to Sta. 1, in situ measurements were done; on the two occasions when all 11 stations across the transect were sampled primary production measurements were done in a constant light-intensity incubator. In situ production measurements at Sta. 1 were done at 6 depths, water samples being taken with NIO bottles from the surface, 5, 10, 15, 20, and 30 m. Four 100 ml Jena glass bottles were filled with water from each depth and one bottle at each depth was completely masked with black tape to give a measurement of dark carbon fixation. Each bottle was inoculated with 1 BCi (37 KBq) Na2 14CO3 and fitted to a clear plastic support which was slung at the requisite depth beneath a moored sparbuoy, constructed to give minimum shading of the surface bottles. At the end of the incubation, the contents of the bottles were filtered with a mild vacuum of <200 mm Hg through 0.45 Bm Millipore ® filters and frozen for return to the laboratory. The filters were subsequently dried to remove unfixed I a c o : , dissolved in 2-methoxyethanol and toluene scintillant and counted in a liquid scintillation counter; the counting efficiency was determined by the external standard, channels ratio method. The rate of carbon fixation was calculated without subtracting the 14C fixed in the dark bottles since there is no theoretical justification for this practice; no estimates were made of extracellular release of dissolved organic carbon. In March and July 1981, primary production measurements were done at alternate stations across the English Channel using a constant light incubator: the light source was two banks of four 5 ft MCFE 65 80W type 84 fluorescent lights. The incubation bottles were placed in four clear perspex tubes laid horizontally round each bank of lights; each tube was divided into six sections, wrapped with various neutral density filters to give a range of light intensities and surface seawater was pumped through to maintain the incubation bottles at ambient temperature. The light intensities in the incubator were 280, 255, 200, 130, and 75 BE m -2 s-l; bottles masked with black tape were used to estimate dark carbon fixation. Incubations were from 4 to 6 h and the water samples were treated as previously described. Photosynthetically available radiation (PAR) was recorded continuously during all in situ incubations with a Lambda Instruments LICOR quantum meter mounted in a position on the ship which gave minimum shading of the sensor. In addition, the attenuation of light in the water column was measured with a submersible light meter constructed in the laboratory, using a United Detector Technology PIN 6D photodiode, fitted with a cosine collector and filters which allowed transmission of light in the wavelength range 400 to 700 nm. Submarine light was measured simultaneously with on-deck light and corrected for variation in ambient light. Submarine light measurements were used to calculate diffuse attenuation coefficients (K) for each depth at every station; continuous surface light measurements were integrated over the period of the incubation and the light flux at each depth was calculated from the estimate of diffuse attenuation coefficient by applying Beer's Law. The data obtained from primary production experiments were used to construct photosynthesis/irradiance (P/I) curves for each incubation; a simple model was fitted to the data by non-linear least squares using a modified Marquadt algorithm (NASH, 1979) of the
28
M.B. JORDANand 1. R. JOINT
form -e.
l-exp
,
where pB is mg C fixed mg Chl a ~ h -l, P~ is the specific rate of carbon fixation at optimal light intensity, a is the initial slope o f the P/I curve, and I 0 is the surface light intensity in IaE m -2 s -t . The model cannot be used when photoinhibition is present; however, this occurred on only two occasions and the model was then used to fit the d a t a at low light levels, the photoinhibited part o f the curve at high light being fitted by eye. RESULTS
Spatial and temporal chlorophyll distribution Figure 2 shows the results for temperature and chlorophyll a for Stas 1 to 6 measured at monthly intervals from M a y to September 1980. The effect o f surface warming was apparent at the time o f the first cruise in M a y and continued until mid-August when the difference in temperature between 10 and 30 m in the middle o f the transect was more than 3°C. By early September, the thermocline had begun to break down and warmer water was mixing down to 40 m. Low concentrations o f chlorophyll a were found across the whole transect in M a y but there was an increase at Stas I and 2 in June when the highest chlorophyll a concentration was found at depths > 3 0 m; over most o f the surface waters, chlorophyll a concentrations were still very low and remained low until August. In July, chlorophyll a concentrations o f >2.5 mg m -3 were measured at 20 m in the middle o f the transect, but surface values were < 1 mg m -3. In August, much higher concentrations were found in mid-transect and the maximum of 9 mg m -3 occurred at a depth o f 5 m. Three weeks later, chlorophyll a values were 1 mg m -3 or less, over most o f the transect, although high concentrations were still found at 10 m at Sta. 1.
TEMPERATURE
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Fig. 2. Temperature profiles for Stas 1 to 6 for 5 months in 1980; the isothermal contours are drawn at 0.5°C intervals and the dates of the surveys are shown on the figures. Chlorophyll a profiles are shown below each temperature profile and the contoured intervals are shown on the figure.
5
6
Studies on phytoplankton distribution and primary production
29
Seasonal chlorophyll distribution at Sta. 1 Station 1 was sampled more frequently than the other stations in 1980 and in 1981 was the subject of an intensive study of primary production. Figure 3 shows the depth distribution of chlorophyll from March to September in 1980 and 1981. In both years, chlorophyll a maxima developed in June or July at 30 m; high chlorophyll a values were measured in mid-May 1981 but these had not occurred in 1980 when the chlorophyll a concentration was < 1 mg m -3. However, the dominant feature in both years was the presence of high concentrations of chlorophyll a in the surface water during August which were followed by chlorophyll maxima at 10 m in late August or September. Identification of the phytoplankton in 1981 showed that the high August chlorophyll a concentrations were the result of a bloom of Gyrodinium aureolum, which resulted in values of 15 mg Chl a m -3 at 5 m in August 1981. Figure 4a shows the water temperatures measured on the transect from Plymouth to Roscoff in July 1981; a well-developed thermocline was present over most of the central Channel. The G. aureolum (Fig. 4c) bloom was at its maximum at Stas 5 and 6, where chlorophyll a concentrations (Fig. 4b) of >22 mg m -3 were measured; highest values of chlorophyll were found in the surface 5 m, although the maximum number of algal cells was at 10 m. During this cruise, primary production measurements were made using a constant light incubator. Photosynthesis/light intensity curves were constructed from the data and values of Pm B, the maximum rate of chlorophyll specific photosynthesis, are shown in Fig. 4d. Minimum values of P~, with the smallest variability in the data were found at the station with the highest
Fig. 3.
Chlorophyll a concentrations measured at Sta. 1 during the spring and summer of 1980 and 1981.
30
M . B . JORDAN and I. R. JOINT
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numbers o f G. aureolum cells. At both ends of the transect, where chlorophyll a concentrations were <2 mg m -3 and G. aureolum numbers were low, P ~ was between 11.2 and 13.4 mg C mg Chl a -I h -~ , but this decreased to 2.8 in the centre o f the G. aureolum bloom.
Water transparency and primary production at Sta. 1 During 1981 a detailed study was made o f water transparency and o f the changes occurring in the p h y t o p l a n k t o n population at Sta. 1. The measurements o f diffuse attenuation coefficient (K) made between the end o f March and the end o f August are shown in Table 1. Also shown are the calculated depths at which the light intensity was 1% o f that at the sea surface: in June, the euphotic zone p r o b a b l y extended through the whole water column because the water depth at Sta. 1 was 50 m. N o measurements o f light were m a d e below 30 m and it is assumed in calculating these depths that the absorption o f light by water below 30 m does not differ significantly from that measured a b o v e 30 m. There were large changes in diffuse attenuation coefficient during the spring and summer; at the time o f the G. aureolum bloom in August, there was a large increase in attenuation coefficient and in June, when the chlorophyll content was low, the attenuation coefficient decreased significantly. Table 1 also shows the rate o f photosynthetic carbon fixation determined from in situ incubations, integrated from surface to 30 m depth. The highest hourly total of carbon fixation was measured in M a y and was double that measured in the G. aureolum bloom in August, although the total chlorophyll in the 30 m water column in M a y was only 60% of
31
Studies on phytoplankton distribution and primary production
Table 1. Diffuse attenuation coefficients, depth-integrated chlorophyll a content and photosynthetic carbon focation rates at Sta. 1 during 1981
Date
Diffuse attenuation coefficient (m-1)
Calculated depth of 1% light (m)
Total* chlorophyll a (B) (rag m -x)
Total* carbon fixation (P) (rag C m-~ h -l)
P/B (rag C mg Chl a -l h-1)
27 March 10 April 5 May 11 May 21 May 27 May 1 June 10 June 22 June 7 July 15 July 5 August 21 August
0.110 0.115 0.135 0.168 0.116 0.109 0.074 0.076 0.056 0.190 0.193 0.946 0.186
42 40 34 27 40 42 63 61 82 24 24 5 25
22.2 50.3 105.9 62.7 44.5 52.6 84.5 25.9 38.5 35.8 29.0 172.9 110.4
12.11 85.17 325.90 122.74 133.29 108.65 130.83 83.82 152.45 145.23
0.55 1.69 3.08 1.96 3.00 2.07 3.65 2.89 0.88 1.32
* Integrated from the surface to 30 m. = No data.
-
that in August. Pm a varied through the season (Fig. 5); the highest value with the largest uncertainty in estimation was at the end of May; low values of P~ were found in March and mid-May but generally less variation in Pm B at Sta. 1 was found than across the transect in J u l y (Fig. 4). DISCUSSION O n e p u r p o s e o f this study was to o b t a i n i n f o r m a t i o n o n the distribution and activity o f p h y t o p l a n k t o n in the English C h a n n e l as p a r t o f a l o n g e r t e r m s t u d y using a U O R to a u t o m a t i c a l l y r e c o r d and s a m p l e c h l o r o p h y l l a distribution (,adKEN, 1981). T h e spatial resolution o b t a i n e d by the classic sampling a p p r o a c h used in this p a p e r is m u c h inferior to t h a t
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32
M.B. JORDANand I. R. JOINT
obtained with the UOR. Also a line transect, such as that employed in the study and by the UOR, is clearly far from an ideal sampling strategy because implied temporal changes in abundance may be due to advection of different water masses into the region sampled and need not reflect changes resulting from in situ production. Nevertheless, accepting these caveats, this study has shown interesting features of phytoplankton ecology in the western English Channel. The dominant feature in 1980 and 1981 was the development of high chlorophyll a concentration in the surface water in July and August (Figs 2 to 4). In 1981, this was shown to be due to a bloom of G. aureolum; it is assumed that this alga was also responsible for the high chlorophyll a values in 1980 because dinoflagellate blooms have been a recurrent feature of the area in the recent past (e.g., PINGREEet al., 1975, 1977). Highest concentrations of chlorophyll a during the bloom were present in the surface 5 m of the water column (Fig. 4). At Sta. 1, during the bloom, the dense algal population had a dramatic effect on the transmission of light and the diffuse attenuation coefficient increased to 0.946 m -~ , reducing the depth of the euphotic zone to 5 m (Table 1). The seasonal change in attenuation coefficient followed the changes in chlorophyll a concentration but was not significantly correlated with it. In 1981 values of K increased in April and May as the chlorophyll a concentration increased but reached a maximum on 11 May, one week after the peak in chlorophyll a abundance (Table 1). There followed a period of low! attenuation coefficients, from mid-May until early July, when the concentration of chlorophyll a in the surface waters was < 1 mg m -3. However, in early June, during this period of low attenuation coefficient, a significant peak of chlorophyll a was measured at 30 m depth (Fig. 3); samples were not taken below this depth but a theoretical euphotic zone of 60 m or more (Table 1) coupled with a weakly stratified water column makes it likely that the peak of chlorophyll a extended deeper than 30 m, perhaps with a distribution similar to June 1980 (Fig. 2). In mid-July, the attenuation coefficient increased slightly although the total chlorophyll a in the column was similar to the previous month. Clearly, at certain times of the year the attenuation coefficient is influenced by something other than the absorption of light by chlorophyll. LORENZEN(1972) suggested that, for a euphotic zone of 33 m, only 10% of the light attenuation is due to plants and TOPLISSet aL (1980 to 198 I) found that non-chlorophyll sources significantly increased the value of K. However, at the time of the G. aureolum bloom in August, it is clear that algal cells were the major factor in producing the very shallow euphotic zone. G. aureolum appeared to control its own vertical distribution in the water column and at the height of the bloom the cells congregated in the surface layers of the water column. In so doing, they produced conditions of light and nutrient limitation which resulted in a reduction in total, depth-integrated primary production. The depth-integrated primary production and total chlorophyll a in the surface 30 m on 5 May and 5 August, are compared in Fig. 6: on both occasions a phytoplankton bloom occurred, but in May the total chlorophyll content of the surface 30 m was evenly distributed with depth. The rapid attenuation of light in the surface 5 m in August resulted in no measurable photosynthesis below 10 m; in contrast, in May, when the total chlorophyll content was 61% of that in August, there was significant photosynthesis at 30 m. The depth-integrated photosynthesis was 325,9 mg C m -2 h ~ in May, twice the rate of 152.5 mg C m -2 h -~ which was measured in August. Therefore, high chlorophyll a concentrations do not necessarily indicate high phytoplankton production and in this case, self-shading in the bloom limited photosynthesis. The maximum primary production in 1981 occurred in May, and not at the time of the highest phytoplankton biomass
Studies on phytoplankton distribution and primary production
33
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Fig. 6. The rates of photosynthetic carbon fixation determined by in situ incubations on 5 May and 5 August 1981, plotted with the chlorophyll a concentrations at each depth; the error bars show two standard errors in the estimate of primary production and the histograms show chlorophyll a concentrations. which was in August. The degree of limitation of photosynthesis in this bloom can also be illustrated by dividing the integrated rate of primary production by the total amount of chlorophyll in the surface 30 m (Table I); this ratio at the height of the G. aureolum bloom was almost as low as the ratio in March before significant production occurred. It is probable that the bloom was nutrient- as well as light-limited, although we have no data on nutrient concentrations at the time of the bloom. However, it is clear that high concentrations of cells in the bloom influenced the ability of the cells to photosynthesise, since P~ in the central channel at the time of the G. aureolum bloom was much lower than in other regions of the channel (Fig. 4); HARRIS (1980) has suggested that nutrient limitation results in low values of Pro n. One further objective of this study was to provide information on phytoplankton physiology which would be useful in interpreting the distribution of chlorophyll in the English Channel as measured by the UOR. FALKOWSKI(1981) has suggested that it should be possible to model the relationship between depth-integrated production and chlorophyll concentration if the available light is measured. FALKOWSKI(1981) related light intensity at the sea surface to depth-integrated values of primary production and chlorophyll to obtain a total water-column light utilization index OF) which he described as a light scaled, depth-integrated assimilation number. A plot of P/B (Table 1) against light gives a straight line of slope W; for the data from Table 1 a value of 0.48 g C g Chl a -1 E -~ m -2 was obtained which is similar, albeit slightly larger than the value of 0.43 g C g Chl a -I E -I m -2 that FALKOWSKI(1981) obtained for the New York Bight. The present data set is smaller and less complete than Falkowski's because not all measurements were made to the bottom of the euphoric zone; nevertheless, 50% of the variance in P/B in our data can be predicted from the variance in light. The similarity in the values of ~P obtained in two different sea areas and over the wide range of conditions found in this study, raises the intriguing question of whether the value of qJ may be constant. If it is, then it will be possible to use the depth-integrated distributions of chlorophyll
34
M. B, JORDAN and 1. R. JOIN'I
d e r i v e d f r o m a u t o m a t e d s a m p l e r s , s u c h as t h e U O R , c o u P l e d w i t h m e a s u r e m e n t s o f s o l a r radiation, to determine depth-integrated primary production.
Acknowledgements--We wish to thank Dr. K. R. Clarke for statistical analysis and model formulation and Mr. G. A. Robinson for the data on phytoplankton species. This work forms part of the near-shore ecology programme of the Institute for Marine Environmental Research, a component of the Natural Environmental Research Council. REFERENCES AIKEN J. ( 1981) The undulating oceanographic recorder, Mark 2. Journal of Plankton Research, 3, 551-560. BOALCH G.T., D.S. HARaOUR and E.I. BUTLER (1978) Seasonal phytoplankton production in the western English Channel 1964-1974. Journal of the Marine Biological Association of the United Kingdom, 58, 943-953. FALKOWSKI P.G. (1981) Light-shade adaption and assimilation numbers. Journal of Plankton Research, 3, 203-216. GLOVER R. S. (1967) The continuous plankton recorder survey of the North Atlantic. Symposia of the Zoological Society of London, 19, 189-210. HARRIS G.P. (1980) The measurement of photosynthesis in natural populations of phytoplankton. In: The physiological ecology of phytoplankton, I. MORRIS, editor, Blackwell Scientific Publications, Oxford, pp. 129-187. HOLLIGAN P. M. and D.S. HARBOUR (1977) The vertical distribution and succession of phytoplankton in the Western English Channel in 1975 and 1976. Journal of the Marine Biological Association of the United Kingdom, 57, 1075-1093. HOLLIGAN P. M., L. MADDOCK and J. D. DODGE (1980) The distribution of dinoflagellates around the British Isles in July 1977; a multivariate analysis. Journal of the Marine Biological Association of the United Kingdom, 60, 851-867. LORENZEN C. J. (1972) Extinction of light in the ocean by phytoplankton. Journal du Conseil, Conseilpermanent lnternational pour l'Exploration de la Mer, 34, 262-267. MADDOCK L., G. T. BOALCH and D. S. HARaOUR (1981) Populations of phytoplankton in the western English Channel between 1964 and 1974. Journal of the Marine Biological Association of the United Kingdom. 61. 565-583. NASH J. C. (1979) Compact numerical methods for computers: linear algebra and function minimisation. Adam Hilger, Bristol, 227 pp. PINGREE R. D. (1978) Mixing and stabilization of phytoplankton distribution on the north west continental shelf. In: Spatial patterns in plankton communities, J. H. STEELE, editor. NATO conference series IV. Marine Sciences 3, Plenum Press, New York, pp. 181-220. PINGREE R. D., P. M. HOLLIGAN and R. N. HEAD (1977) Survival of dinoflagellate blooms in the western English Channel. Nature, London, 265,266-268. PINGREE R. D., P. M. HOLLIGAN, G. T. MARDELL and R. N. HEAD (1976) The influence of physical stability on spring, summer and autumn phytoplankton blooms in the Celtic Sea. Journal of the Marine Biological Association of the United Kingdom, 56, 845-873. PINGREE R. D., P. R. PUGH, P. M. HOLLIGAN and G. R. FORSTER (1975) Summer phytoplankton blooms and red tides along fronts in the approaches to the English Channel. Nature. London, 258, 672-677. TOPLISS B.J., J. R. HUNTER and J. H. SIMPSON (1980--1981) Simultaneous measurements of transparency and irradiance in the coastal waters of North Wales. Marine Environmental Research. 4. 65-79. STRlCKLAND J. D. H. and T. R. PARSONS (1972) A practical handbook of seawater analysis. Bulletin 167 ( second edition), Fisheries Research Board of Canada. Ottawa. 310 pp.
0278--4343/84 $3.00 + 0.00 O 1984 PergamonPressLtd.
Studies on phytoplankton distribution and primary production in the western English Channel in 1980 and 1981 M. B. JORDAN* and I. R. JOINT* (Received 17 May 1983; in revisedform 16 August 1983; accepted 23 August 1983) Abstract--The distribution of chlorophyll on a transect of the English Channel was measured during 1980 and 1981. In both years, high concentrations of chlorophyll a were measured in midchannel in July and August and this was due to a bloom of Gyrodinium aureolum. At a near-shore station close to Plymouth, regular measurements of water transparency and primary production were made during 1981. Values of diffuse attenuation coefficient increased in the spring with increasing chlorophyll concentration; this was followed by a period o f low attenuation coefficients when chlorophyll maxima developed on the thermocline. The attenuation coefficient was greatly increased in late summer as the result o f a bloom of G. aureolum. The high cell density resulted in self-limitation and specific rates of photosynthetic carbon fixation were low during the bloom. The total water-column light utilization index (~) is calculated to be 0.48 g C g Chl a -~ E -mm -2 and the possible use of this index to calculate production from depth-integrated chlorophyll a concentrations is discussed.
INTRODUCTION
THE WESTERNEnglish Channel has been the subject of study since the turn of the century but it is relatively recently that the phytoplankton of the region has been studied. BOALCnet al. (1978) and MADDOCKet al. (1981) described the phytoplankton production of the region between 1964 and 1974 but an important development was the work of PINGREEet al. (1975, 1976, 1977), who related phytoplankton distribution to the differing physical stabilities encountered in the region and demonstrated the importance of frontal boundaries as sites of phytoplankton blooms. Hydrographic conditions across the English Channel in summer vary from stratified near the English coast, through a transitional region to the frontal boundary in the centre of the Channel and then to vertically well-mixed water near the French coast (PINGREE, 1978). The hydrographic conditions, and particularly the vertical stability of the water column, appear to play an important role in the development of dense blooms of dinoflagellates in this region (HOLLIGANand HARBOUR,1977; HOLLIGANet al., 1980). The western English Channel has also been sampled at monthly intervals since 1974 as a standard route of the Continuous Plankton Recorder Survey (CPR) (GLOVES, 1967) and in addition, since 1979, temperature, salinity, and chlorophyll fluorescence have been sampled by the Undulating Oceanographic Recorder (UOR), as described by AIKEN(1981). The UOR automatically records the measured parameters as the recorder undulates between the surface and a depth which depends on the towing cable length; information is therefore obtained in * Natural Environment Research Council, Institute for Marine Environmental Research, Prospect Place, The Hoe, Plymouth Pl I 3DH, U.K. 25
26
M.B. JORDANand I. R. JOINT
both horizontal and vertical planes. AIKEN (1981) showed the structure of temperature and chlorophyll measured by two UOR tows in a transect across the English Channel in August 1979. The purposes of this study were twofold; firstly to obtain data on the seasonal abundance of chlorophyll using standard sampling protocols which could be used as confirmation of the data obtained with the UOR and secondly to study the seasonal changes in water transparency and how this was related to phytoplankton production. METHODS The study area is shown in Fig. 1 ; 11 stations were placed equidistant on the line between Plymouth and Roscoff. This transect is the standard route samplcxl by the CPR and more recently by the U O R (G. A. ROSINSON, personal communication). Preliminary measurements began in 1980 and Stas 1 to 6 were sampled nine times between March and September. In 198 l, all 11 stations were sampled in March and July and an intensive study was made at Sta. l (50 ° 15.00'N, 04 o 09.00'W), which was sampled 13 times between March and August 1981. At each station, salinity and temperature were measured with a Braystoke inductive salinometer. Water samples were taken at 5 m depth intervals using N I O water bottles; subsamples of this water were used for primary production estimation and the remainder was
5° I
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I
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Fig. 1. Chart showing position of the 11 stations on the transect of the English Channel between Plymouth and Roscoff.
Studies on phytoplanktondistributionand primaryproduction
27
filtered through glass-fibre GF/C filters, quickly frozen on dry-ice and analysed for photosynthetic pigment content on return to the laboratory. The filters were extracted with 90% v/v acetone and the extracted pigments were measured in a 4 cm path-length cell in a Pye-Unicam SP8000 recording spectrophotometer; the concentrations of chlorophyll a and phaeopigments were calculated using the equations of STRICKLAND and PARSONS (1972). During 1981, water samples were also preserved with 1% Lugol's Iodine for subsequent identification and enumeration of phytoplankton. In 1981, primary production was routinely measured by two methods. On each of 13 sampling visits to Sta. 1, in situ measurements were done; on the two occasions when all 11 stations across the transect were sampled primary production measurements were done in a constant light-intensity incubator. In situ production measurements at Sta. 1 were done at 6 depths, water samples being taken with NIO bottles from the surface, 5, 10, 15, 20, and 30 m. Four 100 ml Jena glass bottles were filled with water from each depth and one bottle at each depth was completely masked with black tape to give a measurement of dark carbon fixation. Each bottle was inoculated with 1 BCi (37 KBq) Na2 14CO3 and fitted to a clear plastic support which was slung at the requisite depth beneath a moored sparbuoy, constructed to give minimum shading of the surface bottles. At the end of the incubation, the contents of the bottles were filtered with a mild vacuum of <200 mm Hg through 0.45 Bm Millipore ® filters and frozen for return to the laboratory. The filters were subsequently dried to remove unfixed I a c o : , dissolved in 2-methoxyethanol and toluene scintillant and counted in a liquid scintillation counter; the counting efficiency was determined by the external standard, channels ratio method. The rate of carbon fixation was calculated without subtracting the 14C fixed in the dark bottles since there is no theoretical justification for this practice; no estimates were made of extracellular release of dissolved organic carbon. In March and July 1981, primary production measurements were done at alternate stations across the English Channel using a constant light incubator: the light source was two banks of four 5 ft MCFE 65 80W type 84 fluorescent lights. The incubation bottles were placed in four clear perspex tubes laid horizontally round each bank of lights; each tube was divided into six sections, wrapped with various neutral density filters to give a range of light intensities and surface seawater was pumped through to maintain the incubation bottles at ambient temperature. The light intensities in the incubator were 280, 255, 200, 130, and 75 BE m -2 s-l; bottles masked with black tape were used to estimate dark carbon fixation. Incubations were from 4 to 6 h and the water samples were treated as previously described. Photosynthetically available radiation (PAR) was recorded continuously during all in situ incubations with a Lambda Instruments LICOR quantum meter mounted in a position on the ship which gave minimum shading of the sensor. In addition, the attenuation of light in the water column was measured with a submersible light meter constructed in the laboratory, using a United Detector Technology PIN 6D photodiode, fitted with a cosine collector and filters which allowed transmission of light in the wavelength range 400 to 700 nm. Submarine light was measured simultaneously with on-deck light and corrected for variation in ambient light. Submarine light measurements were used to calculate diffuse attenuation coefficients (K) for each depth at every station; continuous surface light measurements were integrated over the period of the incubation and the light flux at each depth was calculated from the estimate of diffuse attenuation coefficient by applying Beer's Law. The data obtained from primary production experiments were used to construct photosynthesis/irradiance (P/I) curves for each incubation; a simple model was fitted to the data by non-linear least squares using a modified Marquadt algorithm (NASH, 1979) of the
28
M.B. JORDANand 1. R. JOINT
form -e.
l-exp
,
where pB is mg C fixed mg Chl a ~ h -l, P~ is the specific rate of carbon fixation at optimal light intensity, a is the initial slope o f the P/I curve, and I 0 is the surface light intensity in IaE m -2 s -t . The model cannot be used when photoinhibition is present; however, this occurred on only two occasions and the model was then used to fit the d a t a at low light levels, the photoinhibited part o f the curve at high light being fitted by eye. RESULTS
Spatial and temporal chlorophyll distribution Figure 2 shows the results for temperature and chlorophyll a for Stas 1 to 6 measured at monthly intervals from M a y to September 1980. The effect o f surface warming was apparent at the time o f the first cruise in M a y and continued until mid-August when the difference in temperature between 10 and 30 m in the middle o f the transect was more than 3°C. By early September, the thermocline had begun to break down and warmer water was mixing down to 40 m. Low concentrations o f chlorophyll a were found across the whole transect in M a y but there was an increase at Stas I and 2 in June when the highest chlorophyll a concentration was found at depths > 3 0 m; over most o f the surface waters, chlorophyll a concentrations were still very low and remained low until August. In July, chlorophyll a concentrations o f >2.5 mg m -3 were measured at 20 m in the middle o f the transect, but surface values were < 1 mg m -3. In August, much higher concentrations were found in mid-transect and the maximum of 9 mg m -3 occurred at a depth o f 5 m. Three weeks later, chlorophyll a values were 1 mg m -3 or less, over most o f the transect, although high concentrations were still found at 10 m at Sta. 1.
TEMPERATURE
20 i "
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.
.
.
.
.
.
27 May
22 J u l y CHLOROPHYLL
26 J u n e
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9
September
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Fig. 2. Temperature profiles for Stas 1 to 6 for 5 months in 1980; the isothermal contours are drawn at 0.5°C intervals and the dates of the surveys are shown on the figures. Chlorophyll a profiles are shown below each temperature profile and the contoured intervals are shown on the figure.
5
6
Studies on phytoplankton distribution and primary production
29
Seasonal chlorophyll distribution at Sta. 1 Station 1 was sampled more frequently than the other stations in 1980 and in 1981 was the subject of an intensive study of primary production. Figure 3 shows the depth distribution of chlorophyll from March to September in 1980 and 1981. In both years, chlorophyll a maxima developed in June or July at 30 m; high chlorophyll a values were measured in mid-May 1981 but these had not occurred in 1980 when the chlorophyll a concentration was < 1 mg m -3. However, the dominant feature in both years was the presence of high concentrations of chlorophyll a in the surface water during August which were followed by chlorophyll maxima at 10 m in late August or September. Identification of the phytoplankton in 1981 showed that the high August chlorophyll a concentrations were the result of a bloom of Gyrodinium aureolum, which resulted in values of 15 mg Chl a m -3 at 5 m in August 1981. Figure 4a shows the water temperatures measured on the transect from Plymouth to Roscoff in July 1981; a well-developed thermocline was present over most of the central Channel. The G. aureolum (Fig. 4c) bloom was at its maximum at Stas 5 and 6, where chlorophyll a concentrations (Fig. 4b) of >22 mg m -3 were measured; highest values of chlorophyll were found in the surface 5 m, although the maximum number of algal cells was at 10 m. During this cruise, primary production measurements were made using a constant light incubator. Photosynthesis/light intensity curves were constructed from the data and values of Pm B, the maximum rate of chlorophyll specific photosynthesis, are shown in Fig. 4d. Minimum values of P~, with the smallest variability in the data were found at the station with the highest
Fig. 3.
Chlorophyll a concentrations measured at Sta. 1 during the spring and summer of 1980 and 1981.
30
M . B . JORDAN and I. R. JOINT
0
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t-ig. 4. Data obtained on the complete transect from Stas 1 to 11 on 15 to 17 July 1981. (a) Isothermal contours drawn at 0.5°C intervals; (b) chlorophyll a contours; (c) log10 number of Gvrodinium aureolum 1-1 plotted at intervals of 0.2 togl0 cell number l-l; (d) P~mdetermined in a constant light incubator; the data at Sta. 9 (+) could not be fitted to the model and/~m was estimated by eye. Pm values are plotted with the 95% confidence intervals determined by large sample maximum likelihood theory.
numbers o f G. aureolum cells. At both ends of the transect, where chlorophyll a concentrations were <2 mg m -3 and G. aureolum numbers were low, P ~ was between 11.2 and 13.4 mg C mg Chl a -I h -~ , but this decreased to 2.8 in the centre o f the G. aureolum bloom.
Water transparency and primary production at Sta. 1 During 1981 a detailed study was made o f water transparency and o f the changes occurring in the p h y t o p l a n k t o n population at Sta. 1. The measurements o f diffuse attenuation coefficient (K) made between the end o f March and the end o f August are shown in Table 1. Also shown are the calculated depths at which the light intensity was 1% o f that at the sea surface: in June, the euphotic zone p r o b a b l y extended through the whole water column because the water depth at Sta. 1 was 50 m. N o measurements o f light were m a d e below 30 m and it is assumed in calculating these depths that the absorption o f light by water below 30 m does not differ significantly from that measured a b o v e 30 m. There were large changes in diffuse attenuation coefficient during the spring and summer; at the time o f the G. aureolum bloom in August, there was a large increase in attenuation coefficient and in June, when the chlorophyll content was low, the attenuation coefficient decreased significantly. Table 1 also shows the rate o f photosynthetic carbon fixation determined from in situ incubations, integrated from surface to 30 m depth. The highest hourly total of carbon fixation was measured in M a y and was double that measured in the G. aureolum bloom in August, although the total chlorophyll in the 30 m water column in M a y was only 60% of
31
Studies on phytoplankton distribution and primary production
Table 1. Diffuse attenuation coefficients, depth-integrated chlorophyll a content and photosynthetic carbon focation rates at Sta. 1 during 1981
Date
Diffuse attenuation coefficient (m-1)
Calculated depth of 1% light (m)
Total* chlorophyll a (B) (rag m -x)
Total* carbon fixation (P) (rag C m-~ h -l)
P/B (rag C mg Chl a -l h-1)
27 March 10 April 5 May 11 May 21 May 27 May 1 June 10 June 22 June 7 July 15 July 5 August 21 August
0.110 0.115 0.135 0.168 0.116 0.109 0.074 0.076 0.056 0.190 0.193 0.946 0.186
42 40 34 27 40 42 63 61 82 24 24 5 25
22.2 50.3 105.9 62.7 44.5 52.6 84.5 25.9 38.5 35.8 29.0 172.9 110.4
12.11 85.17 325.90 122.74 133.29 108.65 130.83 83.82 152.45 145.23
0.55 1.69 3.08 1.96 3.00 2.07 3.65 2.89 0.88 1.32
* Integrated from the surface to 30 m. = No data.
-
that in August. Pm a varied through the season (Fig. 5); the highest value with the largest uncertainty in estimation was at the end of May; low values of P~ were found in March and mid-May but generally less variation in Pm B at Sta. 1 was found than across the transect in J u l y (Fig. 4). DISCUSSION O n e p u r p o s e o f this study was to o b t a i n i n f o r m a t i o n o n the distribution and activity o f p h y t o p l a n k t o n in the English C h a n n e l as p a r t o f a l o n g e r t e r m s t u d y using a U O R to a u t o m a t i c a l l y r e c o r d and s a m p l e c h l o r o p h y l l a distribution (,adKEN, 1981). T h e spatial resolution o b t a i n e d by the classic sampling a p p r o a c h used in this p a p e r is m u c h inferior to t h a t
15-
im -
10-
t t
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t
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I
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t] t !
May
I
Jun
I
Jul
t I
Au9
I
Seasonal variation in Pm B at Sta. 1 in 1981 plotted with the 95% confidence intervals determined by large sample maximum likelihood theory.
32
M.B. JORDANand I. R. JOINT
obtained with the UOR. Also a line transect, such as that employed in the study and by the UOR, is clearly far from an ideal sampling strategy because implied temporal changes in abundance may be due to advection of different water masses into the region sampled and need not reflect changes resulting from in situ production. Nevertheless, accepting these caveats, this study has shown interesting features of phytoplankton ecology in the western English Channel. The dominant feature in 1980 and 1981 was the development of high chlorophyll a concentration in the surface water in July and August (Figs 2 to 4). In 1981, this was shown to be due to a bloom of G. aureolum; it is assumed that this alga was also responsible for the high chlorophyll a values in 1980 because dinoflagellate blooms have been a recurrent feature of the area in the recent past (e.g., PINGREEet al., 1975, 1977). Highest concentrations of chlorophyll a during the bloom were present in the surface 5 m of the water column (Fig. 4). At Sta. 1, during the bloom, the dense algal population had a dramatic effect on the transmission of light and the diffuse attenuation coefficient increased to 0.946 m -~ , reducing the depth of the euphotic zone to 5 m (Table 1). The seasonal change in attenuation coefficient followed the changes in chlorophyll a concentration but was not significantly correlated with it. In 1981 values of K increased in April and May as the chlorophyll a concentration increased but reached a maximum on 11 May, one week after the peak in chlorophyll a abundance (Table 1). There followed a period of low! attenuation coefficients, from mid-May until early July, when the concentration of chlorophyll a in the surface waters was < 1 mg m -3. However, in early June, during this period of low attenuation coefficient, a significant peak of chlorophyll a was measured at 30 m depth (Fig. 3); samples were not taken below this depth but a theoretical euphotic zone of 60 m or more (Table 1) coupled with a weakly stratified water column makes it likely that the peak of chlorophyll a extended deeper than 30 m, perhaps with a distribution similar to June 1980 (Fig. 2). In mid-July, the attenuation coefficient increased slightly although the total chlorophyll a in the column was similar to the previous month. Clearly, at certain times of the year the attenuation coefficient is influenced by something other than the absorption of light by chlorophyll. LORENZEN(1972) suggested that, for a euphotic zone of 33 m, only 10% of the light attenuation is due to plants and TOPLISSet aL (1980 to 198 I) found that non-chlorophyll sources significantly increased the value of K. However, at the time of the G. aureolum bloom in August, it is clear that algal cells were the major factor in producing the very shallow euphotic zone. G. aureolum appeared to control its own vertical distribution in the water column and at the height of the bloom the cells congregated in the surface layers of the water column. In so doing, they produced conditions of light and nutrient limitation which resulted in a reduction in total, depth-integrated primary production. The depth-integrated primary production and total chlorophyll a in the surface 30 m on 5 May and 5 August, are compared in Fig. 6: on both occasions a phytoplankton bloom occurred, but in May the total chlorophyll content of the surface 30 m was evenly distributed with depth. The rapid attenuation of light in the surface 5 m in August resulted in no measurable photosynthesis below 10 m; in contrast, in May, when the total chlorophyll content was 61% of that in August, there was significant photosynthesis at 30 m. The depth-integrated photosynthesis was 325,9 mg C m -2 h ~ in May, twice the rate of 152.5 mg C m -2 h -~ which was measured in August. Therefore, high chlorophyll a concentrations do not necessarily indicate high phytoplankton production and in this case, self-shading in the bloom limited photosynthesis. The maximum primary production in 1981 occurred in May, and not at the time of the highest phytoplankton biomass
Studies on phytoplankton distribution and primary production
33
mg c h l o r o p h y l l a.rn 3. 0 i
o
5 I
10 I
lo_.2o
, ~e ~
10
15 I
.~,o
, 20
,o
sp
40
50
i 30
20 I
m~C,~ 1
~o
r,o
, 6 |0
- 7|0
,
=gc.=~ _1
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Fig. 6. The rates of photosynthetic carbon fixation determined by in situ incubations on 5 May and 5 August 1981, plotted with the chlorophyll a concentrations at each depth; the error bars show two standard errors in the estimate of primary production and the histograms show chlorophyll a concentrations. which was in August. The degree of limitation of photosynthesis in this bloom can also be illustrated by dividing the integrated rate of primary production by the total amount of chlorophyll in the surface 30 m (Table I); this ratio at the height of the G. aureolum bloom was almost as low as the ratio in March before significant production occurred. It is probable that the bloom was nutrient- as well as light-limited, although we have no data on nutrient concentrations at the time of the bloom. However, it is clear that high concentrations of cells in the bloom influenced the ability of the cells to photosynthesise, since P~ in the central channel at the time of the G. aureolum bloom was much lower than in other regions of the channel (Fig. 4); HARRIS (1980) has suggested that nutrient limitation results in low values of Pro n. One further objective of this study was to provide information on phytoplankton physiology which would be useful in interpreting the distribution of chlorophyll in the English Channel as measured by the UOR. FALKOWSKI(1981) has suggested that it should be possible to model the relationship between depth-integrated production and chlorophyll concentration if the available light is measured. FALKOWSKI(1981) related light intensity at the sea surface to depth-integrated values of primary production and chlorophyll to obtain a total water-column light utilization index OF) which he described as a light scaled, depth-integrated assimilation number. A plot of P/B (Table 1) against light gives a straight line of slope W; for the data from Table 1 a value of 0.48 g C g Chl a -1 E -~ m -2 was obtained which is similar, albeit slightly larger than the value of 0.43 g C g Chl a -I E -I m -2 that FALKOWSKI(1981) obtained for the New York Bight. The present data set is smaller and less complete than Falkowski's because not all measurements were made to the bottom of the euphoric zone; nevertheless, 50% of the variance in P/B in our data can be predicted from the variance in light. The similarity in the values of ~P obtained in two different sea areas and over the wide range of conditions found in this study, raises the intriguing question of whether the value of qJ may be constant. If it is, then it will be possible to use the depth-integrated distributions of chlorophyll
34
M. B, JORDAN and 1. R. JOIN'I
d e r i v e d f r o m a u t o m a t e d s a m p l e r s , s u c h as t h e U O R , c o u P l e d w i t h m e a s u r e m e n t s o f s o l a r radiation, to determine depth-integrated primary production.
Acknowledgements--We wish to thank Dr. K. R. Clarke for statistical analysis and model formulation and Mr. G. A. Robinson for the data on phytoplankton species. This work forms part of the near-shore ecology programme of the Institute for Marine Environmental Research, a component of the Natural Environmental Research Council. REFERENCES AIKEN J. ( 1981) The undulating oceanographic recorder, Mark 2. Journal of Plankton Research, 3, 551-560. BOALCH G.T., D.S. HARaOUR and E.I. BUTLER (1978) Seasonal phytoplankton production in the western English Channel 1964-1974. Journal of the Marine Biological Association of the United Kingdom, 58, 943-953. FALKOWSKI P.G. (1981) Light-shade adaption and assimilation numbers. Journal of Plankton Research, 3, 203-216. GLOVER R. S. (1967) The continuous plankton recorder survey of the North Atlantic. Symposia of the Zoological Society of London, 19, 189-210. HARRIS G.P. (1980) The measurement of photosynthesis in natural populations of phytoplankton. In: The physiological ecology of phytoplankton, I. MORRIS, editor, Blackwell Scientific Publications, Oxford, pp. 129-187. HOLLIGAN P. M. and D.S. HARBOUR (1977) The vertical distribution and succession of phytoplankton in the Western English Channel in 1975 and 1976. Journal of the Marine Biological Association of the United Kingdom, 57, 1075-1093. HOLLIGAN P. M., L. MADDOCK and J. D. DODGE (1980) The distribution of dinoflagellates around the British Isles in July 1977; a multivariate analysis. Journal of the Marine Biological Association of the United Kingdom, 60, 851-867. LORENZEN C. J. (1972) Extinction of light in the ocean by phytoplankton. Journal du Conseil, Conseilpermanent lnternational pour l'Exploration de la Mer, 34, 262-267. MADDOCK L., G. T. BOALCH and D. S. HARaOUR (1981) Populations of phytoplankton in the western English Channel between 1964 and 1974. Journal of the Marine Biological Association of the United Kingdom. 61. 565-583. NASH J. C. (1979) Compact numerical methods for computers: linear algebra and function minimisation. Adam Hilger, Bristol, 227 pp. PINGREE R. D. (1978) Mixing and stabilization of phytoplankton distribution on the north west continental shelf. In: Spatial patterns in plankton communities, J. H. STEELE, editor. NATO conference series IV. Marine Sciences 3, Plenum Press, New York, pp. 181-220. PINGREE R. D., P. M. HOLLIGAN and R. N. HEAD (1977) Survival of dinoflagellate blooms in the western English Channel. Nature, London, 265,266-268. PINGREE R. D., P. M. HOLLIGAN, G. T. MARDELL and R. N. HEAD (1976) The influence of physical stability on spring, summer and autumn phytoplankton blooms in the Celtic Sea. Journal of the Marine Biological Association of the United Kingdom, 56, 845-873. PINGREE R. D., P. R. PUGH, P. M. HOLLIGAN and G. R. FORSTER (1975) Summer phytoplankton blooms and red tides along fronts in the approaches to the English Channel. Nature. London, 258, 672-677. TOPLISS B.J., J. R. HUNTER and J. H. SIMPSON (1980--1981) Simultaneous measurements of transparency and irradiance in the coastal waters of North Wales. Marine Environmental Research. 4. 65-79. STRlCKLAND J. D. H. and T. R. PARSONS (1972) A practical handbook of seawater analysis. Bulletin 167 ( second edition), Fisheries Research Board of Canada. Ottawa. 310 pp.