ENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS IN THE SEA 

J. H. Steele 

Marine Laboratory, Abcrdecn 

ABSTRACT 

A theoretical equation for the photosynthesis-light relation is devclopcd which includes 

the effects of inhibition in intcnsc light. Assuming 1) that phytoplankton adapts to seasonal 

light changes and 2) that nutrient dcficicncy affects the carbon:chlorophyll ratio of 

natural phytoplankton populations, equations arc derived which dcterminc photosynthesis 

per unit chlorophyll and the carbon : chlorophyll ratio as functions of incident radiation and 

nutrient concentration. 

These equations appear to describe the main trends in the open North Sea and in a 

sea loch on the west of Scotland. The photosynthesis-chlorophyll relation also describes 

the main trends of observations in the Sargasso. For a very shallow turbid area, the agreement was not so good. 

INTRODUCTION 

The measurement of chlorophyll a concentration in the sea is widely used as a 

parameter for phytoplankton populations. 

The data can be interpreted in two ways, 

as an index of productivity and as an index 

of the plant population. The former is 

probably the most direct application since 

chlorophyll a is the central component of 

the photosynthetic mechanism. By assuming a fixed relation between light and photosynthesis, Ryther and Yentsch ( 1957) 

deduced a formula which estimated the 

gross production from a knowledge of the 

incident light, the extinction coefficient 

and the chlorophyll a concentration. The 

main disadvantage of this method is that a 

fixed light/photosynthesis relation does not 

take account of the known adaptation of 

plants to varying light intcnsitics (Ryther 

and Menzel 1959; Steeman-Nielsen and 

Hansen 1959a). The second use of chlorophyll a, as an index of population, depends 

on the ratio of organic carbon (or dry 

weight) to chlorophyll in the plants. There 

have been several estimates of the carbon : 

chlorophyll ratio but they cover a very 

wide and rather dubious range from 4 : 1 to 

150 : 1 ( Steele 1959). Riley, Stommel, and 

Bumpus ( 1949) suggcstcd that different 

ratios should be used for the tropical Sargasso Sea (140 : 1) and for tcmpcrate rcgions (53 : 1). It seems reasonable that 

there should be widespread changes in this 

ratio for different regions and also for different seasons, but without an understanding of the factors which control these 

changes the use of chloro,phyll as a population index is less than adequate. 

In laboratory cultures these two effects, 

light adaptation and changes in the carbon : 

chlorophyll ratio, have been frequently 

studied. It has been observed that increased light and, especially, decreased 

nutrients produce chlorotic cells, and the 

latter has an obvious correspondence with 

decrcascd photosynthetic rate. In this 

paper, by assuming simplified forms for 

these variations, formulae will be deduced 

which allow their effects to be included in 

the interpretation of ecological data. The 

concepts used are certainly too simple, so 

that the theoretical results must be regarded as a tentative first step. 

RELATION BETWEEN LIGI-IT INTl3NSITY 

AND* PHOTOSYNTIIE~C RATE 

The shape of the curve relating light and 

photosynthesis has been the subject of considerable study. It is obvious that a linear 

relation holds only for lo,w light intensities 

and that as the intensity is increased the 

photosynthetic rate tends towards a maximum value. The most usual formulation of 

this effect has been of the type (Rabinowitch 1945; Smith 1936; Winokur 1948). 

P ( P2m -pQ)% = aI (1) 

where p is the photosynthetic rate with a . maxlmum pm, I is the light intensity and a 

is a constant which dctermincs the initial 

137 
138 J. I-1. STEELE 

4 Pm 

FIG. 1, Typical light/photosynthesis curves dcrived from equation ( 1) for two values of a. 

slope of the curve at low light. By varying 

(E, different curves are obtained (Fig. 1) 

whose changes could be thought to imitate 

the effects of “light” and “dark” adaptation. 

This curve has a serious disadvantage for 

marinc ecology. From ( I) p tends asymptotically to pm as I tends to infinity, In the 

sea, however, it appears that at high light 

intensities /p decreases again so that the . maxrmum, pm, occurs at a finite value of I. 

This can be seen in many descriptions of 

experiments with natural marine populations ( Coblcntz-Mishke 1960; SteemanNielsen and Hansen 1959a; Ryther and 

Menzel 1959) and also from in situ Cl4 experiments (Currie 1958; Rodhc 1958; Steele 

and Baird 1961). Th e experiments of Ryther 

and Menzel (1959) provide the most suitable data since they co,ver a wide range of 

light intensities (Fig. 2). The samples were 

taken from three depths, 0, 50, and 100 m, 

in the Sargasso Sea corresponding to lOO%, 

lo%, and 1% of the surface light. Because 

of the great stability of the water column 

over the range of depths, the samples represent populations of “sun,” “intermediate,” 

and “shade” adapted plants. There is a 

relatively rapid decrease in photosynthetic 

rate for light intensities above the optimum 

and it is this feature which needs to be incorporated in any formulation of the light/ 

photosynthesis relation. 

The following expression 

P = n p,,, Ie’-“I (2) 

can be seen from Figure 2 to give an adequate description of the main features 

100 

50 

I -// 

WorlJ 

. 

. 

50 I % 10 

0 l.'flLYi - 

l 

. . 

-. 

0 2 4 6 8 IO 

I Clo’fcmt candles) 

FIG. 2. Photosynthesis-light intensity data for 

phytoplankton taken from depths in the Sargasso 

Sea coxxsponding to lOO%, lo+%, and 1% of the 

surface light (Ryther and Menzel 1959~). The 

curves are derived from ( 2 ) by choosing appropriate values of ~1. 

(where changing curves are followed by 

changing CI ) . For the moment p, is the 

relative maximum (i.e., 100%) for each 

curve. In this form the inhibition is imitated by the exponentially decreasing term. 

For laboratory cultures, at high light intensities, a similar curve has been found 

(Myers and Burr 1940; see Rabinowitch 

1945, p. 535) and is attrib,uted by Rabinowitch to the inhibition of photosynthesis by 

photo-oxidation. However, for land plants 

it has been suggcstcd (Rabinowitch, p. 874) 

that the midday suppression of photosynthesis is not simply explainable in terms 

of light inhibition but may be a more inhcrent diurnal rhythm. 

This rhythm is observed in the sea and 

in fresh water in terms of diurnal changes 

in chlorophyll concentration (Yentsch and 

Ryther 1957; Shimada 1958; Ichimura 1960) 
ENVIRONMlWTAL CONTROL OF I’IIOTOSYNTEIESIS 139 

and in CL4 uptake (Doty and Oguri 1957). 

It seems likely that seasonal and depth variations in photosynthesis and carbon : chlorophyll ratio will be complicated by thcsc 

diurnal effects although Doty (1959) suggests that at the latitude of the North Sea 

they may be negligible. In this paper only 

the “daily averages” will be considered. 

Whatever the cause, the general agreement 

between this curve (2) and observations in 

the sea make it more useful than ( 1) for 

ecological studies. 

I This general form for the relation needs 

to be converted into a quantitative cxpression by fixing values for the constants. 

There are two constants involved, a and “pnL, 

and these depend on the photosynthetic 

yield at low light intensities and at optimum light intensity. 

At low light intensities it is probable that 

photosynthetic rather than non-photosynthetic factors in the cell will be limiting 

(Tamiya, et nZ. 1953). Thus the defining 

relation should be between light and chlorophyll, and this will bc formalized into 

the strict assumption that, in all circumstances, there is fixed value, a, so that at 

low light intensities 

p = (Y I, per unit of chlorophyll ( 3) 

This has been formulated by Rabinowitch 

(1945, p. 1029) in terms of the maximum 

quantum yield. Recent determinations of 

this factor suggest a value between % to l/s 

(Duysens 1956) and using a mc,an of % 

gives a value for 0! of 

LY = 4.10m4 (g C/lux/hr/g chlor) (4) 

Steeman-Nielsen and Jensen ( 1957) derive 

a value of 3.6 lo-* from Winokur (1948) 

and 4.1 lo-* from Gessner (1944) in the 

same units. 

At higher light intensities, and in particular when photosynthesis is at its maximum pin, it is probable that it is not the 

photosynthetic mechanisms which are limiting, but the ability of the phytoplankton 

cells to assimilate certain compounds. 

Myers ( 1953) in kinetic studies of Chlorella 

pyrenoidosn states that “p, is an inherent 

characteristic of its internal biochemical 

machinery. . . . The rate limiting process 

LIGHT INTENSITY 

L tGHT INTENSITY 

FIG. 3. The theoretical consequences of a&ptation in terms of (a) photosynthesis per unit 

plant carbon, ( b ) photosynthesis per unit chlorophyll. 

which establishes p, must be some cellular 

process other than photosynthesis.” Again 

this will be formalized into the strict assumption that in units of carbon there is a 

fixed value for pm independent of light 

adaptation and with the proviso that nutrients are not limiting. The value to be 

used for p, is that given by Myers, 

pltl. = 0.08 ( g C/g plant C/hr) (5) 

To relate ( 4) and ( 5) in terms of the 

relation given by (2), the ratio c of carbon : 

chlorophyll in the cells must used. 

Thus for (3), in carbon units, for I small 

a1 

=- 

p c (6) 

Also, from (2), for I small 

p = Q p, f3 1 

Therefore, from ( 6) and ( 7) 

a 

c=- 

a p,, e 

(7) 

(8) 

This shows that the carbon : chlorophyll 

ratio depends on the constant CI which in 

turn determines the degree of light or dark 

adaptation. Increasing light adaptation 

produces increases in c and so corresponds 

to the generally expected decrcasing proportion of chlorophyll in the cells. The consequences are shown by Figure 3 in terms 
140 J. I-1. STEELE 

FIG. 4. The cffccts of diurnal light variation on 

the depth distribution of photosynthesis (see 

text ) . 

of carbon and chlorophyll. For the former, 

the maximum remains the same but the 

slope at low light intensities varies, for the 

latter the slope is unchanged by adaptation 

but the maximum varies, These curves are 

similar in principle to those put forward by 

Steeman-Nielsen and Hansen ( 1959a). 

In applying this theoretical relation to 

natural conditions, the first problem conterns the consequences of the diurnal variations in light intensity. As a simple means 

of imitating the general effects of diurnal 

changes, it will be supposed that the light 

increases linearly from dawn to midday and 

then decreases linearly to sunset. Equation 

(2) can then be integrated to give the 

average photosynthetic rate, r), corrcsponding to the average light I, 

+k$ I l- (1+2aI) eezar’ 

1 (9) 

The effects of this in the sea can be found 

using the usual relation 

where k is the extinction coefficient and I0 

is the surface intensity. Figure 4 shows (2) 

and (9) plotted against an arbitrary depth 

scale. Also since a and I ( or I) always 

occur together as nI, this scale is shown on 

the right-hand side. It is apparent that 

except for high values of u1 the curves do 

not differ greatly in their general shape. In 

particular, p still has its maximum close to 

UI = 1. This general shape is very similar 

to those given by in situ Cl4 observations 

( Stecman-Nielsen and Jensen 1957; Currie 

1958; Rodhe 1958; Sorokin, Snopkov and 

Grinbcrg 1959) and also by the earlier 

oxygen results of Jcnkin ( 1937). In these 

observations the maximum usually occurs 

below the sea surface so that there is a decrease near the surface, but the surface is 

not usually so far above the maximum that 

this decrease is considerable. For summer 

in the North Sea (Steele and Baird 1961) 

the maximum appears to be between 100% 

and 50% of the surface light but some shading of the surface bottles may have decreased the inhibition at this level. Steeman-Nielsen and Jensen ( 1957) give a general curve similar to Figure 4 in which the 

maximum is at a depth where the light is 

between ‘h and 1/3 of the surface intensity. 

Sorokin, et al. ( 1959) also found the maximum between 30% and 50% of surface 

light, and the other studies suggest a similar position for the maximum. 

On the basis of this general similarity it 

will be assumed that the plants always 

adapt to the average seasonal light in such 

a way that the sea surface occurs at the 

same position on the light-photosynthesis 

curve. This level will be strictly defined by 

taking a IO = 2 indicated by the dashed 

line in Figure 3. Since the two curves, p 

and p, do not differ greatly in shape below 

this level and since it is only the general 

shape that is important, the equation for p 

will be used to describe natural events in 

the sea rather than @ which has a more 

complex mathematical form. I will be taken 

as the average light intensity during the 

daylight hours. The only change rcquircd 

is in the numerical value of p, and by comparison of ( 2) and ( 9) it can be shown that 

-- 

p, = 0.82 pm (10) 

so that in future (2) will be used with 

p,,, = 0.066 g C/g plant C/hr . 

The application of the relation aI0 = 2 to 

populations in a certain depth layer implies 

that the layer is sufficiently mixed to pre- 
ENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS 141 

vent the plants from being isolated from 

the surface. This simplifying assumption is 

rather vague and the possible theoretical 

conscquenccs of isolation in deeper water 

by a very stable thermocline will be discussed later in this paper. 

The relation aI0 = 2, together with ( 8) 

gives 

(11) 

Thus perfect adaptation by the plants to 

decreasing surface light, IO, would require 

a continually decreasing carbon : chlorophyl ratio. Obviously there must be some 

lower limit for this ratio which will in turn 

define the lower limit of the light range 

within which the plants can adapt. With 

laboratory cultures very low and very high 

ratios can be obtained. For Chlorella, ratios 

of 8 : 1 and 1,600 : 1 have been found 

(Mimer 1953). Fogg (1959) has shown 

that, as a culture becomes nitrate deficient, 

the dry weight : chlorophyll ratio goes from 

75 : 1 to 910 : 1. Steele and Baird ( 1962a), 

using the same methods for chlorophyll and 

carbon as are used at sea (Steele and 

Baird 1961)) found that with cultures of 

Skeletonema and Nnnnochloris the carbon : 

chlorophyll ratios gave minima during the 

exponential growth phase of 26 : 1 and 

28 : 1 respectively; thereafter the ratios increased continuously as the cultures aged. 

In the sea very low values are not found 

although there are very few data for this 

factor at present. Previous results suggest 

that the ratio is usually greater than 30 : 1 

( IIarris and Riley 1956; Parsons and Strickland 1959). A minimum value of 23 : 1 was 

found for very favorable conditions in the 

North Sea ( Steele and Baird 196213). On 

this basis a minimum ratio of 20 : 1 will be 

used for natural conditions. With this value 

the minimum light intensity for which 

adaptation is still possible is IO = 1.82 . 10zk 

lux. 

In these calculations light intensity has 

been expressed in illumination units since 

these are commonly used in laboratory 

work. Natural light, however, is usually 

given in radiation units and the rather arbitrary conversion factor given by Svcrdrup, 

Johnson and Fleming (1942) will be used, 

1.2 ’ 10” lux = 1 g cal/cm”/hour. 

Thus a = 0.48 g C/hr/ (g cal/cm2/hr). Or, 

expressing it in the more natural ecological 

units, a = 0.48 g C/day/( g cal/cm2/day). 

For days as units, the maximum photosynthetic rate becomes pp, . h where h is the 

length of daylight in hours. 

NUTRIENT LIMITATION ON PHOTOSYNTHETIC 

RATE 

So far the role of nutrient limitation has 

been ignored, but it is apparent that in the 

sea, the lack of nutrients must be a dominant 

factor in restricting production. Yet it has 

always been difficult to see how this operates in the sea. The success of the Ryther 

and Yentsch (1957) formula for production 

in terms of light and chlorophyll alone, implies that in this relation the effect of nutrient limitation can be ignored. Similarly, 

Currie ( 1958) showed that for areas with 

high and low chlorophyll contents, the Cl”- 

chlorophyll relations were very similar and 

he suggested that the differences in productivity could not be deduced from variations in the CL4-chlorophyll relation. In 

fresh water Wright (1960) has shown that 

variations in optimum photosynthesis on a 

cell volume basis, are similar to the changes 

in chlorophyll per unit cell volume. He 

suggests that decrease in the latter is caused 

by nutrient limitation. The use of chlorophyll : particulate phosphorus and chlorophyll : carotenoid ratios as indices of the 

chlorophyll content of marine phytoplankton in the sea and in cultures suggest that 

in both situations there can be a wide range 

of values associated with the effects of nutrient deficiency ( Ketchum, & nl. 1958). 

There is supporting evidence for this from 

culture experiments ( Fleischer 1935) where 

it was found that the photosynthesis : chlorophyll ratio remained nearly constant over 

a wide range of nitrate and iron concentrations and it was the carbon : chlorophyll 

ratio which varied. Generally, the decreasing chlorophyll content of cells with increasing nutrient limitation is an obvious 

feature of aging plant cultures (Harvey 
142 J. I-1. STEXLE 

1953; Fogg 1959; Steele and Baird 1962a). 

Thus, although it may not describe fully the 

implications of all the experimental work 

on phytoplankton, these general features of 

ecological and experimental results will bc 

converted into the strict assumption that 

nutrient limitation does not change the photosynthesis : chlorophyll relation but operates by varying the carbon : chlorophyll 

ratio. 

From (2), (3), and nIo = 2, 

p = CY I exp (-21/I,) (g C/g chlor/day) ( 12) 

Since this does not contain pm the simplest 

way to imitate formally the preceding hypothesis is to allow p, to decrease with increasing nutrient limitation. From (8) this 

will produce the postulated changes in c. 

There remains the problem that for this 

to be applied to ecological data, some observable factor must be used as a measure 

of the degree of nutrient limitation and the 

obvious choice would appear to be a nutrient concentration in the water. An apparent indication from cultures of Nitzschia 

closterium of the degree of limitation in 

terms of phosphate ( Ketchum 1939) has 

been used in previous work (Riley 1946; 

Riley, Stommel and Bumpus 1949; Steele 

1958). Yet it is doubtful if any single nutrient can be used as an index for all latitudes and all seasons. Not only are there 

varied opinions concerning which substances are of most importance as limiting 

factors (Daisley 1957; Droop 1957; Ryther 

and Guillard 1959)) but it is not necessarily 

true that the limiting effects inside the plant 

cells will keep in step with external conccntrations in the environment. Thus in the 

development here, instead of defining c1 

priori a relation between limiting effect 

and nutrient concentration, this limiting 

effect will be expressed as a general function 

fPv1 

which will be supposed to decrease with 

some nutrient concentration, N. The comparison of theory and observation will then 

have the purpose of determining to what 

extent realistic relations c,an be obtained 

between f ( N ) and some nutrient, which 

could thus be considered as an index of the 

effects of nutrient limitation for a certain 

area. 

Incorporating this relation, and also nIo 

III 2, in (2) and (11) gives 

2PmWW 

;P= IO exp (L--fW&) 

0.132 h f(N) I =I 

IO 

exp (l-WOO), 

(g C/g C/day) (13) 

a IO 

c=2p,ehf(N) 

1.34 I() 

=-, (gC/gchlor) hf W) 

The natural radiation below which plant 

adaptation is no longer possible according 

to this theory can now be calculated from 

(14) as 15 g cal/cm2/hr or 180 g cal/ 

cm2/day for an average 12 hours of daylight. 

TEMPERATURE EPFECTS 

According to Rabinowitch ( 1945, p. 1231 

et seq. ) it is not unreasonable to suppose 

there is very little temperature effect on the 

photosynthetic rate when light is limiting. 

That is, it may be assumed that the photosynthetic mechanism as such is temperature 

independent. In strong light, on the other 

hand, when non-photosynthetic mechanisms 

are limiting there appear to be strong temperature effects in cultures, with Qlo probably near to 2. It is interesting to note that 

on the above reasoning, a! would be unaffected and p, would bc the temperature 

dependent f ac tar. This implies that the 

effects of temperature differences would 

operate by varying the carbon : chlorophyll 

ratio and the photosynthesis : chlorophyll 

relation would be unchanged. However, 

these temperature effects, which arc extremely important under expcrimcntal conditions, may to some extent be cancclled out 

by adaptation to different climatic regions. 

Further, even with Q1 o = 2, temperature 

could account for only a fraction of the observed changes. 

Since it is difficult to choose a correct 

relation for the temperature dependence 

and since this may be comparatively small 
ENVIRONMENTAL CONTROL OE’ PHOTOSYNTIIEXS 143 

due to adaptation, the cffccts of environmental temperature differences have been 

neglected. 

ETIOLATION 

In considering the relation between light 

and the carbon : chlorphyll ratio, the effects of extremely low light were not considered. It is well known that with land 

plants fairly lengthy periods in the dark 

produce considerable increases in the 

carbon : chlorophyll ratio and this effect is 

used experimentally to produce e tiolated 

plants ( Rabinowitch 1945), 

During winter in temperate latitudes not 

only is the surface light low but extensive 

vertical mixing produced by cooling causes 

the plants to circulate throughout a very 

deep mixed layer in which the average light 

is very much lower. This means that the 

plants are well below the compensation 

level of light where photosynthesis balances 

respiration (Sverdrup 1953). It seems very 

likely that a similar effect of etiolation 

should result under these conditions. Some 

of the data to be presented later suggest 

this but it is not possible to give a definite 

value for the carbon : chlorophyll ratio. 

COMPARISON WITH OBSERVATIONS 

The theory which has been set out here 

predicts patterns in the seasonal changes of 

photosynthetic rates and the carbon : chlorophyll ratios. Strict numerical values have 

been calculated for these changes but because of the many simplifications which 

have been introduced the initial problem 

is to discover whether the general patterns 

rather than the numerical values agree with 

observations. There are, further, the difficulties raised by the observations themselves since none of the available data 

measure directly the predicted factors. 

Equation ( 12) relates photosynthesis to 

units of chlorophyll but Cl4 data probably 

represent net production (photosynthcsisrespiration ) . Particulate organic carbon 

measurements in the sea include “detritus” 

so that the probable carbon : chlorophyll 

ratios in the plants have to be deduced indirectly ( Steele and Baird 1961, 196213). 

The maximum photosynthetic rate in 

40- 

IQI 

SO 

FIG. 5. The correspondence between theorctical cstimatcs of maximum photosynthetic rate and 

observed maxima from in situ CL4 results on the 

Fladcn Ground ( g C/g chlor/day ). 

terms of chlorophyll can be deduced from 

( 12) taking I = % IO. Then, for the North 

Sea, Figure 10, 

pmas = 0.088 10 ( gC/g chlor/day ) , for I0 B 180 g cal/cm2/day 

= 16 (g C/g chlor/day ), 

for 90 < I0 d 180 g cal/cm2/day 

These two relations cover the period when 

a genuine maximum should occur. For 

I0 < 90, the maximum will be at the surface and is given by, 

p,,,,, = 0.48 10 exp ( - &1/90 ) , 

for I0 < 90 g cal/cm2/day . 

Comparing these values with the in situ Cl” 

results collected at the Fladen Ground in 

the northern North Sea (Steele and Baird 

1961) gives the relation shown in Figure 5. 

A part of the variability can be attributed 

to the deviation of natural light from the 

seasonal average . The general-trend for the 

observed values to be lower than the theoretical might be explained as the effects of 

respiration which is 

theoretical estimate. 

not included in the 

A similar comparison can be made with 

in situ Cl4 data collected in the Sargasso 

Sea ( Menzel and Ryther 1961). The obscrvcd range in p,,, is from about 20-30 

g C/g chlor/day in the winter to about 5% 

70 g C/g chlor/day in summer. The corresponding range of light values is 220-580 
ENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS 145 

0’ I - - ’ 1 1 * 1 ’ ’ 

JFMAMJJASOND 

FIG. 8. Seasonal changes in the carbon:chlorophyll ratio, c, for various levels of nutrient limitation, f ( N ) , expressed as a proportion of the optimum. 

Figure 10, the theoretical values of c for 

various degrees of nutrient limitation, -f ( N ) , 

are shown in Figure 8. Whereas light 

changes vary the ratio by less than twice, 

the nutrient changes may bc cxpccted to 

produce much larger variations. The observations in or near the North Sea have been 

described previously (Steele and Baird 

1961, 1962b). G enerally, when the depth 

distribution for a given occasion or season 

provides a fairly wide range of values of 

carbon and chlorophyll, it is possible to 

obtain a regression which gives an estimate 

of the ratio, c, and also an estimate of 

detrital carbon. For the other occasions 

when there is insufficient spread, the average of the chlorophyll and carbon values 

together with the “detritus” value from the 

nearest sampling dates are used to construct 

a ratio. With these values of c and the appropriate radiation, equation ( 14) provides 

an estimate of f(N) for each set of observations. These estimates can then be compared with the nutrient cycles. The calculations are given in Table 1. 

For both Fladen and Loch Nevis there 

is a gcncral corrcspondencc between the 

higher summer values of c and the lower 

nutrient levels at the surface. The summer 

ratios, however, are very much higher at 

Fladen than in Loch Nevis, Figure 9, and 

this is associated with the much lower production rate at Fladcn than in Loch Nevis 

which in turn is due to the very slow upward transport of nutrients by mixing in the 

former area. In both areas the summer 

values of nitrate are very low and at their 

lowest points arc not significantly different 

according to the limits of -t- 0.3 pg at/L 

given by Strickland ( 1958). On the other 

TABLE 1. Calculated nutrient factors, f ( N) and the comparison with observed surface nutrient 

concentrations, especinlly phosphate 

-z-A 

27 III 1 IV 19IV 7v 31 v 11 VII 2 VIII 51X 2X 11 XI 

-____ - -~. -.._-- --. - -. - 

Fladen 

ZN) 

76 23 76 76 145 145 260 260 70 40 

0.32 1.11 0.42 0.46 0.24 0.22 0.11 0.09 0.29 0.50 

Phosphate (pug at/L ) 0.72 0.56 0.56 0.42 0.17 0.15 0.06 0.04 0.14 0.43 

Nitrate ( pg at/L ) 11.2 4.3 0.3 0.4 0.4 0.0 0.2 5.6 

f( N)/Phos. 0.4 2T 0; 1.1 1.4 1.4 1.8 2.2 2.5 1.2 --- _.~_-- -~- - 25 II 10 IV 12 v 14 VII 10 VIII 30 x 7 XII --- -. .- __---____ ~~~ ____-~~ ..- ~ 

Loch Nevis 

ZN, 

92 30 32 74 74 51 293 

0.22 0.96 1.10 0.41 0.37 0.39 0.07 

Phosphate ( pg at/L ) 0.65 0.60 0.45 0.30 0.23 0.60 0.58 

Nitrate ( pg at/L) 7.2 6.2 2.0 0.8 0.1 5.4 

f( N)/Phos. 0.3 1.6 2.4 1.4 1.6 0.6 07 

-__-- - -- -- --- .- -- -~ 17 II 17 TII 28 1V 27 V 25 VI 22VIL 17 VIII 23 IX 2 X 25 XI - ----- - --__-. - -.~-__ _ 

Abercleen Bay 

ZN) 

213 182 182 88 88 88 47 47 47 213 

0.09 0.11 0.19 0.40 0.38 0.34 0.55 0.43 0.43 0.09 

Phosphate ( ,ug at/L ) 0.80 0.76 0.56 0.38 0.53 0.32 0.50 0.54 0.63 0.65 

f( N)/Phos. 0.1 0.1 0.3 1.1 0.7 1.0 1.1 0.8 0.7 0.1 -c - -__-. - _._ __ .-. --. -- - -- .- -- -- ~__ - _..- 
146 J. H. STEELE 

3OOr /’ 9 FLADEN 

I’ 1, 

O’, 11 I 1, , , , , , , F U A UJJASOND 

loo- 

-+--0 

‘JFUAUJJAS 0 N 0 

3 ABERDEEN 

BAY 

FIG. 9. Comnarisons of the carbon: chloroDhvl1 

ratios deduced from observation (-•-) with th’hdsc 

derived from theory using a fixed f ( N ) /phosphate 

relation (-o-) . 

hand phosphate is much more plentiful in 

Loch Nevis than at Fladen and so may be 

a better index of the availability of nutrients from the lower waters. Table I 

shows that for these two areas, excluding 

winter, the ratio f ( N )/phosphate varies 

very much less than either c or f ( N ) . On 

this basis f( N ) may be defined as 

f (N) = 1.7 x phosphate, 

for phosphate < 0.6 Jug at/L ( 15) 

= 1.0 

for phosphate > 0.6 pg at/L 

This has the required form for f ( N ) and 

from ( 15), “theoretical” values of c can be 

derived which, in Figure 9, are compared 

with those deduced from observation. There 

is general agreement over a wide range of 

values except for the “winter” data and this 

may be attributed to etiolation due to very 

low available light. 

For the third area, Aberdeen Bay, it is 

obvious from the results in Table 1 and 

Figure 9 that the agreement is poor. Apart 

from the first and last values of c which 

may bc attributed to etiolation, the main 

disagreement is in the spring, corresponding roughly with the disagreement in the 

photosynthesis-chlorophyll comparison, Figure 7, ‘and perhaps for the same reason. 

For summer and autumn there is approximate qualitative agreement in the form of 

the changes suggesting that a different numerical relation for f ( N ) might be applicable for such very different environmental 

conditions. 

DISCUSSION 

From equations ( 12), ( 13), and ( 14), 

given the incident radiation I0 and a value 

for the effect of nutrient limitation f(N), 

it is possible to predict the photosynthetic 

rate per unit of chlorophyll and also the 

carbon : chlorophyll ratio in the plants. The 

basic postulates are very simplified but 

they contain some of the main features of 

the physiological changes shown by plants 

in culture. Similarly the comparisons with 

observations do not show exact agreement 

but the general correspondence excluding 

very shallow water would suggest that this 

theoretical approach may be a possible first 

approximation. 

In particular, the relation of f ( N ) to surface phosphate for Fladen and Loch Ncvis 

is not intended to prove that phosphate is 

the limiting factor but rather that, in the 

particular circumstances of a euphotic zone 

supplied with nutrients by mixing from below, phosphate can be an index of the degree of limitation exerted by the rate of 

mixing. It is relevant that equation (15) 

is very close to that used by Riley ( 1946) 

for similar conditions on Georges Bank. But 

the lack of generality in this relation is 

shown by the divergence between theory 

and observation for a very shallow region, 

Aberdeen Bay, where nutrient supplies cannot come from waters below the euphotic 

zone, Further, in another paper it will bc 

shown that for the winter bloom in the 
ENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS 147 

FIG. 10. The total daily radiation (IO) and the 

radiation per hour of daylight (I&) for three 

latitudes. 

Sargasso Sea (Menzel and Ryther 1961) a 

relation between f ( N) and nitrate is most 

suitable. Such a lack of generality seems 

reasonable since a nutrient concentration 

does not necessarily reflect the internal 

state of the cell but rather the instantaneous 

balance between the demands of the cell 

and the particular method of supply by the 

environment. 

Although these theories arc tentative and 

it is hoped to test them for a wider range 

of environments, it may be of interest to 

deduce certain of their more gcncral implications. - 

Light data enter these formulae in two 

ways : as the total daily radiation, IO, in the 

photosynthesis : chlorophyll relation, and as 

the average hourly radiation IO/h in the 

carbon : chlorophyll ratio. Both these forms 

are shown in Figure 1O.l The region IO/h 

< 15, where the plants can adapt to light 

changes, includes only 6 months at 60”N, 

about 10 months at 42”N and all the year 

at 32”N. In deeper water these intervals 

correspond approximately with the producl The data for GOoN is based on the average of 

seven years data kindly supplied by the Metcorological Office from records for Lcrwick in the 

Shetland Islands; that from 42”N is taken from 

Kimball ( 1928 ) ; the values for 32”N are averages 

of two years data at Bermuda kindly supplied by 

Dr. David Menzel. 

2 ’ 

I I I I I 1 

loo 200 xx) 4oc 500 600 700 800 900 

RADIATION (1) (9 cal/cm~dq) 

FIG. 11. A comparison of the photosynthesislight relation used by Ryther and Yentsch ( 1957 ) 

with those derived from equation ( 12) for a range 

of values of IO. 

tive periods for these latitudes (Steele 1956; 

Ryther and Yentsch 1958; Menzel and 

Ryther 1961). From ( 13)) the photosynthetic rate in carbon units under 1 m2 is 

S co Pm h-f lN) PdX= & for IO/h > 15 0 

Since this dots not contain IO, the gross 

productivity considered as percentage uptake of carbon is independent of the seasonal light changes during the main productive seasons but depends on h the 

length of daylight. 

The opposite conclusion applies for photosynthesis per unit of chlorophyll. From 

equation ( 12) 

S 00 

0 

p&= (1-;;‘a, IO 

in chlorophyll units which is independent 

of h but is directly proportional to IO. In 

this way ( 12) differs from the empirical 

curve used by Ryther and Yentsch ( 1957). 

Figure 11 shows the comparison between 

their curve and those derived from ( 12) 

for 8 range of values of IO, In temperate 

regions where IO may vary from approximately 200 to 400 g cal/cm2/day during the 

productive season, the Ryther-Yentsch curve 

is a rough average of the seasonal range 

suggested by the theory. In tropical regions 

this average curve would appear to be too 

low for summer conditions, Figure 10, by at 

least a factor of two ( Menzel and Ryther 

1961) . 
148 J. II. STEELE 

The theoretical curves in Figure 11 can 

be used to estimate photosynthesis in a water column knowing k, I,, and the chlorophyll concentrations at appropriate depths. 

When the chlorophyll is approximately constant in the layer O-x and has an average 

Ch then from ( 12), the photosynthesis, P,, 

in this layer is 

a& x P, = - 

k S o 

P d.5 

0.24 Ci, IO 

= 

k exp ( -2e-““ ) - K2 1 

If the light intensity at depth x is sufficiently low so that e-k8 is small, then the 

photosynthesis in the euphotic zone is 

P= o’22 ” I0 (g C/m2/day) k (16) 

This formula provides a simple and quick 

method for calculating gross productivity. 

For the variations in chlorophyll content 

of the phytoplankton, the main general consequence of the theory is the very wide 

range in the carbon : chlorophyll ratio 

which it predicts. Variations by a factor of 

10 to 15 are comparable to the changes that 

would be defined as a plant bloom. Further, the theortically expcctcd timing of 

these variations is similar to the expected 

pattern of such blooms in temperate latitudes. Figure 12 shows a hypothetical seasonal cycle for c-l, which indicates the 

changes that would appear in the chlorophyll concentration even if the carbon remained constant. The winter values arc 

based on a ratio of 1 : 200 corresponding 

to the effects of etiolation in the dark. The 

spring and autumn peaks indicate the consequences of moderate light and a good 

supply of nutrients. The summer minimum 

is the result of strong light and a reduction 

by factor of 7 due to nutrient limitation. It 

is relevant that the spring-summer-autumn 

changes correspond to the typical diatomdinoflagellate-diatom sequence, so that variations in the ratio may be linked to the 

main features of species succession. 

Figure 12 suggests that part of the chlorophyll cycle observed in the sea may indicatc changes in productive rate rather than 

0’ . ’ ’ - ’ ’ * . ’ ’ ’ ’ JFUAUJJASOND 

FIG. 12. A hypothetical seasonal cycle for the 

chlorophyll: carbon ratio which illustrates the main 

theoretical consequences of the typical light and 

nutrient cycles in temperate latitud-ei. 

changes in biomass, This could have important consequences for the assessment of 

the effects of grazing since the apparently 

very low levels to which the herbivores can 

graze down the plants may be partially an 

artifact caused by the very high carbon : 

chlorophyll ratios. Similarly, a large range 

in this ratio could have a dominating effect 

on the net production defined as photosynthesis minus respiration. If the probable 

assumption is made that respiration is rclatcd to the carbon content of the plants 

(r = g carbon respired/g plant carbon/ 

day), then at the depth of maximum photosynthesis (I = 0.5 IO) during the main productive seasons, from (13) 

respiration rate r 

max. phot. rate = 0.066.h.f (N) 

As an example, if r = 0.05 and h = 15, then 

for f(N) = 1.0 th c respiration is 5% of the 

maximum photosynthesis, but for f( N ) = 

0.15 the respiration is 33% of the maximum 

photosynthesis. During the 15 hr when 

photosynthesis is taking place the range 

would bc 3% to 20%, and this is roughly 

that found in Cl4 experiments with natural 

populations ( Stceman-Nielsen and Hansen 

195913; Steele and Baird 1961). 

Lastly, and very hypothetically, another 

possible consequence of these theories concerns vertical changes at a given time and 

place. Previously it has been assumed that, 

in the depth zone studied, mixing and sinking were sufficient to prevent the plants 

from being isolated from the surface for 

long periods. This assumption may not 

hold at greater depths in very stable therm- 
ENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS 149 

oclines ( Ryther and Menzel 1959). Under 

these conditions, the changes from a welllit nutrient-poor surface layer downwards 

to the darker, nutrient-rich waters are very 

similar to the temporal changes from summer to winter. Thus a similar sequence in 

adaptation might be a partial explanation 

of the chlorophyll maxima generally found 

at the foot of the euphotic zone in these environmental conditions. In a previous paper 

(Steele and Yentsch 1960) calculations suggested that these chlorophyll peaks could 

not be explained solely by the accumulation 

of plants due to density changes in the water, so that a “biological” explanation was 

needed. A possible answer was obtained 

from experiments which showed that laboratory cultures could decrease their sinking rate when undergoing changes similar 

to those at the foot of the euphotic zone. 

It is likely, however, that several associated 

physiological changes may occur (Harvey 

1953; Vaccaro and Ryther 1960) including 

an increasing chlorophyll content that 

would provide an additional explanation of 

these very marked peaks. 

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