### 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 asfunctions 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 avery 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,
asanindex ofproductivity and asanindex 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 afixed relation between light and photosynthesis, Ryther and Yentsch (1957) deduced a formula which estimated the gross production from aknowledge of the incident light, the extinction coefficient and the chlorophyll a concentration. The main disadvantage of this method isthat a fixed light/photosynthesis relation doesnot 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,asanindex ofpopulation, 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 4:1to 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 bewidespread changes in this ratio for different regions and also for different seasons,but without an understanding of the factors which control these changes the useofchloro,phyll asapopulation index is lessthan adequate. In laboratory cultures these two effects, light adaptation and changes inthe 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 asatentative first step.

RELATION BETWEEN LIGI-IT INTl3NSITY
AND* PHOTOSYNTIIE~C RATE
The shape ofthe curve relating light and photosynthesis hasbeen the subject ofconsiderable study. It is obvious that alinear relation holds only for lo,w light intensities and that asthe 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 isthe light intensity and a is a constant which dctermincs the initial 137138 J. I-1. STEELE

4Pm

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

slope ofthe curve at low light. By varying (E,different curves are obtained (Fig. 1) whose changes could bethought to imitate the effects of“light” and “dark” adaptation.

This curve hasaserious disadvantage for marinc ecology. From (I) ptends asymptotically to pmas I tends to infinity, In the
sea,however, it appears that at high light intensities /p decreases again so that the

. maxrmum, pm,occurs atafinite 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 alsofrom in situ Cl4 experiments (Currie 1958;Rodhc 1958;Steele and Baird 1961). Theexperiments ofRyther and Menzel (1959) provide the most suitable data since they co,verawide range of light intensities (Fig. 2). The samples were taken from three depths, 0,50, and 100m, in the SargassoSeacorresponding 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 isthis feature which needs to be incorporated in any formulation ofthe light/ photosynthesis relation.

The following expression

P= np,,,Ie’-“I (2)

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

# 100

50

# I

-// WorlJ

.

. 50 I% 10

0l.'flLYi - l

. .

-. 0 2 4 6 8 IO

IClo’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 tothe inhibition ofphotosynthesis by photo-oxidation. However, for land plants it hasbeen suggcstcd (Rabinowitch, p.874) that the midday suppression of photosynthesis isnot simply explainable in terms of light inhibition but may be a more inhcrent diurnal rhythm.

This rhythm is observed in the seaand 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 CL4uptake (Doty and Oguri 1957). It seemslikely that seasonal and depth variations in photosynthesis and carbon :chlorophyll ratio will be complicated by thcsc diurnal effects although Doty (1959) suggeststhat 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 aquantitative cxpression by fixing values for the constants. There aretwo constants involved, aand “pnL, and these depend on the photosynthetic yield at low light intensities and at optimum light intensity.

At low light intensities it isprobable 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 ofchlorophyll (3)
This has been formulated by Rabinowitch (1945, p. 1029) in terms of the maximum quantum yield. Recent determinations of this factor suggest avalue between %to l/s (Duysens 1956) and using a mc,an of % gives avalue for 0!of
LY

= 4.10m4 (g C/lux/hr/g chlor) (4)
Steeman-Nielsen and Jensen (1957) derive

avalue 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 arelimiting, but the ability of the phytoplankton cells to assimilate certain compounds. Myers (1953) in kinetic studies ofChlorella pyrenoidosn states that “p, is an inherent characteristic of its internal biochemical machinery.

. . .The rate limiting process LIGHT INTENSITY

LtGHT 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 besomecellular 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, isthat given by Myers, pltl.= 0.08(gC/g plant C/hr) (5) To relate (4) and (5) in terms of the relation given by (2), the ratio cofcarbon : 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= Qp, f31 Therefore, from (6) and (7)

a c=-
ap,,e (7)

(8)

This shows that the carbon :chlorophyll ratio depends on the constant CIwhich in turn determines the degree oflight ordark adaptation. Increasing light adaptation produces increases in cand socorresponds to the generally expected decrcasing proportion ofchlorophyll in the cells. The consequences are shown by Figure 3in terms140 J. I-1. STEELE

FIG. 4. The cffccts of diurnal light variation on the depth distribution of photosynthesis (see text )

.

ofcarbon and chlorophyll. For the former, the maximum remains the same but the slope at low light intensities varies, for the latter the slope isunchanged by adaptation but the maximum varies, These curves are similar in principle tothose 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. Asasimple means of imitating the general effects of diurnal changes, it will be supposed that the light increases linearly from dawn tomidday and then decreases linearly to sunset. Equation (2) can then be integrated to give the average photosynthetic rate, r),corrcsponding tothe average light I, 

# +k$Il- (1+2aI) eezar’ 1 (9)

The effects of this in the seacan be found using the usual relation

where k isthe extinction coefficient and I0 isthe surface intensity. Figure 4shows (2) and (9) plotted against an arbitrary depth scale. Also since a and I (or I) always

occur together asnI, this scale isshown on the right-hand side. It is apparent that except for high values of u1the 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 seasurface sothat there is adecrease near the surface, but the surface is not usually sofar 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%ofthe surface light but someshading of the surface bottles may have decreased the inhibition at this level. Steeman-Nielsen and Jensen (1957) give ageneral curve similar to Figure 4in which the maximum is at a depth where the light is between ‘h and 1/3of the surface intensity. Sorokin, 

### etal. (1959) alsofound the maximum between 30% and 50% of surface light, and the other studies suggest asimilar 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 bestrictly 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. Iwill betaken

as the average light intensity during the daylight hours. The only change rcquircd isin the numerical value ofp, and by comparison of (2) and (9) it canbeshown that

-- p, = 0.82

### pm (10)

sothat in future (2) will be used with

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

. The application ofthe relation aI0= 2to populations in acertain 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 canbeobtained. For Chlorella, ratios of 8 : 1 and 1,600 : 1 have been found (Mimer 1953). Fogg (1959) has shown that, asaculture becomes nitrate deficient, the dry weight :chlorophyll ratio goesfrom 75:1to 910:1. Steele and Baird (1962a), using the samemethods 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 28:1respectively; thereafter the ratios increased continuously asthe cultures aged. In the seavery 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). Aminimum value of23:1was found for very favorable conditions in the North Sea (Steele and Baird 196213). On this basis aminimum ratio of 20:1will be usedfor natural conditions. With this value the minimum light intensity for which adaptation isstill 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 = 1gcal/cm”/hour.
Thus a= 0.48gC/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 asunits, the maximum photosynthetic rate becomes pp,

.h where h is the length ofdaylight in hours.

NUTRIENT LIMITATION ON PHOTOSYNTHETIC

RATE Sofar the role of nutrient limitation has been ignored, but it isapparent that in the
sea,the lack ofnutrients must beadominant factor in restricting production. Yet it has always been difficult to seehow this operates in the sea. The success of the Ryther and Yentsch (1957) formula for production in terms oflight 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, aresimilar tothe changes in chlorophyll per unit cell volume. He suggeststhat decrease in the latter iscaused by nutrient limitation. The use of chlorophyll :particulate phosphorus and chlorophyll :carotenoid ratios as indices of the chlorophyll content of marine phytoplankton in the seaand in cultures suggest that in both situations there canbeawide range ofvalues 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
awide 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 (Harvey142 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

onphytoplankton, these general features of ecological and experimental results will bc converted into the strict assumption that nutrient limitation doesnot change thephotosynthesis :chlorophyll relation but operates by varying the carbon :chlorophyll ratio. From (2), (3), and nIo = 2,

p= CY Iexp (-21/I,) (gC/g chlor/day) (12)
Since this does not contain pmthe simplest way to imitate formally the preceding hypothesis isto 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 asameasure ofthe degree ofnutrient limitation and the obvious choice would appear to be a nutrient concentration in the water. An apparent indication from cultures ofNitzschia 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 asan index for all latitudes and all seasons. Not only are there varied opinions concerning which substances are of most importance aslimiting factors (Daisley 1957; Droop 1957; Ryther and Guillard 1959)) but it isnot necessarily true that the limiting effects inside the plant cells will keep in stepwith 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 asageneral function fPv1 which will be supposed to decrease with

some nutrient concentration, N. The comparison oftheory 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 beconsidered asanindex ofthe effects of nutrient limitation for a certain

area. Incorporating this relation, and also nIo III2,in (2) and (11) gives
2PmWW ;P= IO exp (L--fW&)

0.132hf(N) I =I

IO exp (l-WOO), (g C/g C/day) (13)

aIO c=2p,ehf(N)
1.34I() =-, (gC/gchlor) 

## hfW)

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 isvery little temperature effect onthe photosynthetic rate when light is limiting. That is,it may be assumed that the photosynthetic mechanism assuch istemperature independent. In strong light, on the other hand, when non-photosynthetic mechanisms

are limiting there appear to bestrong temperature effects in cultures, with Qlo probably near to2. It isinteresting to note that

on the above reasoning, a!would be unaffected and p, would bc the temperature dependent factar. 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 tosomeextent becancclled out by adaptation to different climatic regions. Further, even with Q1o= 2, temperature could account for only afraction of the observed changes. Since it is difficult to choose a correct relation for the temperature dependence and since this may be comparatively smallENVIRONMENTAL 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 etiolated 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 inwhich the average light is very much lower. This means that the plants are well below the compensation level oflight where photosynthesis balances respiration (Sverdrup 1953). It seemsvery likely that a similar effect of etiolation should result under these conditions. Some of the data to be presented later suggest this but it isnot possible to give adefinite 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 isto discover whether the general patterns rather than the numerical values agreewith 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 seainclude “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 (gC/g chlor/day ).

terms of chlorophyll can be deduced from (12) taking I = %IO. Then, for the North Sea,Figure 10,

pmas= 0.08810(gC/g chlor/day )

, for I0B 180gcal/cm2/day

= 16(g C/g chlor/day ), for 90< I0d 180gcal/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,,,,,= 0.4810exp (- &1/90 )

, for I0< 90gcal/cm2/day

. Comparing thesevalues 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 asthe 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 gC/g chlor/day in the winter to about 5% 70 g C/g chlor/day in summer. The corresponding range of light values is220-580ENVIRONMENTAL 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 ofnutrient limitation, -f (N)

, are shown in Figure 8. Whereas light changes vary the ratio by lessthan twice, the nutrient changes may bc cxpccted to produce much larger variations. The observations in ornear the North Seahave been described previously (Steele and Baird 1961, 1962b). Generally, when the depth distribution for agiven occasion or season provides a fairly wide range of values of carbon and chlorophyll, it is possible to obtain aregression which gives anestimate 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 datesareusedtoconstruct

aratio. With these values of cand the appropriate radiation, equation (14) provides

an estimate off(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 atthe surface. The summer ratios, however, are very much higher at Fladen than in Loch Nevis, Figure 9, and this isassociated with the much lower production rate at Fladcn than in Loch Nevis which in turn is due to the very slow upward transport ofnutrients by mixing inthe 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 (pugat/L ) 0.72 0.56 0.56 0.42 0.17 0.15 0.06 0.04 0.14 0.43 Nitrate (pgat/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 (pgat/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 (,ugat/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 afixed f(N)/phosphate relation (-o-)

.

hand phosphate is much more plentiful in Loch Nevis than at Fladen and somay 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 lessthan either c or f(N)

. On this basis f(N) may be defined as

f (N) = 1.7x phosphate, for phosphate < 0.6Jug at/L (15)

= 1.0 for phosphate > 0.6pgat/L

This has the required form for f(N) and from (15), “theoretical” values of ccan be derived which, in Figure 9, are compared with thosededuced from observation. There is general agreement over awide 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 9that the agreement ispoor. 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 adifferent 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 avalue 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 beapossible first approximation. In particular, the relation off(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 ofaeuphotic 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) isvery close to that used by Riley (1946) for similar conditions onGeorges Bank. But the lack of generality in this relation is shown by the divergence between theory and observation for avery 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 theENVIRONMENTAL 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 stateofthe cell but rather the instantaneous balance between the demands of the cell and the particular method ofsupply by the environment.

Although thesetheories arctentative and it is hoped to test them for awider range of environments, it may be of interest to deduce certain of their more gcncral implications. - Light data enter these formulae in two ways:asthe total daily radiation, IO,in the photosynthesis :chlorophyll relation, and as the average hourly radiation 

### IO/h in the carbon :chlorophyll ratio. Both theseforms

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 10months at 42”N and all the year at 32”N. In deeper water these intervals correspond approximately with the produclThe 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) (9cal/cm~dq)

FIG. 11. A comparison of the photosynthesislight relation used by Ryther and Yentsch (1957) with those derived from equation (12) for arange of values of IO.

tive periods for theselatitudes (Steele 1956; Ryther and Yentsch 1958; Menzel and Ryther 1961). From (13)) the photosynthetic rate in carbon units under 1m2is 

# S co Pmh-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 ofdaylight.

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 8range of values of IO, In temperate regions where IOmay vary from approximately 200to400gcal/cm2/day during the productive season,the Ryther-Yentsch curve is a rough average of the seasonal range suggested by thetheory. In tropical regions this average curve would appear to be too low for summer conditions, Figure 10,by at least afactor of two (Menzel and Ryther 1961)

.148 J. II. STEELE

The theoretical curves in Figure 11 can beusedto estimate photosynthesis in awater column knowing k, I,, and the chlorophyll concentrations at appropriate depths. When the chlorophyll isapproximately constant in the layer O-xand has an average Chthen from (12), the photosynthesis, P,, in this layer is
a& x P,= - 

# S
k oPd.5

0.24Ci,IO = k exp (-2e-““ ) - K2

# 1

If the light intensity at depth x is sufficiently low sothat e-k8is small, then the photosynthesis in the euphotic zone is

P= o’22” I0 (g C/m2/day) k (16)

This formula provides asimple and quick method for calculating gross productivity. For the variations in chlorophyll content ofthe phytoplankton, the main general consequence of the theory is the very wide range in the carbon :chlorophyll ratio which it predicts. Variations by afactor of 10to 15arecomparable tothe changes that would be defined asa plant bloom. Further, the theortically expcctcd timing of these variations is similar to the expected pattern of such blooms in temperate latitudes. Figure 12shows ahypothetical 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 tothe effects ofetiolation in the dark. The spring and autumn peaks indicate the consequences of moderate light and a good supply ofnutrients. The summer minimum isthe result ofstrong light and areduction by factor of7due to nutrient limitation. It is relevant that the spring-summer-autumn changes correspond to the typical diatomdinoflagellate-diatom sequence, sothat variations in the ratio may be linked to the main features ofspecies succession.

Figure 12suggests that part ofthe chlorophyll cycle observed in the seamay 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 towhich the herbivores can graze down the plants may be partially an artifact caused by the very high carbon : chlorophyll ratios. Similarly, alarge range in this ratio could have adominating 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 atthe depth ofmaximum photosynthesis (I = 0.5IO) during the main productive seasons,from (13) respiration rate r

max.phot. rate = 0.066.h.f (N)
Asan example, if r= 0.05and h= 15,then for f(N) = 1.0thcrespiration is 5% of the maximum photosynthesis, but for f(N)= 0.15the respiration is33%ofthe 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 ofthese theories concerns vertical changes at a given time and place. Previously it hasbeen 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 atgreater depths in very stable therm-ENVIRONMENTAL CONTROL OF PHOTOSYNTHESIS 149

oclines (Ryther and Menzel 1959). Under these conditions, the changes from awelllit nutrient-poor surface layer downwards to the darker, nutrient-rich waters arevery similar to the temporal changes from summer to winter. Thus asimilar sequence in adaptation might be a partial explanation of the chlorophyll maxima generally found atthe foot ofthe euphotic zone in these environmental conditions. In aprevious paper (Steele andYentsch 1960) calculations suggested that these chlorophyll peaks could not beexplained solely by the accumulation ofplants due to density changes in the water, sothat 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 islikely, however, that several associated physiological changes may occur (Harvey 1953; Vaccaro and Ryther 1960) including

an increasing chlorophyll content that would provide anadditional explanation of these very marked peaks.

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