[Advances in Ecological Research] Advances in Ecological Research Volume 3 Volume 3 || The Production of Marine Plankton

The Production of Marine Plankton J . E . G . R A Y M O N ' I

Department of Oceanography. University of Southampton. England

I . Introduction ...................................................... I1 . Phytoplankton Production ..........................................

A . Methods of Estimating Primary Production ........................ B . Factors affecting Primary Production .............................

1 . Light ...................................................... 2 . Temperature ................................................ 4 . Nutrients - Phosphate and Nitrate ............................ 6 . Minor Nutrients ............................................. 6 . Organic Requirements .......................................

C . Production - Temperature and Stratification ...................... I11 . The Standing Crop of Phytoplankton ................................. IV . Phytoplankton Crop and Annual Production .......................... V . Grazing by Zooplankton ............................................

VI . Zooplankton ...................................................... A . Methods for Estimating the Standing Crop of .Zooplankton ........... B . Regional Crop Assessments of Zooplankton ......................... C . Rate of Zooplankton Production ......................... .-. ...... D . The FeedingofZooplankton ..................................... E . Alternative Food Sources for Zoopla.nkton. ........................ F . Zooplankton - Quantitative Food Requirements . . . . . . . . . . . . . . . . . . .

VII . Conclusion ........................................................ References .............................................................

3 . salinity ....................................................

117 120 120 126 126 133 134 136 138 140 147 165 167 160 168 168 170 178 182 186 188 189 191

I . INTRODUCTION

Production in the marine environment must depend as in any other eco-system on the synthesis of organic matter of high potential chemical energy from inorganic materials of low potential energy . There are only two such primary autotrophic forms of production occurring in the marine environment . Firstly there are the autotrophic bacteria which by relatively simple chemica.1 reactions such as oxidations obtain energy to synthesize complex organic matter . Although our knowledge of the distribution of bacteria in the sea is limited, it appears that the contribution made by these autotrophic bacteria by chembsynthesis must be very small (cf . Steemann Nielsen. 1960) . Krir is (1963) considered that in a special region such as the Black Sea. such production might be very E 117

118 J. E . Q. RAYMONT

significant. However, Sorokin (1964a) points out that the main autotrophic bacteria are probably those oxidizing H,S to sulphate. These are only abundant at the boundary in the Black Sea between the oxygenated and de-oxygenated layers. Even in such an atypical sea as the Black Sea, autotrophic chemosynthesis makes only a small contribution to overall production.

The second source of autotrophic production, the photosynthetic activity of green plants, is overwhelmingly the more important. With solar radiation the plant can build up from carbon dioxide, water and simple inorganic compounds the complex organic materials of high potential energy. Some of this organic material, when synthesized, might be liberated in dissolved form into the sea water. In addition, by death and decomposition of plankton much larger amounts of dissolved organic substances are released to sea water. These dissolved organic materials can be utilized by bacteria, fungi and Protista so synthesizing particulate living matter, which can be used as food, and thus contribute to the biomass of marine plankton. But the production of such dissolved organic substances must depend in the first case on autotrophic synthesis which is due essentially to the photosynthetic activity of plants. Any consideration of production in the sea therefore, as on land, immediately focuses attention on the plant life, in this case of the oceans.

The marine plankton may be regarded as drifting and floating organisms whose existence is independent of the sea bottom. The community may be thought of as consisting of the green plants, the phytoplankton, and the animals, the zooplankton, together with bacteria, yeasts, fungi and other similar organisms. There is a continuous flow of energy through the marine eco-system and it is relatively easy to en- visage the transfer of energy through the primary production of the phytoplankton to the herbivorous zooplankton and thence to the carnivorous zooplankton and nekton. Even in the plankton itself the food web is complex, and there is also the interchange of energy between the plankton and the nekton, and with the various divisions of the benthos. Although it is artificial, therefore, to separate the plankton from the remainder of the marine community, for the purposes of this review production of plankton will be examined as a separate entity.

It is misleading to consider primary production in the marine environment by the phytoplankton without paying some attention also to those plants which occur in shallow waters fixed or lying on the bottom, and which may be referred to as the benthic plant population. These benthic plants, either as living or dead material, are swept into the waters above the bottom and thus may contribute significantly to the food of planktonic animals. The benthic plants may be roughly

THE PRODUCTION OF MARINE PLANKTON 119

divided into the macrobenthic plants which are the typical large seaweeds which occur fixed to rocks around the coast, particularly in temperate regions of the world, and the microbenthic algae. The fixed seaweeds appear to form dense forests in regions where they are abundant, and it might be felt that they make a very appreciable contribution to the production of organic matter in the 8883 . Equally conspicuous in certain shallow marine regions are a few species of flowering plants, such as Zostera, Ruppia, and Thalausia, which grow successfully in fairly soft bottoms of sandy mud. Less obrious but of considerable importance are the microbenthic algae which occur as single celled diatoms and flagellates on rocks, muds and sands, and also on the fronds of the larger seaweeds.

All plants require light as an energy source for the synthetic process. Benthic forms are thus limited to a fairly shallow layer on the coasts. The macrophytes are especially typical fringi ng the continental shelves in temperate latitudes, but they are relatively uncommon in tropical regions, and do not persist very far into really high latitudes. Around island fringes, especially oceanic islands, the benthic algae have very little foothold, but in shallow areas, constant turbulence and increased turbidity sharply cut down light penetration, thus reducing the level a t which these fixed benthic plants can live. Off north-western Europe macrophytes may persist to a depth of some 30 metres; in clear waters as off California or in the Mediterranean, somewhat deeper.

In shallow, muddy areas such as the sheltered Danish fjords, the fixed algae and Zostera zones may not exceed 10 or 15 metres. Since the average depth of the world’s oceans is approximately 3 800 metres, the very small contribution of benthic plants to the production of the oceans as a whole is only too obvious. Wood (1963a) quoting Braarud suggests that the macrophytes may contribute some 2 94. Ryther (1 963) however has recently suggested that we may be under-estimating the role of the benthic algae in productivity and that they may contribute to the particulate organic matter even some distance offshore.

Apart from macrophytes, the algal microbenthos on the bottom deposit may add significantly to inshore production. Grrantved (1960) has investigated the productivity of microbenthos and phytoplankton in very shallow Danish fjords. For the more productive season March to October phytoplankton production amounted to only approximately a quarter that of the bottom microflora which consisted mainly of benthic diatoms. In a further study Grrantved (1962) has investigated the production of microbenthos on exposed tidal flats. The plant population was again mostly benthic diatoms attached to sand grains, though some plankton cells descended to the bottom and were able to live for a time. There was a marked seasonal variation in production but again the

120 J . E . G. RAYMONT

bottom microflora was far more important than the phytoplankton. In offshore waters, and especially in the open oceans, however, the phytoplankton must be all-important in production.

11. PHYTOPLANKTON PRODUCTION The term production in the oceans is usually restricted to primary

production, the synthesis of organic matter by the phytoplankton. So few parameters of production on the higher trophic levels (e.g. zooplankton, benthos, nekton) are as yet established, that estimates of production are normally restricted to primary production alone. Even here it is only comparatively recently that we have been able to gain a reasonable appreciation of the rates of production of plant material. Rate of production must be clearly distinguished from standing crop of phytoplankton which is the amount of the living plant substance existing under a unit area of sea (e.g. beneath mz) or per unit volume (e.g. m3) a t a particular place at a point in time. Standing crop is itself of great significance, but we shall first discuss rates of production.

A. METHODS O F ESTIMATING PRIMARY PRODUCTION

One of the first methods used for estimating primary production was the so-called oxygen bottle method, which is still widely used. In this kind of experiment a series of bottles filled with sea water and containing a phytoplankton population is suspended at various depths in the sea starting at the surface. The rate of photosynthesis as a measure of plant production is estimated by the rate of change of oxygen. concentration (measured by the Winkler method). Various precautions must be taken such as avoiding shading by a bottle at a higher level in the I water, and ensuring that no loss of gas occurs during the course of the experiment. The change in concentration of oxygen in any bottle (AO,) may be due to several factors which may be expressed as follows:

+ A O , = P -RI -RR, -Rb

where R, = Respiration of plant tissue originally present; R, = Re- spiration of newly formed plant tissue during the course of the experiment; Rb = Respiration of bacteria and any zooplankton. The change in oxygen, apart from that due to bacterial and zooplankton respiration, would thus be an estimate of net photosynthesis. But the amount of oxygen consumed due to the respiration of the plant tissue originally present (R,) and the amount of oxygen consumed by bacteria and zooplankton (Rb) can be estimated by suspending a series of so-called “dark” bottles at the same time and at the same depths as the normal “light” bottles. If the amount of oxygen consumed in a “dark” bottle

THE PRODUCTION O F MARINE PLANKTON 121

is added to the amount of oxygen produced in a “light” bottle, the total amount of oxygen is equivalent to (P - R,). As R, is normally very small in short-term experiments, this total amount of oxygen change is practically a measure of gross photosynthesis. If longer term experiments are employed R, may become considerably larger and the estimate of photosynthesis then approaches a net value again.

One disadvantage of the oxygen bottle method is that the temperatures in the “dark” bottle series may be somewhat different, respiration proceeding at different rates in the “light” and “dark” bottles. Further- more, fat may be synthesized to some extent rather than carbohydrates, particularly by diatom cultures, which will af Fect the amount of oxygen produced. Growth, especially of marine bactwia, tends to be increased by surface, and therefore there may be an almormally high density of bacteria in the enclosed phytoplankton cultures. In any event, probably no population of phytoplankton can live perfectly normally enclosed in a relatively small volume of virtually stationary sea water. But, above all, the most serious disadvantage of the oxygen bottle experiment lies in its comparative insensitivity, especially with low concentrations of phytoplankton as in oligotrophic areas of the ;sea; under such conditions the amount of oxygen produced over a moderately short-term experiment may be quite small (cf. Currie, 1959, 1962). The technique is also unsuitable for productivity experiments in very rich, highly polluted, inshore waters, especially with high bacterial populations.

Other methods have been tried for estimating the rate of primary production in the marine environment. Changes in the quantities of nutrients such as nitrate and phosphate, which are essential for the upbuilding of cell tissue, have been used as a measure of plant growth. One of the main difficulties is that unless a steady state in water movements can be assumed, any large scale lateral exchange of water through the area may introduce major errora in calculations. Vertical exchange of water may also be important. In a deep oceanic area the extent of vertical mixing may be assessed so that any nutrient brought into the photosynthetic zone from deeper water may be included in the calculations. In shallow water it may be possible to integrate the whole changes in nutrient from surface to bottom, but the leaching of nutrients from the bottom deposits can be significant. Perhaps the greatest difficulty with using nutrient changes as a measure of production, however, turns on the problem of regeneration. The regeneration of inorganic nutrient materials from organic matter (or mineralization) can be rapid under certain conditions. Investmigations such as those of Harris (1959) suggest that at least a portion of the phosphorus and some of the nitrogen, particularly as ammonia, may be fairly rapidly recycled. Ketchum (1962) suggests that phosphorus may be cycled some 6 or 7 times a year

122 J . E. a. RAYMONT

in the waters of the continental shelf off Woods Hole, and similar determinations for the North Sea over the 7 months of main phytoplankton growth suggest that phosphorus may go through perhaps half a dozen regeneration cycles. Vaccaro (1963) has also pointed to the importance of ammonia in the upper layers being rapidly regenerated and maintaining the cycle of phytoplankton growth. With the possibility of considerable regeneration of nutrients, any estimate of primary production dependent on changes in nutrient level may give only minimal values. These errors were recognized in the early work of Atkins, Harvey and Cooper for the English Channel; nevertheless Cooper (1933) was able to estimate minimal production of phytoplankton for the English Channel over a period of about 5 months from changes in CO,, 0,, phosphate, nitrate, and silicate. The agreement (Table I) is fair except for the case

TABLE I The Theoretical Minimal Production of Phytoplankton in, the

English Channel Calculated on the Basis of Chemical Changes in. the Water (the period of production i s from JanuarylFebruary to July) .

(from Cooper, 1933)

Minimum production of phytoplankton wet weight metric tons per square km. Basis

COZ 0 2

Phosphate Nitrate Silicate

1600 1000 1 400 1600

110

of silicate which probably arises from the rapid recycling of this element. Steele (1956, 1958) has also used the changes in phosphate concentration to calculate the production of phytoplankton on the Fladen (North Sea) ground, where apparently little lateral transport of water occurs. The estimates of production based on phosphate changes and on 14C (vide infra) methods gave fair agreement.

Several workers have used the dependence of photosynthesis on light intensity to establish equations for the rate of primary production. For example, Ryther and Yentsch (1957) suggest that, on average, marine phytoplankton has an assimilation rate of 3.7 g.C/h/g. chlorophyll at light saturation values. They have established the relationship

R k P = - x c x 3.7


for calculating production in a column with a homogeneous distribution of phytoplankton. P = photosynthesis of the population in g/C/m3/day; R = relative photosynthetic rate, dependent on the light surface intensity; C = chlorophyll/m3 in the column. Such a calculation gives only an approximation since the assimilation rate assumed is a mean value for various species. Phytoplankton is very often also markedly stratified rather than homogeneously distributed and there is the difficulty that the existing stock of algal cells must be estimated from the amount of chlorophyll present.

One of the most successful and widely used methods for estimating primary production was developed by Steemann Nielsen (1954) (cf. Steemann Nielsen and Aabye Jensen, 1957). 1-n his technique the radioactive isotope, I4C, is added, as bicarbonate, to a bottle of sea water, the productivity of which is to be measured. The Lotal content of CO, in the water must be known and, assuming that the labelled carbon has been assimilated by the algae, the total amount oS carbon photosynthesized during the period of time may be calculated by determining the amount of 14C present in the plankton when the experiment ends. The plankton is removed by filtration and the amount of 14C measured by the /3 radiation from the plankton retained on the filter. The carbon technique is undoubtedly far more sensitive and iiherefore is of great use in measuring the primary productivity of oligotrophic waters; it avoids the long term experiments necessary with the 0x3 gen bottle technique.

At the same time there are certain difficulties in using this method. For example, it is necessary to assume that “C and the normal isotope

are absorbed at the same rate; Steemann Nielsen has suggested that the error due to isotopic discrimination is not more than 5%. Again, the precise method of filtering, the type of microfilter, and the pressure used for filtration may also be critical in that more delicate phytoplankton cells may be destroyed and EL loss of material encountered. The 14C method may be particularly sensitive to errors of this sort where delicate flagellates form a relatively large part of the phytoplankton population. A difficulty found with the oxygen bottle experiment also applies to the I4C technique, namely that the enclosure of a photosynthetic population in a static volume of sea water does not reflect precisely the conditions operating in the natural environment. Other errors may arise; the time of day in which the estimate is made can be important, since diurnal variations in photosynthetic activity of algae are now recognized, particularly the “afternoon depression” (Doty and Oguri, 1957) which may be especially marked in plankton from warm waters. Difficulties may also be encountered when the algal cells have shells or inclusions of calcium carbonate (e.g. if the phytoplankton is dominated by coccolithophores). Steemann Nielsen ( 1 964a)

124 J. E. 0 . RAYMONT

advocates the use of fuming hydrochloric acid to reduce errors arising from this source. Since “C02 fixation” can occur in darkness and can occur with non-photosynthetic organisms, without any real gain in carbon (Steemann Nielsen, 1960), Steemann Nielsen (1964a) suggests the use of a “dark” bottle; the changes in I4C occurring in the “dark” bottle can then be used as a correction factor for the normal “light” bottle. Perhaps the chief criticism which may be levelled against the 14C technique is that some of the carbon assimilated during the course of the experiment may be used for respiration purposes. The quantity is not known and therefore it is not entirely clear whether the I4C technique measures gross photosynthesis, net photosynthesis, or some measure of photosynthetic activity between these two extreme values. Some workers such as Ryther believe that the value approxiniates to the net photosynthetic rate; Steemann Nielsen believes that with moderate production rates, respiration amounts to about 10% of photosynthesis, so that 14C experiment estimates about 90% of gross production. There is little doubt, however, that the difference between net and gross production varies with the time of year at high latitudes, and also geographically. Thus in oligotrophic tropical waters, net production may be less than 60% of gross production, whereas in high latitudes, during the height of summer, it may be a much higher proportion.

If rates of primary production are to be compared, they must be related to a standard unit of concentration of phytoplankton present in the sea. The measurement of the standing crop of plankton in the sea is a very difficult problem (vide infra). Usually the amount of chlorophyll, as the active photosynthetic pigment, has been used as an approximation of the standing crop of phytoplankton, but this is not constant, varying from species to species and being dependent on the state of nutrition of the individual cell. The chlorophyll content may also change with time of day, light intensity, and with other factors. Chlorophyll and degradation products of this pigment may also occur free in the water and the length of life of such material is still uncertain; the amount of chlorophyll found by the normal filtration and extraction processes may thus be misleading. The precise method of extraction may also affect the amount of chlorophyll; for instance, grinding of the cells during extraction may lead to an increase in the amount of pigment extracted. Clear1y”the concentration of phytoplankton expressed as the amount of organic carbon or of dry organic matter would be 8 much more accurate measurement, but no rapid and accurate method is known for determining either of these quantities. Chlorophyll, therefore, is widely used as an index of the standing crop of phytoplankton.

Any technique which estimates photosynthetic activity may not necessarily be measuring accurately the increase of phytoplankton

THE P R O D U C T I O N O F M A R I N I : P L A N K T O N 125

substance which is the essence of primary production. For example, respiration has already been noted as reducing growth. But there may be excretion of some material in soluble forin which would not appear in 14C measurements. The amount of such “lost” material is usually believed to be small, but Fogg (1963) suggests that the quantity may at times be considerable (vide infra). Other discrepancies between photosynthetic and growth rate may arise. For instance, many nutrients are required for the further synthesis of algal cell substance; the concentration of these nutrients may influence the amount of phytoplankton substance produced, though this is clearly closely related to photosynthetic activity. Ideally, we should measure the actual amount of phytoplankton material synthesized in a given volume of sea water over a period of time, but this again requires rapid and accurate methods for the determination of organic carbon or dry organic matter, and these are at present not available.

Apart from the difficulty of estimating standing crop, the 14C method may be used to measure primary productio I throughout the euphotic zone in the sea, but the precise technique i3 important (cf. Steemann Nielsen, 1964a). Undoubtedly the best determinations are made employing the in situ method by which a seiies of bottles is placed at different depths in the ocean and the light intensity throughout the euphotic zone is also measured. A reasonable method where the time- consuming and difficult in situ method cannot be employed is to place sealed bottles of sea water from each depth on board the research ship, the whole being surrounded by a jacket of ;sea water, and illuminated by fluorescent light sources of known intensity. It is essential, however, to employ glass filters of known spectral transmission; these must be placed above the plankton samples according to the light which they would encounter at their normal depth distribution.

Recently investigations comparing the production of phytoplankton by different techniques have been made. McAllister et al. (1961) enclosed a natural population of coastal phytoplankton in a large plastic sphere sunk just beneath the sea surface. Primary production rates were estimated by oxygen bottle and 14C methods, and showed rather wide differences. Some of the discrepanciea were reduced, if the 14C

method was assumed to measure net photosynthesis, and if in the oxygen experiments the photosynthetic quotient was high (1 -3). Net production of organic particulate carbon was also estimated over three weeks by five methods; 0,-production, 14C, #changes in CO, as revealed by pH, cell counts, oxidizable particulate carbon produced. There was a reasonable measure of agreement, especially witb three of the techniques (cf. Fig. 1). In a later study by Antia et al. (1963) using the same plastic sphere, the 14C method gave good agreement with an estimate of t?

126 J. E. a. RAYMONT

production based on the production of particulate phosphorus. A discrepancy between the 14C and oxygen bottle estimations was believed to be due largely to the 14C method measuring net production whereas the oxygen method measured gross production.

Other comparisons have been made using tank mass-culture techniques by Ansell et al. (1963, 1964). Estimates of production based on

I

1400 - --Values from cell counts

1200 - 1 values from PH 1 Oxidizable carbon increase 0 Radiocarbon uptake

'Oo0-

600-

400 - E

I 2 3 4 5 6 7 8 9 1 0 i 1 1 2 1 3 1 4 1 5 1 6 1 7 1 8 1 9 2 0 2 1 2 2 Time (days)

FIG. 1. The net production of carbon in plastic sphere experiments as measured by five independent methods; (from MoAllister, Paraons, Stephens, and Strickland, 1961).

0, bottle experiments, changes in pH and in phosphate concentration, and packed cell volume obtained after harvesting the algae, were found to show fair agreement.

B. FACTORS AFFECTING PRIMARY PRODUCTION 1. Light

Whatever method is used for estimating primary production, it is clear that photosynthesis is dependent on light intensity. In a typical oxygen bottle experiment such as that of Gaarder and Gran (1927) whereas at a depth of 10m there was no change in oxygen content, at higher levels in the water there was an increase in oxygen content, and a t lower levels a decrease. The depth of 10m therefore in Gaarder and Gran's experiments corresponds to a level where the amount produced by photosynthesis during the course of the experiment (in this caw 24 hours) was exactly balanced by the amount of oxygen consumed by respiration. This depth where no effective production occurs, but where respiratory and photosynthetic activity just balance, has been termed the compensation depth. Its extent will depend on the transparency of


the water. Light is relatively very rapidly reduced in the sea, being partly absorbed and partly scattered. Particlies in the water, whether inorganic or organic detritus, as well as living plankton, all reduce transparency; there is also some dissolved “yellow substance” which absorbs light. Greater light penetration is t,ypical of less productive waters, since algal cells are sparser, but the relatively rapid reduction of light in richer seas is partly due to greater quantities of detritus (cf. Ryther, 1963). The compensation depth is greatly affected by latitude and season, but it is not an absolute value - it will depend aIso on the time of day. At night it does not exist.

Light is absorbed logarithmically in sea water, and even for the clearest oceanic waters about SOYo of the total solar radiation is absorbed in the upper 10m. Although infrared rays are especially rapidly absorbed, even of the visible wavelengths only some 50% remains for the clearest water at 10m depth. Whereas about 1% of incident visible light reaches some 120m in clear tropical oceans, the same reduction to 1% is reached at ca. 50m depth in boreal waters, and in turbid inshore areas the 1 Yo level is reached at depths approaching only 10 or 20m.

TABLE I1 Culture Experiment 22-25 Nwch, 1916

Average Increase in 24 hours (from Bmvder and Bran, 1927)

yo Increase in Cell Numbers

Depth, Oxygen, Lauderia Tlialassiosira Thalaseiosira m cm8/1 glacialis gravida nordenekioldii

0 + 0.20 77 59 10 2 + 0.19 79 58 73 5 + 0.13 70 55 67

10 0 28 34 23 20 - 0.03 0 0 0 30 - 0.05 0 0 0 40 - 0.07 0 0 0

In the oxygen bottle experiments such as those of Gaarder and Gran (Table 11), the decrease in the amount of oxygm produced with increase in depth of the water reflects the rapid reduction in light intensity. These experiments were conducted over a 24-hour period; had shorter term experiments been made during daylight hours only, there would have been greater oxygen production at each depth and the estimated compensation depth would have been greater. Frog the view point of overall primary production, the 24-hour experiment is the most satisfactory. The compensation depth will vary with season in a temperate

128 J . E . G . R A Y M O N T

latitude. Thus the experiment in Table I1 was carried out during the spring; other experiments carried out later in the year, with increasing length of day and greater light intensities, showed the compensation depth much deeper in the water. Other similar experiments such as those of Marshall and Orr (1 928, 1930) who worked on a single species of diatom, Coscinosira polychorda, suggested that whereas in winter, the compensation depth was only a metre or two beneath the surface, during summer it might lie at about 20-30 metres.

One of the most complete studies on the effect of light on photosynthetic activity is that of Jenkin (1937), working with the diatom, Coscinodiscus escentricus. For the English Channel, Jenkin found a compensation depth a t about 45 metres, corresponding to a light intensity of approximately 0.13 g cal/cm2/h. Using the oxygen bottle technique she showed that between this light value and some 1 *8 g cal/ cm2/h (3 5 000 lux), oxygen production, as a measure of photosynthetic activity, increased practically linearly with light energy. At light intensities above this value it continued to rise but at a somewhat lower rate, indicating that some inhibition was occurring; maximal photosynthesis occurred a t a light energy approximating to 7.2 g cal/. cm2/h (of the order of 20 000 lux). Above this intensity, which may be termed the light saturation value, inhibition began to be more obvious and at high light intensities photosynthesis was markedly reduced. These experiments have been confirmed by others. Thus Talling (1960) using Chaetoceros afinis, showed photosynthetic activity to increase linearly from a compensation intensity approaching that of Jenkin to a value of some 5 000 lux; light saturation occurred at a mean value of 25 000 lux. Jenkin’s clear demonstration of inhibition at high intensities shows that even in temperate latitudes about midday during the summer some degree of inhibition of photosynthesis can occur, but this will be confined to algae close to the surface (cf. Fig. 2).

The results of early experiments on primary production such as those of Gaarder and Gran (1927), suggest that some species of diatoms in a mixed phytoplankton population differ in their light requirements. Thus the diatoms Lauderia and Thalassiosira gravida grew best in the upper 2 metres, the latter species probably growing fastest right at the surface. On the other hand, the related species, T. nordenskioldii, appeared to grow best at a depth of 2-5 metres, and presumably had a lower light optimum. Later work, particularly that of Steemann Nielsen and his colleagues, has indicated clearly that different species of phytoplankton have different light optima. Although an average compensation intensity for phytoplankton species of some 0-13 g cal/cma/h, as suggested by Jenkin, appears to be reasonable, the various species exhibit considerable differences in their light optima and saturation


values. But for all of them a similar curve may be constructed for the relationship between photosynthetic activity and light energy. A t low light intensities the photosynthetic rate rises almost linearly with light intensity; a less rapid rise then follows to an optimal value a t light

, Time (h)

FIO. 2. Variation of photosynthetic activity estimated hy oxygen production with depth by the diatom Coscinodkcus ezcentricus in the English Channel; (from Jenkin, 1937 - reprinted from “Plankton and Productivity in the Oceans”, Pergamon Press).

saturation, followed by inhibition at high light intensities (Fig. 3). Ryther (1 956) summarizes his results for various phytoplankton species by stating that species of the Chlorophyta including Dunaliella, Chlamy- domonas, Nannochloris, Platymonas and Carttiria were light saturated a t

Radiant energy (cal crn-2rnin-’1. 400 to 700 rn)L

FIO. 3. The relationship between photosynthesis and 1 ght intensity in phytoplankton, based on the mean curve of Ryther (1956); (from Currh, 1962).


intensities of about 5 000-7 500 lux; diatoms such as Nitzschia, Coe- cinodiscus, and Skeletonema became light saturated at rather higher intensities from about 10 000 to more than 20 000 lux; while species of dinoflagellates (e.g. Exuviella, Gyrodinium, Gymnodinium) were light saturated at much higher intensities of about 25 000-30 000 lux. For all the species investigated, however, inhibition occurred at intensities about 10 000 lux above the light saturation values. Steemann Nielsen and Hansen (1959) have called attention to the different light requirements of phytoplankton from various regions and different depths. Thus they distinguish surface arctic, surface temperate, and surface tropical populations from other phytoplankton assemblages which occur deeper in the euphotic zone at each of these geographical latitudes. The light saturation values differ very considerably for these various groups of species, and the rate of photosynthesis per unit of chlorophyll at light saturation shows very wide discrepancies (compare Fig. 4). It is thus possible to distinguish what may be termed a “sun” plankton, which occurs near the surface and is adapted to relatively high light intensities, from a “shade” plankton which lives towards the bottom of the euphotic zone and is adapted to low light intensities. On the whole, the amount of chlorophyll per cell, or more accurately, the ratio between chloro-

Lux

FIQ. 4. Light intensity and the rate of gross photosynthesis for marine phytoplanltton from different habitats. a = surface plankton; b = plankton from depth corresponding , to 1% of green surface light; 1 = tropical; 2 and 3 = temperate summer; 4 = northern plankton with slight vertical stabilizetion; 6 and 6 = arctic summer; 7 = temperate I winter; (from Steemtmu Nielsen and Hansen, 1969). I

T H E PRODUCTION O F MARINE PLANKTON 131

phyll and carbon, tends to be higher in the E:hade forms. The existence of these shade and sun types of phytoplankton, particularly in the deeper euphotic zones of highly stratified tropical waters, has been noticed recently by many authors, for exam:ple, by Ryther and Menzel (1959). These investigators show that in an area of the Sargasso Sea during winter, when the euphotic zone may approach some 150 metres in depth, the water is mixed and is virtually isothermal to a depth of 400 metres. During this time the phytoplankton at three depths, corresponding to loo%, 10% and 1% respectively of the surface light, was of a similar sun type, being light saturated at about 50 000 lux. In summer, however, marked stratification occiirs so that a clear thermocline exists at a depth of about 25-50 metres. The surface plankton during summer is still of the sun type, but below the thermocline, at a depth of about 100-150 metres, which corretiponds to about 1% of the surface radiation, the phytoplankton is now of the shade type and is light saturated at less than 10 000 lux light intensity. At intermediate depths, between the surface and 100 metres, the plankton is rather intermediate in character. Again, Saijo and Ichimura (1962) have shown for the Japanese waters of the Kuroshio Current that photosynthesis varies more or less directly with light energy at relatively low light intensities. However, for plankton from the surface, 20 metres, and 50 metres depths respectively, there are clear differences in the light saturation values which reflect the sun (surface) type and shade (deeper) type of phytoplankton.

Although many species of phytoplankton may be classed as sun or shade types, the position is by no means simple in that one and the same species can undoubtedly become adapted to different light intensities. Harvey (1955), for example, demonstrated that growth rate in Biddulphia mobiliensis varied according to whether the cells had previously been grown in dim or bright light. Thus Biddulphia grown previously a t intensities of about 4 000 lux grew best in dim light, while cells grown at relatively high light intensities showed their maximum growth rate at about 18 000 lux. But light ie not the only factor which affects the relationship between photosynthesis and light intensity: there appear to be interactions between light, temperature and nutrient level (cf. also Maddux and Jones, 1964). Nutrient level can affect the ratio between chlorophyll and carbon in a pliytoplankton cell, lowered nutrient level tending to reduce the relative amount of chlorophyll (cf. Steele, 1962; Steele and Baird, 1963). Steele indeed considers that there are peaks in the relative amount of chlorophyll in the phytoplankton of temperate regions during spring and early autumn, when nutrient levels tend to be high, and that nutrient limitation during summer may affect the chlorophyll/carbon ratio more than having the usually recognized

132 J . E . G . RAYIIZONT

effect on photosynthetic rate. Steemann Nielsen and Park (1964) have demonstrated that the adaptation of phytoplankton to changed light conditions can be quite rapid. They took plankton from an area in Friday Harbour (Washington State) where there is strong vertical turbulence and where with the lack of stratification the whole phytoplankton is adapted to relatively high light intensities. This plankton was isolated in bottles and transferred to a depth where the light was only 5% of the surface value. The phytoplankton cells showed a change to the dark adapted type within three days, the main change being a marked increase in chlorophyll content. But although surface (“sun”) plankton generally has rather lower chlorophyll content, inactivation of plankton exposed to high light intensities does not necessarily involve an immediate destruction of the chlorophyll. Steemann Nielsen (19624 demonstrated that Chlorella grown in low light intensities and then transferred to high intensities showed a depression in the rate of photochemical and of enzymatic processes; after a short period of being returned to darkness, however, these processes were completely reactivated.

The complex relationship existing between light optima, temperature and nutrient levels, and possibly other factors, is illustrated by the experiments of Curl and McLeod (1961) with the diatom Skeletonema costatum. At temperatures between 5 and 18°C the photosynthetic rate increased with temperature, and the light saturation value was fairly stable a t intensities of 12 000 to 16 000 lux. At temperatures from 20-30°C photosynthesis was diminished but the saturation intensity was also reduced to a value of only about 5 000 lux. Provided nutrients (nitrate and phosphate) were present in maximal amounts, the temperature optimum approached 20°C, but when nutrients were in limited supply, not only did the photosynthetic rate fall off but the temperature optimum was lowered (cf. also Smayda, 1963). Lanskaya (1963) has shown that even when optimum conditions for such factors as light and nutrients exist, phytoplankton species (diatoms, dinoflagellates, and flagellates) show marked variations in rates of division.

Although phytoplankton species adapted to higher as well as to lower light intensities exist in the oceans, in general the very rapid light absorption means that much phytoplankton must carry out photosynthesis a t relatively low light intensities. Some diatoms for instance have been found in the Arctic which will actively photosynthesize under ice (cf. Smayda, 1963). Moreover, when phytoplankton blooms occur, the cells will cause shading to those deeper in the water layers. Thus in experiments using artificial addition of fertilizers (Raymont and Miller, 1962; Ansell et al., 1964) the compensation depth can be very close to the surface because of self-shading by the very heavy crop of

THE P R O D U C T I O N O F M A R I N E P L A N K T O N 133

phytoplankton. Similarly in the experiments of Antis et al. (1963), self- shading occurred with the very heavy crop of phytoplankton, although with stirring, the algal cells could photosynthesize at remarkably low light intensities. With the marked differential absorption of wavelengths of light in the sea, marine algae must not only be adapted to photosynthesis at low light intensities but itlso at wavelengths which may not be maximal for chlorophyll itself. It ;seems extremely likely that the many carotenoids which are present in different forms and in different concentrations in the various algal groups in the phytoplankton, are of significance in absorbing all light wavelengths. Although not every carotenoid may be of equal importance in absorbing energy, it appears to be the total quantity of solar radiation reaching the depths which is of real importance. The marine algae therefore appear to have become adapted to the generally low light intensities in the sea by increasing the chlorophyll content and by possessing active accessory carotenoids.

2. Temperature While light intensity must be of major significance in relation to

primary production in the sea, other factors may also play a part. Temperature is probably of little direct importance since lowered temperature will reduce the respiratory needs of the plant cells and higher temperatures, by increasing respiratcry requirements, can have a beneficial effect on photosynthesis only if very high light intensities are available. It is obvious that photosynthe3is occurs a t high efficiency in the Antarctic where the temperatures may be permanently below O"C, and equally well in tropical regions where temperatures approach 30°C. On mudflats in tropical regions, much higher temperatures may be experienced for at least part of the day. Experimentally it can be shown that increased temperature may have a direct effect on photosynthetic rate provided light saturation is achieved. Thus in the experiments of Curl and McLeod (1961) already quoted, it was shown that the temperature optimum for Skeletonema approached 20°C provided that sufficient light was available. Similarly Wimpenny (1958) investigated the carbon uptake of Rhizosolenia using a, standard illumination of 16 000 lux. Provided this high light intensitj. was available, Wimpenny showed that if the photosynthetic rate at lO'C was regarded as loo%, a reduction in temperature to 5°C lowered the photosynthetic activity to about 45% and a rise to 15°C increased it; to approximately 140%. Although temperature may not appear to have a direct effect on photosynthetic activity in the marine environment, it has extremely important indirect effects on production, particularly in relation to the establishment of stratification and the setting up of a thermocline during the

134 J . E. Q. RAYMONT

warmer period of the year in temperate and high latitudes. Temperature also plays a part in the species succession of phytoplankton, especially in temperate latitudes. Thus, Thulassiosira nordenskioldii is an important diatom a t the very beginning of the spring increase in the temperate northern Atlantic of America and Europe. Later in the spring, species of Chuetoceros and particularly Skeletonema take over. It has long been considered that Thulussiosira is favoured by the lower temperatures at the start of the spring increase, and that the slight rise in temperature later on is largely responsible for the subsequent flowering of Skeletonema. Even this succession, however, may not be entirely a result of temperature, since Braarud (1962) has suggested that Thalas- siosira has very high nutrient demands which would be satisfied only at the beginning of the spring increase. But temperature has a part to play in species succession. The abundance of peridinians, mainly in the summer period, in temperate latitudes, is thought to be associated with the generally higher temperature requirements of these algae. To some extent this agrees with Braarud's (1961) observation that for several dinoflagellates temperature optima are relatively high. Species succession in phytoplankton, however, is by no means limited to temperate latitudes; it is found clearly in Arctic waters (e.g. Digby, 1953; Bursa, 1963; Holmes, 1956); it is true of Antarctic waters (Hart, 1934), and is found also in warmer, subtropical waters (e.g. Riley, 1957; Hulburt, Ryther and Guillard, 1960). Thus although temperature may play a part, it is undoubtedly not the only factor in the succession of phytoplankton forms; the rapid take over from one species to another and the fact that one species may flower at two different periods in the year when temperature conditions are considerably different, points to the collective action of several factors (cf. Smayda, 1963).

3. Salinity Other factors beside light and temperature may influence primary

production. Salinity variations can be shown experimentally to have an effect on photosynthetic rate. Curl and McLeod found Skeletonema had an optimum rate of photosynthesis at salinities ranging between 15 and 20%,, though the process could go on over as wide a range as 11 to 40%,. Braarud (1961) demonstrated that some species of dinoflagellates, Ceratium, Peridinium, Prorocentrum, reproduce more actively at lowered salinities. Provasoli and McLaughlin (1963) have shown t8hat Peridinium balticum and Peridinium chattoni are even stenohaline brackish water forms with an optimum range of only 8 to 12%" for photosynthesis. By contrast, Exuviellu is a common brackish water form, but has very wide salinity limits, occurring a t salinities of 8 t o 35%"; the optimal salinity for photosynthesis is about 20 bo 25%,.


Similar work by Pintner and Provasoli (1963) has shown that marine chrysomonads may also be either stenohaliiie or euryhaline forms. For example, Coccolithus huxleyi has a remarkaldy widespread distribution in the seas and can tolerate salinities certainly down to IS%,. Although salinity therefore may have some effect on productivity rates of individual species, generally in the sea even near the surface, the variations in salinity are so very slight that this factor cannot be important in oceanic productivity. Even in inshore waters the variation in salinity is much more likely to operate in the successicm of phytoplankton species than as a factor in overall production. Since salinity and temperature, however, influence the density of sea water, salinity can affect the flotation of phytoplanktonic species. Thue Braarud (1962) suggests that oceanic phytoplankton usually consisto of either species with large cells with good flotation, or of minute forms with a higher reproductive rate. A number of coastal species are unable to avoid sinking when temperature and salinity changes reduce the specific gravity of the water. They therefore may disappear for some time, and only spore formation will carry the species over to a later flowering when changes in the density of sea water permit active reproduction again. Significant indirect effects of lowered salinity on production in relation to stratification are mentioned later.

4. Nutrients - Phsphate and Nitrate For many years the concentration of two major plant nutrients,

nitrate and phosphate, has been recognized as one of the major factors limiting primary production in the oceans. The cycle of phytoplankton growth in temperate latitudes with the marked spring and autumn peaks and the depression of production during the summer has been linked with the changes in nutrient levels. Investigations such as those of Atkins, Harvey, and Cooper at Plymouth, and of Marshall and Orr in the Clyde sea area, as well as those of Bigelcw, Lillick, and Sears (1940) for the Gulf of Maine area, suggest that the lack of nitrate or phosphate, whichever is in shortest supply, during summer when a thermocline is strongly established, acts as a marked brake on phytoplankton production. The work of Riley and his colleagues in Long Island Sound (e.g. Riley and Conover, 1956), where greater quantities of nitrate and phosphate are present over winter, indicateri that a limitation is placed on phytoplankton production during the summer by the depletion of nitrogen. In certain areas of the Gulf of Maine, over the Faroe-Shetland Ridge and in Friday Harbour, where marked turbulence occurs and there is a lack of stratification so that nutrients are not normally depleted over the summer, production may be increased. The clearest demonstration of the relationship between EL constant supply of nitrate

136 J . E . (f. RAYMONT

and phosphate and primary production is provided by the major upwelling areas such as those off West Africa, off Chile and Peru, and off the coast of California. In each region the relatively high concentrations of nitrate and phosphate are accompanied by rich growths of phytoplankton (cf. Hart, 1953; Hart and Currie, 1960; Clowes, 1950, 1954; Gunther, 1936; Sverdrup and Allen, 1939). Just recently the investigations of the Indian Ocean Expedition have pointed to a fairly rich production off southern Arabia associated with upwelling water. Above all, in the Antarctic (Hart, 1934, 1942), constant upwelling on a relatively gigantic scale permits a high rate of production as long as the light conditions are sufficient for photosynthesis. Areas of divergence may also be marked by nutrient-rich water reaching the surface. The well-known divergence close to the Equator in the Pacific Ocean is marked by a high rate of productivity (Austin and Brock, 1959; Hela and Laevastu, 1962) in the rich surface water. Holmes (1958) and Bogorov (1958) similarly relate high rates of production and of standing crop in Pacific waters to areas marked by nutrient-richer surface water. Indeed, turbulence, convection currents, current boundaries, as well as more major upwelling, are of significance in renewing phosphate and nitrate to the surface and raising primary production.

In the absence of such vertical water movements, generally in tropical and subtropical regions a strong thermocline is permanently established, and the lack of nitrate and phosphate occurring in the euphotic zone puts a sharp brake on primary production. Admittedly much of the earlier work dealt with the standing crop of phytoplankton in tropical and subtropical areas rather than with primary production, but the work especially of Steemann Nielsen (1954) and Steemann Nielsen and Aabye Jensen (1957) permits some summary to be made for production. Thus for tropical areas the rate of primary production is low amounting to some 0.1 to 0.2 g C/m2/day, and in areas such as the Sargasso Sea, where the upper water layers are especially depleted in nutrients, the production may be even lower. As against this, inshore temperate areas which are fairly rich in nutrients and also rich upwelling areas anywhere in the world may show a production varying from 0.5 to 3.0 gC/m2/day.

If we assume a direct dependence of production on nutrient level, it must be admitted that in temperate regions the fall in phytoplankton after the spring increase does not always precisely accompany the reduction in nutrient concentration. The picture is confused here by our inability often to distinguish between the standing crop of plankton and rates of production. During the summer also the standing crop may be maintained at a relatively low level by grazing although production may be proceeding at a somewhat higher rate than was originally


supposed. Equally Cushing ( 1959a and b) has demonstrated for tropical waters that rates of production may be higher than were earlier en- visaged, and that our ideas on tropical production have been unduly influenced by the usually low value of the phytoplankton standing crop. Nevertheless, rates of production are limitled by nutrient levels, although there have been relatively few laboratory experiments which have demonstrated conclusively this precise dependence for any particular phytoplankton species. The work of Ketchum (1939) demonstrated that the growth of Nitzschia was unaffected as long as about 16 mg of phosphate-phosphorus/m3 were present. Growth could continue at concentrations below that figure although on a somewhat reduced level, but at concentrations below 5 mg/m3 the rske of division fell off very sharply. More recent investigations such as those of Curl and McLeod (1961) also demonstrate the importance of nutrient level on photosynthetic rate. It is almost certain that just as different species of phytoplankton may have different light cha,racteristics so the precise nutrient levels demanded by different species also varies. Barker (1935) showed that some flagellates could grow effectively at greater dilutions of both nitrogen and phosphorus than typical diatoms. On the other hand, the investigations of Ryther (1954) suggest that the green algae Nannochloris and Stichococcus flourish only at relatively high nitrogen concentrations. Again Kain and Fogg (1958) ;suggest that Isochrysis has higher phosphate needs than most diatoms. Precise phosphorus requirements are particularly difficult to establish since many phytoplankton cells apparently absorb phosphate extremely rapidly, though they may later release a considerable proportion of the nutrient either as phosphate or in labile organic forms which :me rapidly converted into orthophosphate. Unfortunately even less is known of the precise nitrate requirements for single species of phytoplankton. Field observations suggest that the diatom Thalassiosira node wkioldii possibly has very high nutrient requirements as also does the neritic coccolithophore, Cricosphaera carterae. Although therefore we may know but little con- cerning the precise concentrations of nitrate and phosphate required, the history of the culture of phytoplankton diatoms and flagellates focuses attention on the absolute need for i;hese nutrients. From the classical work of Allen and Nelson (1910) to the highly specialized techniques of Provasoli and his school, the successful culture of phytoplankton organisms depends inter alia upon a relatively high concentration of nitrate and phosphate. Moreover the mass culture experiments carried out by Ketchum and Redfield (1938) and by Ketchum (1939), as well as the field fertilization e~periinents~of Gross et al. (1947, 1950), Raymont and Adams (1958) and Anriell et al. (1963, 1964), all point to the importance of nitrate and phosphate in primary production.

138 J . E. 0. RAYMONT

Under culture conditions it is possible by varying the amounts of nitrate and phosphate in the medium to affect to some extent the composition of the phytoplankton crop. However, Redfield (1934) showed early on that the N:P ratio in the sea approximates by atoms t o 16: 1, and though there are considerable variations in parts of the ocean, the average phytoplankton in the oceans maintains the same ratio. In a recent review Redfield, Ketchum, and Richards (1963) have shown that despite low N: P ratios which may occur in Long Island Sound and south of New York, the ratio in the phytoplankton still keeps fairly constant until extremely low nitrogen values are reached. Jeffries (1 962) has also called attention to remarkable variations in the N:P ratio in polluted estuary waters, but phytoplankton composition remained probably near normal. In nature therefore it seems that the algae assimilate only as fast as the limiting nutrient is regenerated, and marked variations in the N:P ratio of the phytoplankton are unlikely.

The remarkable growth of marine phytoplankton at such great dilutions of all nutrient requirements as normally occur in the sea is partly explained by the microscopic size of the phytoplankton cells, which allows better diffusion of nutrients and also confers a vastly greater surface to volume ratio, thus promoting absorption. It is likely, however, that to some extent the variations in the size of phytoplankton species, and even within a species, are related to nutrient requirements. Braarud (1962) suggests that Rhizosolenia styliformis and Thalassiothrix longissim are mostly oceanic species of relative large cell size which require favourable nutrient conditions. With the more coastal diatom Skeletonem costatum, under satisfactory nutrient conditions there is rapid cell division, followed by auxospore formation, which maintains a relatively large cell size. As nutrients are used up, however, the cells diminish in size and tend to sink; spore formation then commonly follows. Margalef (1 958) has also studied the succession of phytoplankton forms with particular reference to average cell size. He believes that in a spring burst, growth commences mainly with small cell diatoms which are capable of rapid division, but these are succeeded by medium-sized species and finally by an increasing proportion of the motile phytoplankton forms with a lower rate of division. One factor in this “size succession” is believed to be changing nutrient concentration.

5. Miw Nutrients So far only what are frequently called the major phytoplankton

nutrients, nitrate and phosphate, have been considered. Largely as the result of laboratory experiment, it has become increasingly obvious that a number of other elements normally present in trace concentrations in sea water are also easential to healthy plant growth. Iron, manganese,


copper, zinc, cobalt, and molybdenum are usually considered as such limiting trace elements. With the more crude culture media such as are used for mass cultures of marine algae, there are usually sufficient concentrations of these elements in the chemicals added, or in such materials as sterilized soil extract added to the cultures, to provide sufficient trace substances. However, where precise artiflcial media for the culture of marine algae are listed (e.g. Provasoli et al., 1957; Pro- vasoli, 1963) small quantities of these elements must be added to the medium.

Although culture experiments demonstrate that these elements are essential to the growth of phytoplankton, our knowledge of the concentrations of these elements in the sea, and even more of the spatial and temporal variations, is so limited that we cannot say whether they are ever limiting in nature. The position is corn plicated by the fact that some of these elements such as manganese and iron occur to a remarkable extent as particulate matter varying in size from colloidal aggregates to particles that may be retained by normal filtration. Indeed the amount of true ionic iron which can exist in sea water is extremely small, Algal cells can make use of some particidate forms, for example, of iron, and therefore the question of whether such elements ever become limiting is even more difficult.

Silicon might be considered as a possible limiting nutrient in so far as it is essential to the growth of diatoms and to silicoflagellates. Normally silica is present in relatively considerable quantities, though even in the Antarctic where very large amounts exist, Ha& has reported the presence of exceptionally thin-shelled diatoms which may reflect a lack of silica over a short period of time. Silica, however, appears to be rapidly regenerated in sea water, and it is extremely doubtful whether it can ever be regarded as seriously limiting production. The possibility still exists that with iron, and possibly with manganese, aggregation of particles may occur in the upper layers of an ocean so that the element might sink and be lost to the euphotic zone. If' this depletion occurs at all, it will take place in nutrient-poor waters, especially in open oceans far from land. The experiments of Menzel, Hulburt, and Ryther (1962) in which Sargasso Sea water was enriched with nitrate, phosphate, and iron may be of interest here. In short-term experiments iron as well as nitrate and phosphate appeared to be essential for growth of phytoplankton, but to some extent the result varied with the species of algae present. This raises the very interesting possibility that not only may phytoplankton algae differ in their minimum nitrate and phosphate requirements, but they may show differences with regard to their requirements for trace elements. For example, it has been suggested that Skeletonem has fairly high iron requirements, and indeed this mainly

140 J. E. G . RATMONT

coastal species may be limited to neritic regions partly on nitrogen and phosphate requirements, but equally on the relatively greater demands for trace elements. In this connection Hulburt and Rodman (1963) have suggested that the sporadic blooms of neritic species in the open sea may be occasioned by the temporary presence of larger quantities of iron or some similar nutrient which normally limit their distribution. However, the experiments of McAllister et al. (1961) in which coastal plankton species bloomed successfully indicated that trace metals (Fe, Cu, Mn) were not limiting. It is probable that species have different trace element requirements. Jones and Haq (1963) believe that blooms of P h e o c y s t i s may depend on some minor nutrient. Tranter and Newel1 (1963) suggest that iron may be important in oceanic waters off Australia. Pintner and Provasoli (1963) state that trace metal requirements are excessively low for the chrysomonads. Johnston (1964) also believes that different species may have varied requirements. He has emphasized the great importance of trace metals such as iron, manganese, copper, and molybdenum; under special conditions in a few areas some of these elements may be temporarily limiting. Although in northern seas sufficient quantities of these trace metals are normally present, with the high pH of sea water they may be virtually unavail- able to the phytoplankton cells. A chelating agent may therefore be of the greatest significance in making the metals available. In the sea, organic acids present in great dilution may act as such chelating agents. This in turn focuses attention on dissolved organic factors in sea water.

6. Organic Requirements Early experiments on the laboratory culture of marine algal species

proved fairly conclusively that even when nitrate, phosphate and trace elements were supplied to the algae, growth was often impeded unless some organic constituents were also present in the water. Work over the last few years has shown an increasing number of organic substances which are mostly present at very low dilutions in the sea (cf. Hood, 1963) (Duursma, 1961). Although most of these are extremely difficult to identify, a recent review by Provasoli (1963) lists such materials as carbohydrates, amino-acids, fatty acids, organic acids, vitamins, and inhibitory substances as occurring in sea water.

The variety of organic substances present in sea water is remarkable. Analyses by Tatsumoto et al. (1961) and by Park et al. (1962) have revealed some 17 or 18 amino-acids existing in surface and deeper ocean waters. The studies of Koyama (1962) showed not only a variety of amino-acids, but of carbohydrates, fatty acids, metallo-organic substances as well as vitamin compounds. Much dissolved organic material arises from the decomposition of planktonic and nektonic organisms.

T H E PRODUCTION O F M A R I N E I'LANKTON 141

But some may arise from the excretion of planktonic organisms; Pomeroy et al. (1963) have called attention t o the importance of ex- creted phosphorus in production. Organic nitrogen (urea, amino-acids, etc.) typically forms a fraction of the excr1:ted nitrogen of marine animals. But organic material is also liberated during the metabolism of phytoplankton algae, though Duursma (1!361) contends that practically all the dissolved organic matter in sea water is derived from decomposition and no clear evidence exists for appreciable quantities being liberated. Apart from highly toxic materials liberated in the growth of species like Gymnodinium, Goniaulax, Prymnesium (cf. Gunter et al., 1948; Abbott and Ballantine, 19b7; Brongersma - Sanders 1957) which can affect adversely a wide range of animals, there are a number of algae which can favour or discourage the growth of other species by excreting growth-promoting or growth-inhibiting substances (cf. Jerrgensen and Steemann Nielsen, 1961). There are a number of investigations reporting the production of ext ra-cellular substances by marine algae. Collier (1953) described carbohydrate-like substances, apparently produced by algae, and later (1958) showed the production of carbohydrate-like substances by Prorocentrum and by Gymnodinium breve. Guillard and Wangersky (1 958) demonstrated the production of soluble extra-cellular ca,rbohydrates by a variety of flagellates, the amount released being highest in stationary c r declining cultures. Curl and McLeod (1961), studying the culture of Skeletonema, suggested that extra-cellular substances are produced a t certain stages of growth. Parallel work with fresh water algae such as that of Fogg and of Proctor (1957) indicates that nitrogenous cirganic materials, carbohydrate-like substances and lipids produced by algae may be liberated into the water. Many workers have suggested chat the secretion of these substances tends to occur when algae are becoming somewhat un- healthy, especially during intensive blooms. While there is considerable evidence that this is true for many specie,3, Fogg (1963) advances strong arguments for the view that some excretion of material occurs during normal healthy growth of both fresh .water and marine algae. Indeed, Fogg criticizes the 14C method for estimating primary production by suggesting that an appreciable propclrtion of the fixed carbon may appear in soluble form in the filtrate, quite apart from losses from the breakage of cells during filtration. The recent experiments of Antia et al. (1963), using the plastic sphere technique, have confirmed a considerable excretion of organic matter by healthy algae. Fogg draws particular attention to the importance of glycollic acid in algal metabolism; his experiments suggest that quite an appreciable amount may be released during active photosynthesis of phytoplankton. Though this may introduce errors in calculating the primary production, it should

€42 J. E. a. RAYMONT

be noted that some of the glycollate released may be used by bacteria to synthesize particulate matter, thus contributing to production as a whole. The possibility also exists that algae may themselves absorb such extra-cellular substances and use them in synthesis. A moat interesting related observation by Smith et al. (1960) is that carbamino- carboxylic acids may be used as a carbon source by phytoplankton, apparently even preferentially by Nitzschia. Similarly, Parsons and Strickland (1962) have commented on the limited heterotrophy of algae. Although in their work uptake of such dissolved organic carbon as glucose and acetate was due to microorganisms, such as bacteria, we know that limited uptake of carbon compounds can occur in algal groups. Thus Lewin and Lewin (1960) and Lewin (1963) showed that different diatom species show marked differences in their heterotrophic abilities; some can utilize such organic carbon as glucose and lactate, though generally their heterotrophic powers appear to be rather limited. Among the flagellate chrysomonads, however, Pintner and Provasoli (1963) showed that an array of organic acids as well as carbohydrates may be used as carbon sources, though specific differences again are evident; Coccolithus huxleyi, for example, shows very little ability to utilize organic carbon. These same authors noted that glycero-phosphate may be used in place of orthophosphate. As regards nitrogen, such substances as adenylic acid and a range of amino-acids may be employed by these flagellates, though these substances appear to be inferior to inorganic nitrate. Guillard (1963) had shown that some diatoms and unicellular flagellates could make use of organic nitrogen (amino-acids, urea, uric acid) in bacterial-free culture, and Provasoli and McLaughlin ( 1963) demonstrated limited utilization of dissolved organic nitrogen by dinoflagellates.

At first sight it might seem that this limited heterotrophic ability of phytoplankton is unimportant in the oceans, but it must be remembered that the amount of dissolved organic matter, relatively, is very large in sea water. Provasoli (1963) suggests that it may be some 7 to 8 times the amount of particulate matter in the euphotic zone, where the plankton is, of course, relatively rich; in deep waters the dissolved organic matter may approach 1 000 times the particulate matter (cf. Duursma,, 1961). Parsons and Strickland (1962) suggest that the average amount of dissolved carbon in .sea water is about 1 g/m3, but in surface waters and near land the concentration may be 5 to 10 times greater. Despite the earlier work of Krogh (1934) which suggested a mean value of > 2.OgC/ m3 and that the amount of dissolved organic matter was relatively stable in the oceans, there appear to be considerable variations both horizontally and vertically. Duursma (1961) finds lower values in the northern Atlantic; few areas exceeded 1.0 gC/mS, but the upper layers


showed considerable seasonal variations. Values quoted by Provasoli (1963) include 2.8-3.4 g C/m3 for the Black Sea with a marked seasonal variation, and up to 4.(igC/m7 in the Ihltic. Inshore regions may have very high values; even 8.0g C/mJ in the Wadd:n Sea (Duursma, 1961).

If photosynthetic organisms can make use, a t least temporarily, of some of this vast reserve of dissolved organic substance, it can play a significant part in particulate production. Eut the possible heterotrophic powers of phytoplankton must be also considered in relation to the important observations of Bernard (19!i3; 1963), Bernard and Lecal (1960) and of Kimball et al. (1963) that considerable populations of photosynthetic organisms may apparently exist in some seas, such

‘ as the Mediterranean and parts of the Indian Ocean, a t depths well below the euphotic zone. Many of these algae are not dying populations which have descended into the deep layers, but are in healthy condition and are actively living at these depths. Wood (1963a and c), Bernard, as well as Kimball et al., have all suggested that such organisms must be living heterotrophically at such great depths. Though coccolithophores often tend to dominate these deeper-sea populakions, other algal groups, diatoms, flagellates, and dinoflagellates, are also represented. Especially in such seas where primary production in the euphotic zone may not be very high, and therefore the amount of particulate matter reaching deep water may be much reduced, productioi due to this deep-living phytoplankton may be extraordinarily significant to the whole economy of the deeper layers.

Apart from the possibility that some pl1,ytoplankton may utilize dissolved carbon and nitrogen, certain species are known to have definite demands for specific organic constituents. Organic substances may be important as chelating substarices m d a number of marine phytoplankton forms are now known to have specific vitamin requirements. Among the many growth-promoting and growth-inhibiting substances in sea water, Belser (1959) demonstrated 10 growth-promoting substances on a marine bacterium of which three, biotin, uracil, and isoleucine appeared frequently in sea water s#tmples. Other substances have been recently assayed (Belser, 1963). Collier (1953) and Wangersky (1952) both reported the presence of ascorbic acid in sea water, and later studies by Collier et al. (1956) suggested that nicotinamide as well as ascorbic acid could affect the growth of marine species. Harvey (1955) suggested that cystine was necessary for the growth of some diatoms, and Provasoli et al. (1957) indicated that divalent sulphur is probably necessary, a point which has also been recently taken up by Curl (1962a) for the growth of Skeletonenza. Wood (l”963b) lists several organic substances which influence photosynthesis and growth of flagellates and diatoms. At this stage we crinnot list all the organic

144 J . E. G . RAYMONT

compounds which may be present in sea water and which may promote the growth of phytoplankton, but three vitamins (cobalamine or vitamin B,,; thiamin or vitamin B,; and biotin) appear to be of more general significance to a number of species (cf. Belser, 1963). The main produ- cers of these vitamins are marine bacteria, but some algae apparently synthesize vitamins; the red algae are often especially rich, though there is some question as to whether these are not really accumulated by these macrophytes (Provasoli, 1963). Kanazawa (1961) records a considerable list of vitamin B complex from algae. The very fact that some algae can synthesize vitamins underlines the point that phytoplankton species differ greatly in their precise requirements even for these three vitamins. Since also it is only by most careful culture techniques that we can test for vitamin requirements, it is not surprising that specific needs are known only for comparatively few phytoplankton forms; the oceanic phytoplankton is particularly unknown in this regard.

As regards vitamin B,,, the work of Provasoli and his colleagues (e.g. Provasoli, 1958), of Droop (1957) and others, as summarized by Provasoli (1963), suggest that a number of dinoflagellates and some diatoms (e.g. Xlceletonema) all require vitamin B12. On the other hand, some algae such as Rhodomonas, Dunaliella, Nannochloris, and Phaeo- dactylum do not require the vitamin. Presumably they synthesize it from simpler substances. Species which require B,, show considerable differences in their ability to grow successfully with various analogues of this vitamin; how far such analogues occur in the oceans is unknown. Differences in the spatial concentration of B,, or temporal variations might, however, limit production. Investigations by Droop suggested that a considerable amount, probably sufficient for the needs of the algae, were present in inshore waters (5-10 mpg/l), but work by Cowey (1956) in the North Sea and the Norwegian Deeps indicated that while this order of concentration might be present in winter, in summer the concentration fell to 1/10 of the value. Daisley and Fisher (1958) also showed for the Bay of Biscay that the euphotic zone had only about 0.6 mpg/l as against about 4 times that value at intermediate depths (from 200-2 000m). For the Sargasso Sea, Menzel and Spaeth (1962) found only up to 0.1 mpg/l of vitamin B,, in the upper layers with some seasonal variation; below 200m the concentration of about 0.2 mpg/l. was relatively constant. Several authors therefore (e.g. Provasoli, 1963) doubt whether sufficient B,, is always present for phyDoplankton, especially in the open sea. Skeletonema as a main spring diatom has been observed to reduce the vitamin B,, content of waters in Long Island Sound appreciably, though the amount there is relatively large (cf. Vishniac and Riley, 1961). Antia et al. (1963) obtained evidence


for considerable utilization of vitamin B,, in their culture experiments, but biotin did not appear to be used. The work of Guillard and Cassie (1963) suggests that phytoplankton B,, requirements may be slightly greater than was first considered. Thus they find minimum needs for both neritic and oceanic forms of about 5-18 molecules of B,, per cell, as compared with 3 per cell suggested by Droop. These authors make the interesting suggestion that B,, may be required by some phytoplankton species only a t a particular stage in their life history; for example, by Skeletonema at auxospore formation.

The absolute requirement for thiamin varies also from species to species of marine phytoplankton. For example, Phaeodactylum and Nannochloris, which do not require B,,, do riot need thiamin. On the other hand, Skeletonema, which requires B1,, citn grow without the addition of thiamin. Pintner and Provasoli (1963) found that chrysomonads generally required B, rather than BIZ. A sum :nary of the requirements of various algae for B12, thiamin and biotin as given by Provasoli (1963) is seen in Table 111. Vishniac and Riley (1961) found only barely detectable amounts of thiamin, in contrast LO B,,, in the more open water of Long Island Sound; such small concentrations could limit the growth of species unable to synthesize the vitamin. We lack knowledge, however, of the variations in concentration of growth promoting substances in the oceans and of the precise nutrient requirements of individual species so that it is not possible to imsess their exact role in primary production. It seems likely that at times insufficient amounts may be present, at least in the open sea far from land. The requirements of neritic species also probably exceed that cbf most oceanic forms (cf. Hulburt, 1962; Hulburt and Rodman, 1963) and, more generally, the vitamin requirements of planktonic species probably play an important part in spatial and temporal succession.

The whole array of dissolved organic substances may be of significance in this connection. The production of extracellular substances imposes a biological history on the water, and Lucas (1947, 1955, 1961) in particular has called attention to the great importance of this biological conditioning to both phytoplankton and zooplankton. Several studies of species succession have included conditioning of the water as one factor. Lillick (1940), for the Gulf of Maine, thought that subtler differences due to conditioning of the water were responsible in part. Conover (1956), describing a rather simila,r study of seasonal succession in Long Island Sound, stated that conditioning of the water was an important aspect of the species succession, and suggested that Schroederella was particularly favoured by the products of blooming of earlier species. Margalef (1958) has also called attention to t’he importance of external metabolites. He describes three main phases i n a species succession, the

TABLE I11 Sunant any of Vitain in Requirements of Fresh- Water and iWari?ze Algae

(from Procasoli, 1963)

algal group Number of KO Require B,, Thiamine Biotin B,, + Biotin + B,, + biotin species vitamins vitamins thiamine thiamine + thiamine

Chlorophyceae Euglenineae Cryp tophyceae Dinophyceae Chrysophyceae* Bacillariophyceae Cyanophyceae Rhodophyceae

68 9

11 17 22 39 10 4

24 0 0 1 1

21 9 0

44 9

11 16 21 18

1 4

10 8 2 1 2 1

1 1 2 5

11 3 1 4

26 6 7 0 1 4 9 1 2 4

Totals 180 56 124 43 18 52 2 6

Totals for single vitamins 103 78 10

*Two chrysomonads require Blr + biotin


third consisting mainly of more slowly dividing motile algae characterized by species with metabolites of high toxicity. He suggests that these phytoplankton species havc n relatively high immunity to these toxic substances.

It has long been recognized that in a given region, inshore areas usually show greater production and standing crop than more oceanic areas. The difference is normally attributed to the more turbulent mixing of coastal regions assisting in the replenishment of essential nutrients in the euphotic zone (vide infra). But examples were known when even though nitrate and phosphate were relatively plentiful, inshore areas displayed increased production. Bran (1931) suggested that coastal regions might benefit from other micronutrients brought down by land drainage. In the Antarctic where phosphate and nitrate is abundant, Hart (1942) noticed that neritic areas, which could stretch out to a considerable distance from land, showed greater production. He suggested that the important factor might be micronutrients, such as trace metals, which were carried out from che land. It may well be that an organic growth-promoting substance, rather than a trace element, is in part responsible for this beneficial neritic influence. To some extent a similar condition is found at the boundaries of ocean currents. For many years it has been widely recognized that standing crop and productivity tends to be higher at current boundaries. Un- doubtedly part of this increased production is due to extra nutrients which are made available in the euphotic zone in such areas. But even in situations where there is no nutrient lack or appreciable difference in concentration, a marked improvement in production is often found in areas of water mixture. The so-called “island effect” is possibly explained on the same hypothesis. This effect (e.1;. Doty and Oguri, 1956; Jones, 1962) is a tendency to an increase in primary production and also to a genera1,rise in standing crop of plankton in the regions round oceanic islands. Jones found, for example, an increase in plankton crop to a distance of nearly 200 miles from the Marquesas Islands. Although increased nutrients such as nitrate and phosphate can certainly occur around oceanic islands, it seems impossible from Jones’ results to explain the increased plankton as due to nutrient level at such a distance from the island. The presence of an increased concentration of a trace element such as iron, or equally likely, of a mi cronutrient organic substance draining from the regions of the islands, seems a more probable explanation.

c. PRODUCTION - TEMPERATURE AND STRATIFICATION

In tropical regions the small variation in light intensity over the year means that the euphotic zone is more or less constant in depth. On the

148 J . E . G. RAYhZONT

other hand, in temperate and high latitudes the change in the compensation depth from winter to summer is very appreciable. An indication of the steadily rising amount of light energy reaching increasing depths of the sea in a temperate latitude from January to June is given in Table IV. The rate of primary production must be markedly reduced at such latitudes during the winter owing to the shorter day and the very much reduced light beneath the surface ; the compensation depth is so near the surface that only the uppermost stratum can be actively photosynthesizing. But owing to turbulence, the algal cells may easily be carried out of this surface layer, and in the subsurface layers light penetration is no longer effective. Thus primary production is non- existent except for the surface itself. In the absence of turbulence, algal

TABLE IV Average Energy in gcallcm2/day in Lat. 52" N , January to June,

reaching the Surface and Reduced by the Energy Extinction Coeficient of Coastal Water (Type 1 of Jerlov, 1951) (after Cushing, 1959)

Jan. Feb. March April May June

Surface 18-98 44.91 92-09 164.25 219.20 242.06 l m 7 -00 16.57 33.98 60.61 80.88 89.32 5 m 2-70 6-38 13.08 23-32 31-13 34-37

10 m 1.12 2.65 5 *43 9-69 12-93 14.28 20 m 1-20 2.14 2-85 3.15 30 m 0.66 0 ~ ~ 7 3

cells might be confined to the surface and thus there might be even during winter at least a surface blooming of phytoplankton. Even with the increase in light during the spring, the vernal blooming of phytoplankton, which is such a conspicuous feature of temperate and high latitudes, is dependent to a large extent on how far turbulence is active in the region. Normally some degree of stratification of the water is essential to reduce the passage of algal cells from the relatively shallow photosynthetic zone. Riley (1946) in particular has stressed the importance of stratification in initiating the spring increase in temperate latitudes. For the Gulf of Maine, Riley has demonstrated a direct correlation between the phytoplankton rate of increase and the stability of the water column (Fig. 5) . This stability of the water depends to a large extent on temperature conditions insofar as warming of the surface layers will cause them to become less dense, so restricting mixing with underlying layers. Stability therefore tends to increase in the spring with rising temperature, and thus it is possible to establish a correlation


in higher latitudes early in the spring between the rate of primary production and temperature increase. Although! therefore, temperature may have little or no direct effect on phytoplankton production, it plays a most important part in stabilizing water layers.

Slight reduction in surface salinity may also play a part in stabilization, and some of the more marked production (of coastal shallow water can be attributed to this increased stability (cf. Braarud and Klem, 1931; Gross et al., 1947; Marshall and Orr, 1948:. Under such conditions phytoplankton production may be possible during the winter but it is

I Depth

FIG. 5. Estimated mean daily rate of phytoplankton increase during March-April in relation to the reciprocal of depth of the zone of vertical turbulence; (redrawn from Riley, 1942).

restricted to an extremely shallow surface layer. In parts of the Baltic reduced salinity of the upper layers produces this stability throughout the year so that production of phytoplankton may also continue over winter months (cf. Steemann Nielsen, 1935; 190-0). Recently Steemann Nielsen (1964b) has studied in some detail two areas in the Baltic which show different rates of primary production. In the Kattegat the rate at the surface was remarkably stable over much of the year, at least for the period, March-November; light appeared to be a limiting factor for the surface algae only during the very darkest months of December and January. At greater depths, light was a limiting factor throughout many months of the year. The relatively efficient praduction and the maintenance of a fairly even rate at the surface was m.ainly due to the marked stratification which prevented algal cells from being carried away from the lighted surface. By contrast in the Great Belt region, stratification waa less strong, and with the greater degree of mixing, production over the year was much less constant; even at the suIface illumination could become a limiting factor over a considerable period of the year.

The importance of light penetration in relation to the depth of the

-

P


mixed ( i t . unstratified) water layer has been emphasized by Riley (1942-46) and also by Sverdrup (1963). Sverdrup has used the term “critical depth”, which may be defined as the depth above which the total photosynthesis is equivalent to the total respiration per unit of surface. In a thoroughly mixed upper water layer it might be assumed that the plankton cells were practically evenly distributed; production would therefore decrease logarithmically with depth since light decreases logarithmically, but respiration will be approximately constant with depth (cf. Fig. 6). For effective production, there must be a critical

d 0 2 4 6 8 10 1 2 1 4

Relative photosynthesis

PIG. 6. The relation between total photosynthesis and respiration in a column of water. Total photosynthesis is shown for three dates: A in summer with bright sunshine; B in summer with cloud; C in winter; (modified and redrawn from Ryther. 1966).

depth which must exceed the thickness of the mixed layer. In the Nor- wegian Sea, Sverdrup demonstrated that the spring increase in phytoplankton occurred in early April, and that the period coincided with time of increasing stabifity, so that the mixed layer was only about 50-100m depth, whereas the critical depth exceeded 100m. Kalldal (1953), investigating the phytoplankton seasonal changes in the Nor- wegian Sea, states that a fairly early spring growth commences with increased light penetration, but that the considerable mixing of the water layers prevents a real increase of phytoplankton until May/June when stability is established. The main growth (June/September)

THE PRODUCTION O F MARINE I’LANKTON 151

appears to coincide with the period of stability. Holmes (1956) finds for the Labrador Sea that from November to April there is very little phytoplankton with the marked instability of the water column. Over the May/June period, increasing stability rtnd increased radiation apparently are mainly responsible for the phjtoplankton peak. In the Arctic waters off Bear Island, Marshall (19,58) showed that during March/April the mixed layer shallowed to less than the critical depth and effective production of phytoplankton commenced, whereas in the warmer Atlantic water nearby, the mixed layer only became shallower than the critical depth by about May and June, and phytoplankton production was correspondingly delayed. At these high latitudes the stability of the water in late spring may be due in part to the melting of ice; the phytoplankton outburst in polar regions frequently seems to follow the melting ice edge (cf. Braarud, 1935; Hart, 1934). Zenkevitch (1963) also mentions that in Arctic seas the algal bloom follows the ice melt and believes that this is due to the importance of critical depth exceeding the mixed turbulent layer.

The vernal blooming of phytoplankton, while mainly due to increasing light intensity and length of daylight, is tlius dependent to a considerable extent on stabilization. Some of the cliscrepancies in the time of commencement of the spring increase, observed by many workers (e.g. Kreps and Verjbinskaya, 1932; Corlett, 1953; Conover, 1956; Fish, 1925; Bigelow et al., 1940) may be explained as due to differences in stabilization of the water column. Strong winds will reduce stability; thus shelteredareasmay bloom earlier than exposedregionsat similarlatitudes.

The continued rise in temperature during late spring and early summer in temperate regions causes increased stratification of the water, so that typically a marked seasonal thermocline exists over the summer. In normal seas this thermocline restricts the continued supply of essential nutrients to the euphotic zone where they are being extensively utilized. Reduced surface salinity with a stable water column may also be detrimental to nutrient replenishment later in the season when nitrogen and phosphorus have been extensively utilized, and thus may lower productivity. Steemann Nielsen (1 958) has shown that in coastal areas off Greenland, zones of very low piioduction are associated with lowered salinity surface water which prevents the vertical transport of nutrient rich water from below. Where there is considerable mixing of the water layers, a high production follows. Anderson (1964) refers to the outflow of the Columbia River off the M’ashington and Oregon coasts, producing a permanent halocline. This may effectively reduce the thickness of the mixed layer in winter, but in summer, with the addition of a seasonal thermocline, may act ;LS a barrier to vertical movement of nutrients.

152 J . E . a. RAYMONT

When such density differences restrict vertical transport of nitrate and phosphate to the euphotic zone, regeneration processes in the photosynthetic stratum itself may be of the greatest significance, in that excretory material and some organic detritus can be converted relatively rapidly to inorganic phosphorus and nitrogen, mainly as ammonia, so keeping some phytoplankton growth continuing. Rates are the major factors and there appears to be variation between nitrogen and phosphorus regeneration (cf. Harris, 1959; Vaccaro, 1963; Pomeroy et al., 1963; Hoffman, 1956; Menzel and Ryther, 1964; McAllister et al., 1961; Antia et al., 1963). Nitrate regeneration appears to be especially slow. In any event, regeneration usually is insufficient, and with the restric- tion in vertical transport of nutrients, a reduction in primary production typically occurs during the summer months. With the autumn break- down of the seasonal thermocline and the consequent increased supply of essential nutrients to the euphotic zone, an increased production again leads to the so-called “autumn peak”, but this is usually short-lived owing to the rapidly decreasing light.

Too often this picture of a spring and autumn peak in phytoplankton with a smaller and variable production over summer (cf. Fig. 7) has

- lee. I Jon. I Feb. I Mar. 1 Apr. I May 1 June 1 July I Auq. 1 Sep. I Oct. 1 Nov. I Dc

FIG. 7. Diagrammatic representation of the seasonal cycles in light, nitrate and phosphate, and phytoplankton in a typical northern temperate sea. (Reprinted from Plankton and Productivity in the Oceans, Raymont 1963, Pergamon Press).

been based on estimates of standing crop of phytoplankton rather than on rates of primary production, though the few seasonal estimates of productivity such as those of Ryther and Yentsch (1958), Anderson (1964), Steele (1958) and Steele and Baird (1961) confirm the high rate in spring and the lowering of rate in summer. The large densities of zooplankton over summer may reduce the phytoplankton standmg

THE PRODUCTION O F MSRINE I'LANKTON 153

crop very greatly, although primary production is continuing at a very high level, so that crop estimates may give misleading impressions of production (vide infra).

There is a marked tendency at higher latitudes for the spring increase to occur much later, for example, in May or June as recorded by Gran (1931), Steemann Nielsen (1935), Kreps and 'Jerjbinskaya (1930), and Gillbricht (1959), in the Arctic. Digby (1953) did not obtain any appreciable phytoplankton production until May o f eastern Greenland; the peak density occurred in July, with a smaller scxondary peak in August, but the whole production was finished by September. Corlett (1953) also shows differences in timing of the spring diatom outburst with latitude in various oceanic areas of the northern Atlantic. In the Labrador Sea, Holmes (1956) finds the double peak in phytoplankton production; until March there is virtually no algal growth owing to the marked instability of the water column and the poor light conditions. The spring peak occurs about May and June, a,nd there is a smaller rise in September. Zenkevitch (1963) has summarized the position for the Arctic: the nearer to the Pole, the later becomes the vernal outburst and the more rapidly is it over. In the Circumpolar Ocean, for example, the phytoplankton burst lasts hardly more than one month (August); in the Laptev Sea the outburst lasts from the end of June to about the end of September. On the other hand, in the most southern of the sub-Arctic seas, the south-western Barents Sea, the period of phytoplankton growth may approach 8 months (April to October/November), and there is a typical spring and smaller autumn bloom. In. the Antarctic, Hart (1934, 1942) has also shown that the timing of the spring increase becomes later as one proceeds farther south. Not only does the outburst become later, but the amount of time during which diatom growth proceeds becomes shorter until at the highest latitudes there may be only one short continuous burst of phytoplankton production.

Although typically in north-western Europe and the north-eastern American coast the spring increase is about March, the phytoplankton flowering may occur earlier; for example, Ccmover (1956) and Riley (1952) found an increase in early February in Long Island Sound and Block Island Sound, and Fish (1925) believes that at Woods Hole the increase is as early as December. This earlj flowering may depend partly on the sheltering of waters in these areas. Certainly the timing of the increase is not entirely associated with latitude. Thus Riley (1957) recorded for the North Sargasso Sea (latitude :35"N) a small diatom increase as late as April and this was confirmed by Hulburt et al. (1 960) off Bermuda. However, Menzel and Ryther (1960; 1961) find slightly farther south that a winter flowering may occur in any month between November and April. I n contrast to temperahe latitudes, in tropical


areas the small variation in light and temperature throughout the year tends to maintain phytoplankton production at a relatively constant level. Normally in tropical regions, the thermocline is permanent, and therefore there can be little effective nutrient replenishment and little variation in nutrient level in the euphotic zone throughout the year. At all times, nutrient level is low and regeneration inside the euphotic zone is a most important factor in the maintenance of primary production. Regions of upwelling or of current divergences are, of course, ex- ceptional in that nutrients are brought near the surface and production tends to be high. Apart from these regions, however, there may be areas in warmer seas where the relatively small differences between “summer” and “winter” temperatures are sufficient to cause further stratification of the upper layers and the establishment of a seasonal thermocline. If the cooling of the uppermost strata is sufficient and there are also strong wind effects, some mixing may occur in the cooler months leading to a small winter flowering of plankton. Menzel and Ryther (1960; 1961) found areas of the Sargasso Sea near Bermuda where such a winter blooming might occur depending on the degree of vertical mixing. Maximum production occurred when the upper water . was practically isothermal to ca. 400m, approximately the depth of the permanent thermocline. When over the summer months a seasonal thermocline was evident at about 100m. depth, production was reduced (cf. Steele and Menzel, 1962). Hulburt et al. (1960) suggest that the April flowering near Bermuda may be three or four times that of the autumnlwinter level of production; summer production is even lower.

Farther south, in tropical waters, the stratification of the uppermost layers is permanent; mixing cannot occur appreciably even throughout the euphotic zone and so a winter blooming does not normally occur. There is a tendency therefore in tropical areas for there to be relatively little change in phytoplankton density over the year. Corcoran and Alexander (1963) have suggested that there is little seasonal cycle in Florida current waters, though they have recorded occasional high levels of production and crops reaching even 0.5 mg chlorophyll alms. Cushing (1959a and b) has pointed out from the results of earlier workers such as Riley et al. (1949) and Bernard (1939) that for the Sargasso and Mediterranean a slight seasonal fluctuation in phytoplankton crop with a more productive season in winter may be evident. But close to the Equator the productive season is perhaps even earlier and the seasonal fluctuations are less. Cushing suggests a seasonal amplitude of 5 times for the Sargasso Sea, whereas a fluctuatior, of some 50 times might be true for higher latitudes.

Zenkevitch (1963) has pointed out that although very high crops of phytoplankton can occasionally be found in the coldest Arctic waters,

THE PRODUCTION O F MARINE I’LANKTON 155

this is not necessarily a true estimate of productivity. He suggests using an index which averages the crop to a depth of 30m, and takes into account the duration of the phytoplankton increase in months, relative to the whole year. The index is:

mean crop (0-30m) x duration of flowering (months) 12

Using this index he shows that for the Arctic basin the biomass may be only one-twentieth that of the northern I3arents Sea. The factors responsible for this low production are fairly obvious. Although in seas north of Siberia the low surface salinity may impede circulation and reduce productivity, in the Arctic Ocean proper it is essentially the thick ice cover, which does not permit phytoplankton growth for some 10 months of the year, which is mainly responsible. Even the northern Barents Sea is far less productive on this annual basis than a warm temperate area. Zenkevitch includes an index based on this same for- mula for the Sea of Azov, a warm temperate area which being largely enclosed, has a high productivity. But the rich ;$owth of phytoplankton also ccntinues for between 9 and 10 months of the year, so that the index of production for the Sea of Azov is some 15 times that of the northern Barents area.

~ _ _ ~ ~ _ _ _ _ _ _ _ _

111. THE STANDINQ CROP OF PHYTOPLANKTON

These estimates of Zenkevitch really represent an average biomass of plankton over the year; they are therefore estimates of standing crop rather than production. Reference has already been made to the difficulty of estimating standing crop; one widely used method is chlorophyll concentration although we have already noted some of the errors in this technique. Earlier methods for estimating standing crop were almost all based on counts of phytoplankton cells. These were collected mainly with the finest silk nets, which though rihowing some variability in porosity, have an average pore size of 40p x 5Op. But apart from variations in mesh size due to manufacture, to the degree of wetting, to age and strain, such nets will clog to varying degrees depending on the concentration of phytoplankton and detritus They will therefore in effect vary greatly in catching power. but in any event a large number of the finest photosynthetic organisms (below 50p) will normally pass through them. The term nanoplarikton has been given to these very small photosynthetic organisms which normally escape the finest nets, and it has become obvious, especially in the last 20 or 30 years, that the nanoplankton may make a significant contribu1;ion to the standing crop and indeed to production.

The nnnoplanktoii plants belong to a variety of algal groups; some

156 J . E . G . R A Y M O N T

are small diatoms or dinoflagellates, but others belong to the Chryso- phyceae, Chlorophyceae, and Cryptophyceae. Various methods have been used to try to estimate nanoplankton densities; for example, the fixation of samples of sea water, followed by sedimentatiQn and counting with reversed microscope; centrifugation; filtration through hardened filter papers or through membrane or sintered glass filters. All such methods have disadvantages. Many of the delicate cells are destroyed by fixation and by centrifuging, and cells cannot be adequately counted if they are first filtered. Counting of unconcentrated samples is equally unsatisfactory. Although, therefore, we have no single method which estimates nanoplankton adequately, it is abund- antly clear that the use of fine silk nets to estimate the phytoplankton as a whole is entirely misleading as a quantitative method. Contributors to a recent symposium on primary production have indeed stated that net samples alone should no longer be employed for quantitative estimation (Braarud, 1958). The chlorophyll extraction method probably gives a fair indication of the standing crop of phytoplankton under most conditions, since provided a suitably fine filter is employed, both nanoplankton and larger phytoplankton will be captured. But the im- perfections of the chlorophyll method (see page 124) must still be taken into account.

A comparison of the density of the nanoplankton and of the remainder of the phytoplankton, often termed the “net” phytoplankton, shows that nanoplankton may be sometimes important in certain regions. In more inshore waters at temperate latitudes the net phytoplankton, especially diatoms, is frequently dominant over much of the year, but Lohmann (1908; 1911) showed that the nanoplankton could be very important at certain months. Harvey (1950) for the English Channel found a very much larger crop by filtration estimates, which included nanoplankton flagellates, as against fine net samples which would normally retain only the larger phytoplankton. Gross et al. (1947, 1950) found that the nanoplankton could form a very appreciable part of the crop in shallow temperate waters. Yentsch and Ryther (1959) have also called attention to the importance of the nanoplankton fraction in the waters off Woods Hole. Small flagellates have been recorded in considerable numbers in the North Sea (Gramtved, 1952) and in the Baltic area (Steemann Nielsen, 2951). The same author (1935) has recorded nanoplankton flagellates in cold seas, as did Braarud (1935) around Iceland, and Halldal (1953) found appreciable numbers of coccolithophores and flagellates in the Norwegian Sea (cf. also Bursa, 1963). More generally at high latitudes it is the larger diatoms which tend to dominate the phytoplankton. Although much of the earlier work at high latitudes did not specifically estimate nanoplankton but relied on

THE PRODUCTION O F M A R I N E P L A N K T O N 157

net hauls, more recent work such as t,hat of Burkholder and Sieburth (1961) indicates that in the waters of Antarctica diatoms are probably all-important; the only other organism which bulked large in the phytoplankton was Phaeocystis.

It is perhaps in the warmer seas that the nanoplankton algae, including the coccolithophores, become of particular significance. The investigations of Lohmann and of Bernard (1953) in the Mediterranean, of Riley (1957) for the Sargasso Sea and of Bsharah (1957) for the Florida Current call attention to the importance of nanoplankton in warmer waters. Hulburt, Ryther, and Guillaxd (1960) report on the prevalence of coccolithophores in waters off Bermuda; though the nanoplankton was not quantitatively measured, small coccolithophores, flagellates and other nanoplankton forms made a considerable contribution to the total crop. Hulburt (1962), dealing with the tropical north Atlantic finds that small flagellates and coccolithophores are fairly regularly distributed in these warmer waters together with diatoms and dinoflagellates. Wood (1 963a) considers that the nanoplankton generally becomes increasingly important in tropical seas, although there are exceptions, such as a considerable abundance of diatoms occurring off the Australian coast, end also off the western coast of India. On the other hand, north and south oS the subtropical conver- gences, and above all, at really high latitudes, especially south of the Antarctic Convergence, diatoms become all-im portant.

A comparison between the nanoplankton and larger net phytoplankton has recently been made by Teixeira (1963) and Teixeira and Kutner (1963) for Brazilian waters. In the shitllow lagoon waters, the net plankton, consisting mainly of large diatoms, comprised only about 3% of the total which was dominated by the nmoplankton; but even in offshore waters up to 400 miles from the coast the dominance of the nanoplankton was still very clear, with the net plankton contributing less than a fifth to the total standing crop. A f13w nanoplankton species seem characteristic of polluted waters with high organic content (e.g. Ryther, 1954), but in general these very small algae are particularly adapted to oligotrophic waters where they may contribute considerably to the overall production. Thus in Teixeira's investigations, it appeared that the net plankton contributed only 10% to total photosynthetic activity in offshore waters when the 14C method. was used.

IV. PHYTOPLANKTON CROP AND ANNUAL PRODUCTION The size of standing crop is a most significant factor in total produc-

tion since rate is reckoned as the amount of cai-bon (or organic matter) synthesized per unit of carbon (or organic mcitter) present as phytoplankton. In general, as Steemann Nielsen has pointed out (1958b; F'

158 J. E. ct. RAYMONT

1963), arms of high standing crop tend to have fairly high productivity rates (cf. Holmes, 1958, 1962; Bogorov, 1958). High latitudes tend to have very high plankton productivity for a short period of the year. Boreal regions also usually have a higher standing crop and productivity; Bogorov (1958) states that in the Pacific, the boreal area is some 10 times richer than tropical waters (cf. Holmes, 1958). The earlier work of Hentschel and Wattenberg (1930) also associates the distribution of phosphate in the southern Atlantic Ocean with the richness in density of plankton organisms.

In relation to total production the standing crop under a square metre of sea surface is of importance. Riley et al. (1949) suggest that in the offshore waters of the north-western Atlantic the total crop of phytoplankton beneath a square metre of surface at lower latitudes may not be very much smaller than that at a higher latitude, such as the Gulf of Maine, provided that the very short spring burst of phytoplankton in boreal waters, which may not be effectively utilized, is omitted from the calculation. One of the chief factors in calculating the crop beneath a unit of surface at different latitudes is the greater depth of the photosynthetic zone in more tropical areas. Riley’s comparison of the total annual crop in the Gulf of Maine area and in the continental slope water to the south-east suggests that the difference in biomass is not very great, largely owing to the greater depth of the euphotic zone in the more southern waters. With Sargasso Sea waters, however, the total population is probably lower even though the photosynthetic zone is greater. Ryther and Yentsch (1958) have shown that although offshore waters can occasionally show high rates of production which are comparable to inshore areas, these are due to temporary enrichment and are not sustained; production over a whole year is greater st inshore stations. Their suggestions for the annual production from the nutrient rich Long Island Sound waters to the impoverished Sargasso Sea are:

gC/m2/year

Long Island Sound = 380

Shelf waters = 160-100 (depending largely on distance from coast)

Ryther (1963) has summarized regional differences in annual productivity: (1) for tropical open oceans, production is 18-50 g C/m2, (e.g. Sargasso) though where some mixing occurs as off Bermuda the annual value may reach 70 g C/m2.

North Sargasso’Sea = 78.

THE PRODUCTION O F M A R I N E P L A N K T O N 159

(2) in temperate and subpolar waters rates arc! about 70-120 g C/m2. A t high latitudes very high rates may hold for E,hort periods (even up to 5 g C/m2/day) but the flowering period is short. (3) Antarctic production - approximately 100 g C/m2/year except for especially rich zones (e.g. South Georgia). (4) Arctic - very low production in true Arctic - perhaps < 1 g C/ m2/year in Polar Sea.

Apart from very shallow, highly productive inshore areas, continental shelf waters do not exceed offshore regions at the same latitude very greatly. The timing of the phytoplankton cycle may be strongly affected, and the crop per unit volume is far higher.

Both Anderson (1964) and Teixeira (1963) suggest that productivity and standing crop are both much higher in inshore waters than offshore in temperate and tropical regions respectively. Ketchum et al. (1958) point out that tropical oceanic waters may sometimes show high rates of production, but in general the net photosynthetic production in tropical oceanic waters is low; nutrient impotrerishment of the surface layers and the lack of effective vertical mixing probably causes the phytoplankton to be in less “healthy” cordition, so reducing the effective production over the year. Yentsch and Vaccaro (1958) point out that nitrogen deficiency causes a reduction in chlorophyll, and may also lead to temporaiy disbalance in the chlorophyl1:carotenoid ratio. Steele (1962) and Steele and Baird (1962) have demonstrated that the chlorophyl1:carbon ratio is influenced by nutrient level, thus in turn affecting productivity.

A factor in the total production of a column of sea water is not only the depth of the euphotic zone but also the precise distribution of the algal cells. In earlier considerations of critical depth it was assumed that the algae were regularly distributed throughout the photosynthetic zone so that production rate decreased logaritl-.mically from the surface (cf. Fig. 6). We know little of the precise distribution of phytoplankton throughout the euphotic zone at high latitudes; the photosynthetic zone is relatively thin and continual wave action may give a reasonably equal distribution, though the recent study by ‘Burkholder and Sieburth (1 961) for Antarctic waters suggested that the maximum chlorophyll concentration occurred at the surface. Halldal (1953) observed a fairly even distribution of phytoplankton in Norwegian Sea waters with a deep mixed layer, but in July, August and September when stratification was obvious, the majority of the aigae were massed in the upper 25m. In tropical waters, surface inhibition of photoeynthesis has been clearly demonstrated, and a maximum of phytoplankton is frequently found at some depth in the photosynthetic zone (e.g. Menzel and Ryther,

160 J . E. G . R A Y M O N T

1960; 1961). Hulburt, Ryther, and Guillard (1960) found in the seas off Bermuda that the phytoplankton at 50m depth was always richer than at the surface; usually different species were represented also at the two levels. Several recent investigations indicate, indeed, that the phytoplankton maximum in warmer waters may be near the bottom of the euphotic zone. In temperate latitudes during winter the photosynthetic zone is extremely shallow; there may be surface algal maxima temporarily, but mixing is usually active. In spring and summer the phytoplankton may by no means be equally distributed, and with surface inhibition, there may be a maximum somewhat below the surface (cf. Anderson, 1964). Sometimes, where a marked thermocline occurs, maximum density of algae may be associated with this layer. For example, in the Black Sea a thermocline occurs at a depth of about 20m and at this level there is a maximum of phytoplankton although the total depth of the euphotic zone approaches 60m (Sorokin, 1964a). Steemann Nielsen (1964a) has drawn attention to the importance of the vertical distribution of phytoplankton throughout the euphotic zone in relation to production under a unit of surface. In tropical latitudes, or in temperate latitudes during bright summer days, overall production may be markedly increased by a greater density of phytoplankton at somewhat deeper levels. By contrast, at temperate latitudes with average or poor light conditions, production may be increased by a more or less regular distribution of phytoplankton or even by having algae massed nearer the surface. In the tropics, if plankton were equally distributed from the surface throughout the euphotic zone, the rate of production would be maximal at some intermediate depth (ca. 20m). Only with a reduction of incident light to 50% throughout the day would maximal production approach the surface.

V. GRAZING BY ZOOPLANKTON Although the standing crop of phytoplankton is closely related to

overall production beneath a square metre of surface, the size of standing crop may be at times misleading since the quantity of algae removed by grazing, essentially by the zooplankton, is not taken into consideration. Harvey et al. (1935) drew attention to the remarkable reduction in phytoplankton crop immediately following the spring outburst in English Channel waters and noted that this was accompanied by marked grazing activity of the increasing zooplankton population. Over the summer, Harvey et al. concluded that although replenishment of nutrients from below the thermocline limited production, the generally rather low, but fluctuating, phytoplankton crop waa largely determined by the rate of grazing of the zooplankton. Regenera- tion of nutrients within the euphotic zone was also important. Clarke

THE PRODUCTION O F MARINE FLANKTON 161

(1939) also believed that over the productive periods of phytoplankton growth in temperate latitudes, the zooplankton was largely responsible for regulating the size of plant population. The importance of grazing activity had been noted in Arctic waters by Braarud (1935), by Bigelow et al. (1940) for the Gulf of Maine, by Wimpeiiny (1936, 1938) for the North Sea, by Holmes (1956) in the Labrador Sea, by Hart (1942) for the Antarctic, and in other areas. Grazing intensity of course may vary, especially at high latitudes. Thus Halldal (1953) considers that in the Norwegian Sea it was much more intensive in spring than later in the year. In very productive areas, such as Long Island Sound (Riley, 1956; 1959), Block Island Sound (Riley, 1952) and Tisbury Great Pond (Deevey, 1948), the phytoplankton crop may be rich, and grazing appears to exert little influence on the density of the algae (cf. also Gross et al., 1947). Despite these exceptions, the effect of the herbivorous zooplankton - appendicularians and salps, a majority of copepod species, many euphausids, the shelled pteropods, cladocerans and many meroplanktonic larvae - on the phytoplankton crop can be remarkable. The rapid reduction in phytoplankton crop seen in temperate and high latitudes may therefore not be a result of nutrient lack but of grazing activity.

Cushing et al. (1963) deal with the relations between a Calanus population feeding on a phytoplankton burst in the North Sea over a period from March to June. From a comparison of the crop of phytoplankton present and the estimated rate of algal production, he believes that grazing is the dominant cause of algal mortality; there was no evidence of a lack of nutrients during the erdy decline in the algal population. Grazing is believed to be the niajor controlling factor, according to Cushing, in the temperate spring outburst of phytoplankton. With intensive grazing there is considerable regeneration of nutrients in the euphotic zone, and only when the rate of regeneration decreases does the reduction in concentration of nutrients due to the thermocline becoming a limiting factor.

Harvey et al. (1935) obtained a minimal estimate of overall production of phytoplankton from the reduction in nutrier.t level over the period of the spring increase. For 1933, density was estimated at 85 000 plant pigment units/m3,* whereas the actual value of the standing crop was only 2 500 units/m3. For the following year, Harvey found that the standing crop was only 2-3% of the estimated total production. Hart (1 942), following Harvey’s calculations, suggested that the standing crop of phytoplankton in the highly productive South Georgia region of the Antarctic was only 2% of the calculated production; for oceanic

* Arbitrary pigment units were used as a measuremimt of chlorophyll before pure chlorophyll was used aa the standard method of estimation.


Antarctic areas the grazing activity was so intense that the standing crop was only 0.5% of the calculated productions. A number of workers (Riley, 1946; Gauld, 1950; Cushing, 1950a and b; Mare, 1940) have noticed the relatively small standing crop of plant plankton when zooplankton density is high. But the time relations between phytoplankton and zooplankton growth must be remembered; a zooplankton population can graze down plant cells in a matter of a few days, although the animals grow and reproduce more slowly. On the other hand, a relatively small algal population can reproduce exceedingly quickly, and thus with good growth conditions and in absence of grazers, can become a very dense population in a few days. The importance of this time factor in phytoplankton/zooplankton relationships has been well emphasized by both Steemann Nielsen (1937, 1963) and Clarke (1939).

The importance of grazing as a factor in phytoplankton production has led to a number of mathematical treatments. Fleming (1939) expressed the difference between an initial population of phytoplankton and the population at some time interval as the “increment”. Clearly total production can be equivalent to increment only if no death of cells or removal by grazing occurs. Most workers agree that relatively little natural mortality of algal phytoplankton normally occurs, but an animal population may remove a considerable proportion of the phytoplankton by grazing. Fleming proposed the term “yield” for the difference between the total production and the increment, assuming that the difference was due to the removal of algae by zooplankton alone.

Fleming proposed an equation :

- _ - P(a - (b + ct)) dP dt

This expresses the rate of change of a phytoplankton population (P), where a = rate of division of the phytoplankton cells assumed constant over a period; b = initial grazing rate; c = the increase of grazing rate which is assumed to be linear. If the grazing rate is assumed t o be constant and if (a - b) is positive (i.e. if the rate of division of the phytoplankton exceeds the constant grazing rate) then the phytoplankton population must continue to increase. However, the rate of increase in density of the algae is slower than the true rate of division owing to the constant grazing. The actual population increase may be so slow that the phytoplankton appears hardly to change a t all although the actual fraction per day removed by grazers may be very considerable. If the rate of grazing exceeds the algal reproduction rate the population will decline, and if grazing is very intense may lead to a typical rapid reduction following the spring bloom.

Fleming integrated his equation using values for phytoplankton and


zooplankton coefficients suggested by Harvey, and obtained a sym- metrical curve for the algal population change which agreed fairly well with field observations. He also computed the total production of algae, assuming a cell division rate of one division in 36 hours and that this rate remained constant over the period iinder investigation. The peak in standing crop was achieved in 37 days, and the total production was calculated over double this period, by which time the crop had declined to a very low value. Fleming obtained a calculated total production for the whole period of > 80 000 pigment units - a value which agreed remarkably well with Harvey’E estimate from nutrient depletion. Thus the yield increased enormously in the second month of the spring increase and the standing crop was a mere fraction of the total population (cf. Fig. 8).

Feb. Mar. Apr.

FIG. 8. Calculated total production, total yield, and population baaed on observations of Harvey et al. Total yield represents total amount removod by grazing (assumed rate of division once in 36 hours); (from Fleming, 1939; reprintel from “Plankton and Produc- tivity in the Oceans”, Pergamon Press).

Riley and Bumpus (1946) have also emph:tsized the importance of grazing on Georges Bank. After the expected phytoplankton winter minimum, there is a spring burst, followed by a decline. The zooplankton which is also low in winter over tht: Bank rises rather more slowly than the phytoplankton, but! with increasing speed from about May onward. There is therefore 8 positive correlation between the phytoplankton and zooplankton in winter and early spring, but this changes to a marked negative correlation during May. A number of zooplankton species showed this same change, though the exact time of

164 J . E . G . R A Y M O N T

the onset of the negative correlation depended on the month when the zooplankton species reached its seasonal peak. Riley and Bumpus con- clude that while the early correlation is due to some beneficial factor such as increasing temperature, common to both phytoplankton and zooplankton, the sharp change to an inverse relationship in May is due to the grazing activity of the zooplankton. The authors have also calculated that while the percentage of the phytoplankton production consumed by the zooplankton is relatively small (less than 10%) until April, it rises sharply in May to over 40%.

Riley (1946, 1963) has developed a mathematical model somewhat similar to that proposed by Fleming for the rate of increase in a phytoplankton population. He believed that SO-SO% of the phytoplankton variations on Georges Bank (Gulf of Maine) could be accounted for in terms of depth and illumination, temperature, nutrients (phosphate and nitrate) and zooplankton density. The relationship may be expressed :

- = P(Ph - R - G ) dP dt

where P is the total phytoplankton population, expressed per unit area’ of sea surface; P h = photosynthetic coefficient; R = coefficient of phytoplankton respiration ; G = zooplankton grazing coefficient. Riley states that these must be regarded as ecological variables rather than constants. Photosynthesis was found to vary more or less linearly with incident illumination during winter and early spring. It may thus be assumed to vary similarly with depth. By experiment, a photosynthetic constant (p) was established: its value, if light intensity is measured as g cal/cm2/min was 2.5. Thus:

P h = PI (where p is ca. 2.5)

Illumination decreases logarithmically in the sea so that at depth z the illumination I, is:

I, = I,e-kz

(where I, is the incident illumination, and k is the extinction coefficient). Riley assumed a limiting depth for photosynthesis where the light intensity was 0.0015 g cal/cm2/min (i.e. this is the compensation intensity). If the depth a t this intensity is z (i.e. the depth of the euphotic zone), then an average photosynthetic rate may be computed for the whole euphotic zone by integrating the illumination from the compensation depth to the surface and dividing by the depth. Thus:

T H E P R O D U C T I O N O F M A R I N E PLANKTON 165

The rate will also be affected by nutrient depletion, designated as N. For phosphate, this is believed to vary with the concentration below a maximum of 0.55 pg atoms P/1 (i.e. 16 mgP/ni3).

If the thickness of the mixed layer is greater than the euphotic zone, turbulence (V) will also reduce the photosynthetic rate. Riley suggests that the depth of the mixed layer may be somewhat arbitrarily defined as the maximum depth a t which the density does not exceed the surface density by more than 0-02 at units. Thus:

depth of euphotic zone depth of mixed layer

______ V =

(provided mixed layer is the greater). Thus:

As regards R =respiration rate of the algae, temperature must be taken into account. Thus:

RT = RoerT

(where RT = respiration a t temperature T ; R, a t temperature 0 " ; and r is a constant for the rate of change in respiration with temperature). This value has been experimentally determined as 0.069 for a 10°C increase.

Lastly the grazing rate G may be stated as:

G = gZ

where g is the rate of reduction of phytoplankton per unit of animals; Z is the quantity of herbivorous zooplankton. It' is likely that g will vary with temperature, though perhaps not lineaiily ; different broods of herbivores and of course specific differences may affect the grazing rate also. An approximation can be arrived a t from the minimum daily food requirements of Calanus as deduced from the respiratory rate. Riley supposes a daily food intake of from 1'2% (winter) to 7.1% (summer), and calculates an average value for g from these data. Thus:

dP d t - = P(Ph - R, - G )

becomes :

166 J . E. Q. RAYMONT

The rate of change of phytoplankton population may be expressed therefore in terms of five ecological parameters : solar radiation, transparency of water, depth of mixed layer, temperature, and zooplankton quantity.

Riley obtained average numerical values from seasonal field data from Georges Bank. Over short periods of time approximate integration was possible, assuming a constant mean value for the variable over that period. A relative curve of seasonal change was obtained. By statistically determining the best fit of the curve for all the phytoplankton cruise data, the actual seasonal changes and the theoretical curve may be compared. Figure 9 shows the good measure of agreement.

FIQ. 9. The seaaonal cycle of phytoplankton calculated by approximate integration of the equation for the rate of change of the population. For comparison, observed quatitias of phytoplankton are shown as dots; (from Riley, 1946; reprinted from ‘‘Plankton and Productivity in the Oceans”, Pergamon Press).

Riley has applied the same methods to other areas showing seasonal phytoplankton cycles. In the coastal waters of New England off Woods Hole, the cycle is considerably different from that of Georges Bank owing to different values of some of the various parameters. Riley has been able to obtain again a fairly good agreement between the mathematical model and the field data. In a more recent study (Riley, 1963) he has been able to make a similar calculation for data obtained by Kokubo from Husan (Korea). The changes in the phytoplankton in these waters differed quire appreciably over the two years, but the theoretical and field data agreed very well. The autumn of 1932 waa more favourable to phytoplankton owing to light, nutrients and sparse zooplankton (see Fig. 10).

The development of other models introducing certain refinements has been reviewed by Riley (1963). A correction may be introduced, for example, for the loss of algal crop due to sinking and death, apart from


the grazing activity of zooplankton. The phosphate distribution, as one of the major limiting nutrients in the upper lityers, may be computed by an assessment of the eddy diffusion in the water layers and the concentration of phosphate in deeper water. An equation for phytoplankton p at depth z, introducing these terms is as follows:

where v = sinking rate, p = density of water, A = coefficient of vertical eddy diffusion. Such a type of equation may be applied to two depth intervals to deduce grazing and sinking rates. A succession of depth

- .. . ,001 h Husan I \

I IAI 300

100

1932 1933

FIQ. 10. Comparison of observed seasonal cycles of phyboplankton (solid lines)] with theoretical cycles (dotted lines) at Husan; (from Riley, 1963; reprinted from “The Sea”, Interscience Publishers).

intervals from the surface to below the euphotic zone ks then studied in turn. Steele (1956) used this type of equation for calculating production on the Fladen ground and compared the production by 1% measurements with these theoretical calculations. The good measure of agreement in his results underlines the usefulness of such models. Cushing (1953) developed rather similar models, but includes the preying of zooplankton carnivores on the herbivorous members of the community, thus introducing another term in the mathematical equation. In a later study Cushing (1959a) developed a ldathematjcal model for studying an area in the North Sea over a period covering the spring outburst of phytoplankton. He believed that no significant depletion of nitrate and phosphate occurred during this increase and that regeneration of nutrients maintained the nutrient level. Thus the rats of change of the phytoplankton population was dependent on algal rates of division with changing light intensities and the depth of light penetration; on the

168 J. E. G. RAYMONT

thickness of the mixed layer; and on the rate of change of the zooplankton population. Cushing believes that grazing in this area of the North Sea was so intense that practically the whole of the production was grazed down over the spring outburst so that the final standing crop was extremely small. Other models have been developed recently by Steele and Baird (1962), but it is agreed generally that until we have greater knowledge of the precise physiology of algae, and especially of the factors affecting grazing and the rates of change of the zooplankton population, we cannot obtain much more accurate pictures of the seasonal changes in phytoplankton.

VI. ZOOPLANKTON Although the zooplankton grazes upon the phytoplankton and

therefore temporally and spatially the two populations may show some alternation, over the broad oceans, areas of rich zooplankton corre- spond to productive phytoplankton regions (Steemann Nielsen, 1958b, 1962b). At any latitude there is also a marked tendency for shallow coastal regions and for submarine banks to have a richer phytoplankton and a correspondingly higher zooplankton crop than deep oceanic regions. Such observations on zooplankton abundance are founded upon biomass and not on a rate of production of zooplankt,on. Even biomass of zooplankton, however, is open to varied interpretation since the methods for sampling zooplankton are by no means accurate or uniform (cf. Zooplankton Symposium, 1962).

A. METHODS FOR ESTIMATING THE STANDING CROP O F ZOOPLANKTON

Essentially almost all methods for estimating zooplankton crop rely upon the catching power of fine mesh nets, usually of nylon or silk. Mesh size is, therefore, of the utmost significance and poses problems of selection. Whilst a few species of zooplankton may measure several centimetres in length, few plankton animals exceed a few millimetres in size. A whole range exists however from those of several miilimetres, the macroplankton, to the very small-sized protozoans, especially small ciliates and flagellates, measuring a few p in diameter. The finest silk nets (200 mesh per inch) will capture the very young, small, stages and eggs of planktonic animals, as well as rneroplanktonic larvae, the smallest copepods, appendicularians, an'd similar small animals, providing quantitative estimates. Such fine nets filter too slowly and too small a volume of water to sample quantitatively the larger, more active, zooplankton - euphausids, the larger copepods, chaetognaths, mysids and especially large pelagic decapods. Relatively coarse nets can be used for the macroplankton, but between these two extremes every mesh size selects a particular range of zooplankton. Even the finest silk nets do


not catch the very smallest protozoans quantitatively, and these must be sampled by other methods. Recently, high-speed samplers such as the Isaacs Kidd mid-water trawl have been developed to sample large volumes of water and to obtain samples over considerable areas. While such techniques are of great advantage in estimating the distribution of the larger forms, alone they cannot give an accurate quantitative sampling of the whole zooplankton.

Another problem is the clogging of the meshes. In a rich phytoplankton bloom the filtration power of a net may be so reduced that it prevents quantitative sampling. Equally, certain of the more gelatinous zooplankton such as salps, medusae, ctenophores and siphonophores, when abundant, may clog the meshes of the net and reduce filtration. Some salps, jelly-fish and ctenophores show a marked tendency at times to intensive swarming. Not only will the net tend to be clogged in passing through such populations, but any quantitative sampling is always made more difficult if the zooplankton has marked patchy distribution. Even apart from salps and ctenophores, patchiness is an extremely common feature of zooplankton distribution.

Various types of meter have been developed to measure the actual volume of water passing through nets. Usually they are placed in the mouth of the net. While such devices increase the accuracy of volume measurements, their presence may reduce catching power, and some animals may actively avoid the mouth of the net.

The whole problem of the proper sampling of the zooplankton is dependent on precise knowledge of vertical distribution. Unfortunately zooplankton varies enormously in its vert'ical distribution; often there is a rich layer close to the surface and another maximum at a depth approaching a thousand metres. The work of Leavitt (1935, 1938), Jespersen (1935), Sewell (1948), Zenkevitc h and Birstein (1956), Vinogradov (1962a) and Hardy and Gunther (1936), all deal with the problem of the vertical distribution of animal plankton. Though there is fairly general agreement that very deep wa,ter has reduced populations, there appears to be no clear pattern of general distribution. In Arctic as well as Antarctic seas (cf. Hardy and Gunther, 1936; Zenke- vitch, 1963; Johnson, 1963) there is a marked tendency for the greater biomass of zooplankton to be beneath the surface layers but the distribution varies. Moreover, the zooplankton is characteristically marked by vertical migration. This may occur diurnally, and more especially in colder waters, there may be marked seasonal migration. The problem of correct quantitative assessment of the richness of various strata thus becomes more difficult.

Apart from the problem of catching plankton quantitatively there is the question of estimating the catch. The direct numerical count is


laborious and time consuming, and the taxonomic identification of the great variety of zooplankton species is difficult. Even if this is done, numbers of various zooplankton animals may not be a satisfactory index to the crop, the size and biomass of species varying enormously. Wiborg (1954) and others have estimated the relative volumes of the major zooplankton representatives, and thus computed the volume of the crop. Another widely used method is to measure the total volume of the zooplankton haul, usually by a displacement technique or estimate of settled volume. This is open to error if the catch contains a considerable proportion of the more gelatinous zooplankton. Many investigators attempt to avoid this error by first removing such animals as salps, medusae and siphonophores. A pump-and-hose method is used by some research workers to avoid the errors associated with nets. While useful for quantitative work in shallow water, it is inapplicable to oceanic depths.

For the measurement of zooplankton biomass, volume is obviously imperfect; a better estimate would be wet weight of crop or dry organic weight. One of the few observations employing these methods is that of Curl (1962b) who studied the biomass of plankton south of New York. Curl includes data for converting wet and dry weights, and carbon, nitrogen and phosphorus content for various species of zooplankton. He emphasizes that organic weight is the best unit for biomass, but for general assessments of zooplankton crop it would be difficult to use organic weight methods. In any event, the problem of selection of net mesh size is still a major difficulty. The symposium held on zooplankton estimation (Rapports et Proces Verbaux, 1962) emphasized the di%% culties of agreeing on standardization. Wickstead (1963) has recently suggested that two nets of different mesh size should be vertically hauled together. The recent discovery of an abundant population of zooplankton animals living right at the surface in oceanic regions poses again problems for the correct sampling for this particular layer.

B. REGIONAL CROP ASSESSMENTS O F ZOOPLANKTON

Despite the difficulty of estimating zooplankton, the crop tends to be richest where primary production and the size of standing crop of phytoplankton tend to be high (Steemann Nielsen, 1958b; 196213). The work of Hentschel (1933-36) in the southern Atlantic Ocean demonstrated the remarkable agreement between the quantities of phytoplankton and the crop of zooplankton, despite seasonal and other fluctuations. A recent survey by Reid (1962) for the Pacific Ocean also indicates good correspondence between the phosphate concentration of the upper waters, suggesting high primary production and the volumes of zooplankton. There are several broad oceanic surveys which demon-

THE PRODUCTION O F MARINE !?LANKTON 171

strate the relative abundance of zooplankton i n colder, boreal waters as compared with the low crop in warm seas. Jespersen (1924) found that although there may be considerable variations in zooplankton abundance in warmer waters, for instance, in the Atlantic considerably greater quantities of zooplankton were found north of the Azores than off the American coast and near Bermuda, the boreal regions were much richer. Thus in subtropical and tropical regions, plankton volumes varied from less than a litre to two litres an hour; in the northern Atlantic west of Ireland, Jespersen found volumes approaching 7-8 litres per hour; and in the colder seas north of Scotland much greater amounts approaching 18 or 19 litres per hour. In general, Jespersen suggests that for the open oceans the average crop of zooplankton in cold northern waters is at least some eight times that of tropical seas. Such waters are characterized by low nutrient level and poor production. Wherever in tropical regions upwelling brings nutrients to the surface, increased primary production is accompanied by richer zooplankton. King and Hida (1957) have recentby recorded a new area of abundance in the region of upwelling and divergence in the equatorial central Pacific. A summary of the varying standing crops of zooplankton in different oceanic regions is given by Hela and Laevastu (1962).

One of the problems in comparing zooplankton production at low and high latitudes is that the seasonal abundance of zooplankton shows very wide changes at higher latitudes. By contrast, though there is usually some seasonal change and though different species may breed at different times of the year, in general in warm seas .bhe fluctuations are comparatively small. In Indian waters the zooplankton as a whole shows some fluctuations in abundance over the year and this is probably associated with the monsoon affecting phytoplankton production. Wickstead (1958) demonstrated changes similar to the spring and autumn peak of zooplankton production in the Singapore Straits, probably associated with monsoon weather conditions. Moore ( 1949) suggested for waters round Bermuda that the zooplankton under these more oceanic conditions showed relatively little seasonal fluctuation, and Menzel and Ryther (196lb) found a small spring maximum of zooplankton in the Sargasso Sea, but as a whole the fluctuation was small with a low standing crop of zooplankton. Bsharah (1957) found in the Florida current region a small seasonal fluctuation in plankton, but the maximum averaged no more than two or three times that for the remainder of the year.

By contrast in temperate and high latitudes the abundance of plankton in spring and summer shows a remarkable increase over winter, and frequently there may be a peak production in late summer

172 J . E . G . R A Y M O N T

or early autumn. The amplitude from winter minimum to annual maximum may be a t least 40 times, with inshore waters (cf. Russell and Colman, 1934) showing fluctuations far greater than 40 times. High latitudes may show an enormous increase in zooplankton volumes over the productive season (cf. Fish, 1954 for the Labrador Sea).

A typical cycle of zooplankton seasonal changes in northern temperate waters comes from the work of Harvey et al. (1935); from a minimum in January - February there was a rise in zooplankton to a maximum in spring and a second maximum occurs in late summer. The zooplankton was dominated by copepods. Deevey (1956) dealing with the zooplankton in Long Island Sound and Block Island Sound also found marked seasonal fluctuation in zooplankton with the maximum in summer. Wiborg (1954) recorded a spring or early summer peak in zooplankton and a second rise between August and October, the chief contributor to this reproductive cycle being the copepods. Digby (1954) observed a later summer maximum for Greenland waters when the volume was some 20 times that of the winter minimum. Fish (1954 and Kielhorn (1952) found very great changes in zooplankton abundance between summer and winter with a maximum about July and August in waters of the Labrador Sea. Comparative work in the Antarctic (e.g. Mackintosh, 1934; 1937) suggests that a rapid increase in the zooplankton occurs during the spring and summer and that a peak value is achieved during the Antarctic summer, about February. By the late summer the population is declining again and reaches low values over winter.

To some extent, however, this pattern can be changed by vertical migration. Foxton (1956) has stated that seasonal variations in plankton volume in the Antarctic are much reduced if sampling is continued down to at least a thousand metres depth. Hansen (1960) also refers to this problem of vertical migration and the biomass of zooplankton with reference to the Norwegian Sea. Hansen was investigating mainly the upper 50 metres, and in the open Norwegian Sea the average biomass in June was some 30 times that for the minimum period in November/ December. This, however, was partly explained by a marked migration especially of copepods. I n coastal waters, where some of the neritic copepods remained nearer the surface, the fluctuation between summer and winter was not nearly so great.

Despite seasonal fluctuations, however, zooplankton at high latitudes tends to be more abundant than in warm waters, and at any latitude neritic plankton tends to be richer. Clarke (1940) investigated the waters south-east of New York and found them to be very much richer than in the area of mixing between the continental slope and the Gulf Stream to the south-east. The fluctuations between winter and summer in the


coastal waters were far greater ( x 20 to x 40) than in the “slope” water (some x lo), but the average volume of zooplankton in the coastal zone was about 4 times greater than in the “slope” area. In the Sargasso Sea, Clarke found that the average volume of plankton hauls was much less - only approximately one-quarter that of the “slope” stations. The seasonal fluctuation in the Sargasso was negligible.

Foxton (1956) also found that the mean volume of zooplankton increased fairly steadily from the subtropics through the sub-antarctic to Antarctic areas. He believes that the standing crop in the Antarctic was at least 4 times that of tropical southern areas; even then the Antarctic plankton may not have been adequately sampled. There was some indication of a reduction at the highest latitudes. Certainly in the northern hemisphere at the very highest lakitudes it appears that the biomass of zooplankton is very much reduced. Zenkevitch (1963) has summarized the general quantitative distribution of zooplankton in northern seas. Allowing for the fact that the zooplankton in very cold seas may be richer in the lower layers, it appears from the work of Russian investigators that the total biomass of zooplankton is very low in the Polar basin. In the area north of Siberia the markedly lower salinity may affect the biomass, but the gene]-a1 low productivity of Polar waters is reflected in the low zooplankton crop. Figure 11 illustrates the remarkable rise in zooplankton density from low numbers in the warmer Pacific seas, through high numbers in boreal waters, and the very sharp reduction in really Arctic areas. As regards the Arctic and sub-Arctic seas of the U.S.S.R., Zenkevitch points out that the south-western Barents Sea is by far the most productive. A zooplankton biomass up to 2 000 mg/m3 was recorded in the summer in some areas, but even for the whole Barents Sea, the mean annual biomass is quoted as 140 mg/m3. As compared with this, the biomass in the colder seas is much lower; thus in the Laptev Sea and the eastern Siberian Sea Zenkevitch quotes Jashnov that even in the summer, the biomass does not exceed 72 mg/m3 on average. But Zenkevitch points out that in the more central Arctic basin there seems to be a very significant decrease in zooplankton. He quotes only 12 mg/m3 in the upper 100 metres; a rise to nearly 30 mg/m3 in an intermediate layer; but only some 7 mg/m3 in the deep layer below 800 metrlss. Johnson (1963) also refers to the low standing crop of zooplankton in the Arctic basin. This agrees with the very low primary production.

A summary of the biomass of zooplankton, as measured by displacement volume, is given by Bigelow and Sears (1939) for areas of the northern Atlantic. Seas around Iceland, the Faroes and the north of Scotland appear to be especially rich. Bigelow and Sears suggest that the continental shelf waters off the north-east coast of U.S.A. rank next in

174 J. E. G . RAYMONT

quantity for the northern Atlantic. There is a considerable seasonal fluctuation but the summer maximum (0.7-0.8 cc/m3) compares favourably with that of the North Sea and is considerably higher than the volume of zooplankton in the English Channel (cf. Table V).

Tranter (1962) has studied the biomass of zooplankton in Australian seas. Oceanic regions, except where upwelling occurs, have a low crop - normally < 25 mg/m3 (wet biomass weight). Continental shelf areas had a higher crop, and inshore shallow stations, for example a t Port

3000

n E - ._ c 2000

VI c

E ._ 0

3 L

0 1000

8 n

z 5

Inn 1 2 4

-ILL 6 7 8

FIG. 11. Change in number of specimens per ma from tropical part of Pacific Ocean (l), through northern part of the Pacific (2, 3), Bering Sea (4, 5), Chukotsk Sea (6, 7), and Arctic Basin (8) - after Brodsky, 1956; (redrawn and modified from Zenkevitch, 1963).

Hacking, even larger amounts. At times the Port Hacking plankton included large numbers of salps, but if these are excluded, the biomass (> 200 mg/m3) is still higher than offshore. Tranter uses a conversion factor to compare his data with plankton volumes recorded by Bigelow and Sears. He also includes zooplankton quantities obtained by Russian workers from the Pacific and converts these data to plankton volumes (Table V). Tranter’s values for oceanic Australian waters (0.02-0.05 cc/m3) are similar to those of the Russian investigators for the subtropical Pacific. The richer equatorial Pacific area (0.1 cc/m3) is approximately equivalent to Australian shelf waters. But in large area of the boreal northern Pacific zooplankton volumes are very much greater, reaching even 1.0 cc/m3 in summer, and being maintained throughout the year at amounts exceeding 0-5 cc/m3. Zenkevitch (1963) quotes very high quantities for the summer zooplankton of far northern Pacific seas. If the same conversion factor be applied to his data to


obtain approximate plankton volumes, the plankton during the summer in the Bering Sea and Sea of Okhotsk exceeds 1.0 cc/mJ (Table V). Similar values are found in summer in the sou:h-western Barents Sea. By contrast the biomass in the Laptev and eastern Siberian Sea is low (0.07 cc/m3) and is even more reduced in the central Arctic basin (Table V).

Regional comparisons of biomass arc usual1.r. expressed in terms of unit volume, and the density of zooplankton is of the utmost significance for the nutrition of higher trophic levels. But with the great difference in depth between coastal and oceanic regions, the biomass beneath a unit area of sea surface is sometimes considered. Riley et al. (1949) compared the production beneath a square metre of sea surface for coastal areas south of New York, for the semitrcpical Sargasso Sea area, and for the mixed continental slope water between. Riley found that the inshore water showed its typical greater richness; the mean ratios for the volumes of zooplankton of the three areas: coastal, “slope”, and tropical waters, were approximately 10: 4: 1. Oceanic plankton also appears to have a generally lower organic content. Despite the greater depth of oceanic areas and the much greater crop fluctuations near shore, especially in coastal boreal waters, Riley’s investigations generally confirm the original view that tropical waters are usually poorer in zooplankton biomass than temperate waters, especially inshore areas.

Grice and Hart (1962) provide a more recent comparison for approximately the same region. They investigated the zooplankton of the upper two hundred metres of water between New York and Bermuda and confirmed the richness of the coastal areas. In numerical abundance, the ratio between coastal, “slope” and Sargasso Sea waters averaged some 22 : 4: 1. By volume, the same comparison yielded ratios of approximately 50:3:1. Their results confirmed the very much greater seasonal fluctuations in neritic waters (approximately x 30) as compared with the subtropical Sargasso waters (approximately x 4). Although in coastal regions virtually the whole column of water from surface to bottom was sampled, but only the upper 200 meixes in oceanic stations, the greater richness of coastal waters is still evident. The volume in the coastal area exceeds that of most boreal northern Atlantic regions. The very low quantity found for the Sargasso Sea is similar to the values suggested for subtropical Pacific and Australian oceanic regions (Table V).

Despite the low biomass of zooplanktoil in trol ical waters, apart from areas of upwelling or divergence, it has been suggested, notably by Cushing (1959a and b), that in tropical oceans in view af the more rapid utilization and regeneration of nutrients the system of plankton production may be more efficient even though gross production is much lower


than at high latitudes. The standing crop of phytoplankton is small and as the different members of the zooplankton in tropical waters tend to breed at different periods of the year, there is always a fairly ateady grazing population and the phytoplankton never blooms excessively.

TABLE V Comparison of Volumes of Zooplankton from Different Oceanic

and Coastal Regions ~~ - _ _ . _

Plankton volume (cma/ma)

Region Winter Summer

Northern Atlantic - Iceland Faroes, Greenland 0-84*

~~~~ ~~

Authority

Coastal shelf, north-eastern U.S.A. 0.2-0.3 0.7-0.8 ~ i ~ ~ l ~ ~ and sears (1939) North Sea 0-5-0-6

~ _ _ _ _

English Channel 0-1 ____

Laptev and eastern Siberian Sea 0.07 Central Arctic Basin 0.01

Sea of Japan 0.03-0.5 1.0 Zenkevitch (1983) Okhotsk Sea 1 -&3 *O Bering Sea 1 *5-2 *5

___

Pearly Mean ~ ~~~

Barents Sea 0.14 Zenkevitch (1963)

Australian oceanic waters 0.02-0 *05

Australian shelf waters 0.1 Trantor (1982)

Australian inshore waters > 0.2

Subtropical Pacific < 0.05

Equatorial Pacific 0.1

Boreal northern Pacific 0.5-1-0

Russian data quoted by Tranter (1982)

New York- Bermuda Coastal waters Slope waters Sargasso waters

1 *07 0.27 Grice and Harb (1962) 0.02

Most of smaller copepods not included owing to mesh size.

T H E P R O D U C T I O N O F M A R I N E P L A N K T O N 177

The relationship between the phytoplankton and the zooplankton therefore approaches a steady state; continuous grazing releases excretory material which is rapidly remineralized, and the nutrient concentration remains very low as it is continuously utilized. The opposite condition is seen in colder waters where typically an enormous early burst of phytoplankton is followed by very heavy grazing, but frequently there is a considerable time lag between the increase in phytoplankton and the rise in the zooplankton herbivores. Only when the crop of phytoplankton has been sufficiently reduced does new regeneration take place. This concept of the very efficient use of primary production in warmer waters has been supported more recently by the work of other investigators. For example Menzel and Ryther (1961) have found that off Bermuda the zooplankton uses almost 100% of the production of algae. Grice and Hart (1962) suggest a remarkably efficient utilization of the phytoplankton in Sargasso waters, the herbivores showing far greater diversity of species than in neritic and. in boreal waters. Pre- sumably the herbivores are more specifically adapted to utilize the various types of food efficiently; they perhaps have very specialized food requirements. Grice and Hart also call actention to the balance between herbivores and carnivorous groups in the zooplankton. In warm subtropical waters about half the zooplankton is herbivorous as against 65 yo in neritic boreal areas. Two predominantly carnivorous groups (the chaetognaths and siphonophores) were also much more important in warm tropical waters in respect to the zooplankton as a whole than in the coastal areas. In tropical waters therefore, not only is the herbivorous plankton utilizing the phytopbnkton as efficiently as possible, but it would appear that the herbivore population is kept in delicate balance with the carnivorous forms. In coastal and boreal waters there may be an excessive production of herbivorous plankton following a phytoplankton outburst. This may account in part for the sudden great swarms of salps which Grice and Hart observed in the more neritic areas. Steemann Nielsen (196213, 1963) has pointed out that in warm oligotrophic waters the herbivores mush search out their food and the greater depth of the euphotic zone will make greater energy demands on the zooplankton for the food obtained. Since less of the food aseimilated is presumably available for growth and reproduction, it is likely that the zooplankton will be longer-lived. The ratio between the standing stock and the rate of production for both herbivorous and carnivorous plankton animals will vary, but it will tend to be higher in oligotrophic areas than in the nutrient-richer wihxs of temperate and higher latitudes. In these typically richer regions any factors which allow phytoplankton growth to start more slowly, and so allow the zooplankton to begin grazing down the phytoplankton crop, will prevent

178 J. E. C,. RAYMONT

the enormous burst, of phytoplankton typical of high latitudes. Stee- mann Nielsen believes that such “explosions” of phytoplankton occur only if a very rapid burst of algal growth precedes the reproduction of the zooplankton. Thus with particularly good light conditions and the rapid stabilization of the upper water layers, the rapid algal bloom typical of neritic areas may get ahead of zooplankton growth. More generally the relationship between phytoplankton and zooplankton is probably more stable. This “wastefulness” in production at higher latitudes may be only apparent; material not consumed or only partly digested by the zooplankton may be used effectively by other members of the marine eco-system. Vinogradov (196213) has suggested that excessively rich algal crops may also supply food to deep layers through extensive vertical migrations of the zooplankton. Although some bathypelagic zooplankton may feed on detritus, many will be filter feeders migrating periodically towards the surface. When such plankton descends again their faeces and their bodies may be preyed on by zooplankton of the mid-water strata. The total biomass of the intermediate layers may thus be greater since these can be made up not only of filter feeders which migrate but of predators and detrital feeders. The amount of detritus descending to deeper levels is probably very small and is relatively resistant, so that the biomass of zooplankt,on at great depths is much reduced. In the deep sea as in oligotrophic shallower layers there is presumably a delicate balance between the herbivorous and carnivorous population.

At high latitudes the breeding, especially of herbivorous copepods, is largely influenced by phytoplankton outbursts though Heinrich (1 962) states that some copepods breed before the phytoplankton outburst. Grainger (1959) suggests that while the herbivorous copepods at high latitudes breed essentially near the time of the major phytoplankton growth and show enormous fluctuations in population, the carnivorous forms do not show nearly as great numerical changes seasonally and may breed at different times of the year. This is perhaps borne out by the observations of Dunbar (1946, 1962) on chaetognaths and amphipods; for example, Sagitta elegans arctica appears to have a very long spawning period (July to February) in Arctic waters and the spawning time does not depend on food availability.

c. RATE O F ZOOPLANKTON PRODUCTION

So far discussion has been limited to the standing crop of zooplankton; estimation is difficult and our knowledge is limited. But estimates of tfhe rates of production of zooplankton are even more difficult. One of the earliest attempts was that of Riley (1947). Over the region of Georgea Bank, Riley proposed that the size of the herbivore population (H)

THE PRODUCTION O F MARINE F’LANKTON 179

which made up the bulk of the zooplankton a t a time t might be expressed by the equation:

where A = rate of assimilation of food by herbivores H - H e(A-R-C-D)t

t - 0

R = herbivore respiration rate C = rate of consumption of herbivores by predators D = herbivore death rate.

An estimate of the rate of assimilation may be deduced indirectly from the phytoplankton density and the known grazing rates of copepods. Over the period of the spring increase, however, allowance must be made for excessive grazing by the copepods. Riley assumed a maximum limit for assimilation equal to 8% of the animal’s weight per day. As regards herbivore respiration rate, laboratory experimental results may be used. Thus the respiration of Calanus gives an indication of the loss of matter due to respiration, due regard being paid to the effect of temperature. Riley uses the seasonal changes in the population of Sagitta elegans, which he regards as the main zooplankton predator on Georges Bank, to estimate the rate of predation. A constant was determined statistically for the amount of matter consumed per unit predator, and predation was considered proportional to the niimbers of Sagitta.

The herbivore death rate (D) which includes such things as natural death, dilution, etc., was also deduced statistically.

v E \ V

Observed zoopbmkton popJlalion 0- 4

Colculaled popdolion - -

(b) 20 -

10 -

- P’

/’ ‘%n +Feb Mnr Apr May dun Jul plug k p Oct Nov Dec

FIG. 12. (a) The rate of growth of the zooplankton on Georges Bank. (b) Calculated end observed seasonal variations in zooplankton demity on Georges Bank; (from Riley, 1947; reprinted from “Plankton 5nd Productivity in the Ooeene”, Pergemon Press).

180 J. E . a. RAYMONT

Figure 12a shows the rate of change of a population of zooplankton obtained by Riley using the various coefficients calculated. An approximate integration of the curve may be obtained by employing mean value for the factors in the equation over short time intervals. This theoretical curve has been fitted to the field data for Georges Bank - there is a considerable measure of agreement between the actual and theoretical curves (cf. Fig. 12b).

Cushing (1959a) used a mathematical model to assess the production of Calanus and other small copepods as the herbivore plankton in the North Sea over a period of six months. He deduced the rate of increase of the algae from the light energy available at various depths during the six months (cf. p. 167), and estimated the grazing rate from the minimal food requirements necessary for maintenance, reckoning also the rate of increase of the herbivorous copepods. His analysis of this rate of increase is especially interesting as he obtained his data from the egg production of Calanus in relation to food concentration. Marshall and Om had already shown that egg production appears to be a function of food concentration. Cushing estimated the percentage mortality for juvenile stages of Calanus and the mortality of the adults for various weekly periods between January and June. The production of Cabnus and of other herbivores over the six-month period is shown in Fig. 13. Cush- ing’s results suggested that the copepods were undernourished during the first months of the year, but they fed excessively over t,he main period of phytoplankton production. This apparent “wastefulness” of production in boreal waters has already been noted.

Details of the rates of production of zooplankton must, however, depend on a far wider and more accurate knowledge of the biology and especially of the physiology of plankton animals. Even our knowledge of breeding cycles of zooplankton is limited; we know fairly accurately the breeding cycles of a few species of copepods, of a few euphausids, some amphipods and sagittae. Most of these are boreal species; knowledge of the breeding of tropical plankton is especially lacking, and deep- sea plankton is virtually unknown as regards its breeding habits.

Since zooplankton is so difficult to keep in the laboratory the effect of various environmental factors on reproductive rate, especially the effect of food supply, is almost unknown. The work of many investigators, notably Marshall and Orr’ (1956), dealt with the stimulating effect of food on reproduction in Calanus. Marshall (1949) also suggested that abundant diatoms increased the production of other copepods. Barnes (1957) indicated a stimulating influence of phytoplankton production on the liberation of cirripede nauplii. Edmondson (1962) demonstrated that the density of phytoplankton was related to successful reproduction of copepods and other animals. Work on bivalve larvae, summarized

THE PRODUCTION O F MARINE I'LANKTON 181

by Loosanoff and Davis (1963), alao indicates the importance of an adequate food concentration for the rearing of various species. While such observations demonstrate repeatedly the importance of food supply on egg and larval production, we do not have detailed and accurate knowledge of the precise operation of this factor. The tank

1.'

0.

0.0

L

x 0 .- Y Y 5" 0.00

c

0.000

0.0000

i

FIQ. 13. The theoretical production of algae, and of Calanm and "other copepods" as mg wet weight per litre for the period January to June; (from Cushhg, 1969; reprinted from "Plankton and Productivity in the Oceans", Pergamon Press). 0

182 J. E . a. RAYMONT

culture of zooplankton with fertilization experiments (e.g. Raymont and Miller, 1962) has also not yielded precise data on the rate of zooplankton production in relation to phytoplankton crop. Investigations by Reeve (1963) have made an important contribution in dealing with the efficiency of utilization of phytoplankton, even though the species studied (Artemia) is not a marine plankton animal. Our knowledge of the metabolism of zooplankton animals is excessively limited, though Conover (1 962) has maintained Calunus hyperboreus for considerable periods of time and has been able to relate feeding to activity, and to respiration, and to make some estimates of efficiency and growth. A survey of our knowledge of aspects of metabolism, including utilization of food, excretion, and respiration (Raymont, 1963) reveals that data on maintenance and growth requirements and even of the metabolic food reserves of zooplankton are very 1imit)ed (cf. Raymont et al., 1964).

Investigations of the metabolism of plankton have been handicapped because of the difficulties of culturing zooplankton species in the laboratory. Although it is possible to obtain egg production from Calanus Jinmarchicus and C. hyperboreus, and to rear various stages, so far the culture of successive generations has eluded us. Jacobs (1961) made an important contribution in growing Pseudodiaptmus coronutwr in the laboratory through several generations, using phytoplankton aa food, but this copepod is not a truly planktonic species. The most important recent advance is that of Zillioux and Wilson* (unpublished) who bred Acartia tonsa through five successive generations using phytoplankton cultures as food. Continuation of such experiments should allow the medium and the food requirements of planktonic animals to be accurately defined, as with the work of Provasoli and his colleagues (e.g. Shiraishi and Provasoli, 1959) on the nonplanktonic copepod Tigriopw. Only then can we study adequately the factors affecting the metabolism and growth of plankton animals. Meanwhile mathematical models help us to appreciate the problems and point the way to future research.

D. THE FEEDING OF ZOOPLANKTON

The trophic relationships of animal plankton species is a complex problem. Perhaps the copepods are best known for their food requirements and of these Calanus has been particularly studied. An excellent summary is included in the work of Marshall and Om (1955): a wide variety of diatoms is utilized as food, from the large Coscinodiscus and Ditylum to the smaller species such as Skebtonema and Nitzmhia closterium. Dinoflagellates such as Peridinium, Gymnodinium, md Prorocentrum are also widely eaten, but there is some selection; for

I am greatly indebted to the authors for permission to use the unpublished data


example, Ceratium is apparently not taken. Sinall nanoplankton flagellates can also be consumed, though these must probably exceed 2-3p diameter; a small species such as Nannochhis may not therefore be retained. Marshall and Orr have also studied the problem of the suita- bility of phytoplankton species as nourishment, using oviposition as a criterion. Thus, while all diatoms appeared to be useful as food, only some flagellates were satisfactory. For example, diets of Dicrateria, Hemiselmis and Chlorella apparently did not contribute to egg production. Beklemishev (1 954) found that the copepads Calanus spp. , Metridia spp., and Eucalanus consumed mainly diatoms in northern Pacific waters; larger cells were definitely crushed by tbe mouth parts. In more southern latitudes, more flagellates, dinoflagelltrtes and coccolithophores were also eaten, and this was probably true during the summer months in more temperate waters.

With small copepods such as Pseudocalanus, Parmalanus, Tenma, and Acartia, the diet appears to be rather similar, mainly diatoms and certain flagellates (cf. Gauld, 1951; Raymont, 1959; Raymont, 1963), but differences exist. Thus Conover (1956) has suggested that although Acartia feeds on a wide variety of phytoplankton, the setae are rather coarse so that Acartia tends to be a ‘‘wasteful” feeder. More interesting differences arise however with species such aEs Centropages, Labidocera and Anomalocera which appear to be at least partly carnivorous. Anraku and Omori (1963) confkm that certain calanoid species differ in their feeding habits. They examined the mou1;h parts of the calanoids and made feeding experiments using diatoms, animal food (Artemia nauplii), and a mixture of the two. Results showed that whereas Calanus Jinmurchicus was essentially herbivorous, Acurtia tonsa, Centropages hamatus and Centropages typicus were essentially omni- vorous, with Centropages apparently preferring animal food. LabicEocera was almost entirely predatory, and this applied even more strongly to Tortanus discaudatus (cf. Kaymont, 1963). Gauld (1964) agrees that Anomalocera and Labidocera are essentially carnivorous, and that Centropages, Temora and Acartia take some animal food. This problem of differences in the food eaten, even in one group of zooplankton animals, applies particularly to deep-living speoies. Thus Beklemishev found that deep living copepods such as Caidius and Uwtanus consumed large diatoms, and Conover (1960) has shown conclusively that Calanus hyperboreus, though a deep-living species, is essentially herbivorous. On the other hand, other deep-water species such as Bathy- calanus and Eucheirella are in all probability partial carnivores, and Euchaeta, Scottocalanus, Megacalanus, and Valdiviella, amongst others, are almost certainly carnivores. Perhaps even essentially herbivorous species may take some animal food when food h3 scarce.


Although a species such as Calunus appears to feed on a wide variety of phytoplankton there may be some selection. Harvey (1937) found that the copepod selected Lauderia in preference to Chaetoceros or Nitzschia. Mullin (1963) tested 4 species of Calunus on 8 different food species of phytoplankton. The larger-celled species were selected; from a mixture of 5 food species, the smaller nanoplankton algae contributed less than 6% to the diet. Petipa (1959) claims a considerable degree of food selection for Acartia spp. from the Black Sea.

Less is known of the diet of other groups, but among the euphausids Euphausia superba (Barkley, 1940) appears to be exclusively a herbivore, feeding on diatoms, probably selecting the smoother celled, smaller species. On the other hand, species of Thysanoessa and Megany- ctiphanes are believed by Einarsson (1945) to be essentially detritus feeders or carnivores. Work in the Clyde sea area (Macdonald, 1927; Mauchline, 1959) suggests that Meganyctiphanes is largely a filter feeder in the smaller stages, while the larger older forms are mainly carnivorous on copepods and on other zooplankton; some detritus appears to be taken.

Some mysids filter phytoplankton effectively, and in shallow water may live on bottom material and detritus. Bathypelagic species are usually regarded as mainly carnivorous though some detritus is probably eaten. Ostracods were also thought to be filter feeders, but Cannon (1931; 1940) has shown that whereas Cypridina is a filter feeder, the large Gigantocypris mfilleri is apparently carnivorous. Loosanoff and his colleagues have investigated the food of bivalve larvae, especially those of Crassostrea and Venus mercenaria (Loosanoff and Davis, 1963). Food for young larval molluscs must be of suitable size; usually algal cells greater than lop in diameter cannot be ingested, but size is not the only factor. Thus bacteria and certain flagellates will not promote good growth in oyster larvae. Davis (1953) showed that 9 species of bacteria and 1 species of flagellate failed to produce growth, although 5 other flagellate species (Dicrateria, Hemiselmis, Isochrysis, Chromulina and Pyramimonm) all gave good growth. The requirements even changed with the age of oyster larvae. The larvae of Venus mercenaria appear t o be able to grow on Chlorellu and even on some bacterial cultures which are unsuitable for oyster larvae. However, for many bivalve larvae a mixture of Momchrysis and Isochrysis appears to be most suitable (cf. also Walne, 1963).

The specific food requirements of cirripede larvae have also been investigated. Early work suggested that diatoms and flagellates might be utilized, but the work of Costlow and Bookhout (1967, 1958) indicated that algal (Chlanzydomonas) food needed to be supplemented with a little animal (Arbacia eggs) material. Moyse (1963) has recently added


a more detailed study of the food requirements of different species of barnacles. Ohlorella and Dunaliella were valueless apparently for all species. Balanus balanoides was successfully reared on diatoms (Skele- tonema, Ditylum, Asterionella), but not on flagellate diet. On the other hand, Chthamalus could be reared on severd flagellate species, but diatoms were not utilized.

Most fish larvae, though they may take a small amount of phytoplankton food in early stages, feed mainly on zooplankton. Cod larvae feed on euphausids, decapod larvae, and other crustaceans; occasionally they take the larvae of other fishes (Wiborg, 1948a and b, 1949). Most investigators have emphasized the importance of copepods as food for larvae of fishes, and both Marak (1960) and Wiborg emphasize the question of size selection. However, there may be a greater degree of selectivity. Shelbourne (1963, 1957, 1962) showed that while small copepod nauplii were taken by larval plaice, the appendicularian Oiko- pleura was the most important constituent in the diet. Ryland (1964) has recently confirmed the overwhelming importance of both Oiko- pleura and Pritillaria as food for larval plaice. Except for fish larvae, our knowledge of the food habits of carnivorous zooplankton is particularly I fragmentary. Pelagic heteropods are known to feed on copepods but to a large extent on chaetognaths. Medusae and ctenophores are known to feed on copepods, on sagittae and on fish 1arva)e. The ctenophore Beroe feeds on Pleurobrachia; apparently in Russian waters it feeds exclusively on Bolinopsis. The siphonophores are an exclusively carnivorous group feeding on such zooplankton as copepods and other crustaceans, but recently, in Florida waters, Bayer (1963) ha:3 observed that Velella, Porpita, and even Physalia are themselves eaten by the snail Janthina. Although our knowledge is limited, the complexity of the zooplankton , food net is quite extraordinary. Our knowledge of the diet of bathypelagic plankton is far less. Most deep-sea plankton has been regarded as filtering out detritus particles, or being carnivorous on other plankton. Vinogradov (1962b) has pointed out that small particles will de- compose fairly rapidly during their descent into the deep layers and , probably only the resistant non-assimilable fraction remains.

The problem of how far bacteria might add to the food of zooplankton has been investigated to some extent, mainly with surface plankton animals, chiefly copepods and bivalve larvae. I11 general, bacteria seem to be unimportant. In any event, in really deep water most micro- biologists suggest that the bacterial population is very much reduced; there is doubt whether it could add significantlj to the diet of the larger zooplankton. It is possible that bathypelagi c plankton (copepods, mysids, and decapods) could filter off Radiolaria and Foraminifera occurring in the deeper water layers (cf. Vinogrsdov, 1962b). We do not


know the specific requirements of these protozoans, but some Radio- laria might consume bacteria. Murray (1963) suggests that Foraminifera can feed on dead material and possibly on detritus and bacteria, though living phytoplankton appears to be preferred. However, the recent work of Freudenthal and his colleagues (unpublished),* using labelled food cultures, shows that planktonic Foraminifera prefer Nitzschia and some flagellates; bacteria although ingested apparently do not contribute to the nutrition.

Vinogradov (1962b) suggests that zooplankton from intermediate depths by extensive diurnal vertical migrations obtains food from the upper water layers. Faecal pellets produced by this migrating plankton may assist with the nutrition of the plankton of the deeper layers. Apart from these coarse filter feeders, the majority of the deep-sea plankton will be carnivorous.

E. ALTERNATIVE FOOD SOURCES FOR ZOOPLANKTON

The kdings of Bernard, Wood, and others that various Protophyta may occur in the deep layers of the ocean, far below the euphotic zone, implies that these plant cells may also serve as food for deep-sea zooplankton. However, the amount of food available to deep-sea plankton must be extremely limited. There is little doubt as Zenkevitch and Birstein (1956) have suggested that deep-sea plankton is very reduced in density. Vinogradov (1962a) has commented on the extraordinarily rapid reduction of biomass of zooplankton in really deep water. At high latitudes, for example, he suggests that the biomass below 6 0001 metrea is only l/lOOOth that of the uppermost water layers. Although Vino- gradov believes that few deep-sea animals feed mainly on detritus, this may be an important accessory food. Investigations, especially summarized by Krey (1961), suggest that detritus can account for a very large fraction of the total organic suspended matter; this is true even of the surface layers where the contribution from living plankton may be expected to be high. In deeper water the actual quantity of orgmio matter is much lower, but the proportion of detritus may reach almost 100%. In a later study, Krey (1964) shows that despite considerable fluctuations in the amount of suspended matter, there is a marked tendency for the amount to fall with depth and in very deep water extremely little material is present. This Krey attributes partly to the eating of material by organisms in the upper layers, but above all to the mineralization processes occurring in deep water. The fraction of living material in the total suspended matter shows, as would be expected, 8 remarkably sharp fall in really deep water.

Although the very small amount of suspended material in deep waters * I em much indebted to the authors for permission to use their data.


may be used by filter feeding animals, there is in relative terms a far greater amount of dissolved organic material (of. Duursma, 1961). Putter (1909, 1925) suggested that this dissolved malker might be used as food by marine animals, but direct experiment indicates that even if meta- zoans can absorb such substances, the gain in energy will be negligible. But small protozoans might utilize dissolved organic material effectively. Apart from relatively large planktonic protozoans such as Radiolaria and Foraminifera, there may be a considerable population of very small protozoans, particularly ciliates, in the seas. If such ciliates could feed on the dissolved matter, they in turn could serve as the base of a food chain leading to metazoan bathypelagic plankton.

Heterotrophic bacteria are certainly able to use dissolved organic material, and in forming particulate living substance, they could serve as food for Protozoa, or in turn, for Metazoa. Elven though Metazoa may not filter bacteria directly, a food chain through larger Protozoa could build up a useful food supply in deep water. The problem, however, largely turns on the density of heterotrophio bacteria in deep-water layers. Plating techniques and direct counts can give markedly variable assessments of the bacterial population. Moreover it is almost impossible to separate bacteria quantitatively by filtralion; a considerable proportion of the bacteria will pass even very fine filters and thus comparisons of the amount of particulate organic matter left on the filter and of the so-called “dissolved” organic maliter passing through the filter cannot give a correct assessment of the bacterial population. To a large extent bacterial substance will be included in the “dissolved” organic fraction. Earlier observations summarized by Zobell (1946) suggest that deep water has relatively small populations of bacteria. Kriss (1963), however, indicated that even in deep-water layers there may be considerable populations of heterotrophic bacteria, especially in tropical waters, which Kriss considered richer in organic material. The recent investigations of Sorokin (1 964b) throw doubt on these rich populations of heterotrophic bacteria in deep water. Even a limited heterotrophic bacterial population, in providing particulate material for higher trophic levels, would be of great advantage in deep water. Parsons and Strickland (1962) have attempted an assessment, and have assumed a value of 0.1 mg. per m3 as the standing crop of micro- heterotrophs. Assuming a growth rate similar to the phytoplankton, they obtain a production equivalent to about 0.5 - 1% of that due to photosynthetic organisms. But bacteria can exist through the whole column of water, and even though their denriity is much reduced at deeper levels, their contribution to the production of particulate living matter may not be inconsiderable.

Another possible source of particulate food for the zooplankton in the

188 J . E . a. RAYMONT

oceans appears from the recent investigations of Baylor and SutcliBe (1963). They observed that particulate organic matter may be formed in sea water when active foaming occurs from the dissolved organic matter. Riley (1963b) also discusses the adsorption of dissolved organic matter onto the surface of bubbles to form particles. Such particles consist not only of organic aggregates, but have interstices which may then trap bacteria and even plankton and inorganic material. Bacteria and protozoans may use this substrate and in turn these particles may serve as food for zooplankton. Riley has shown that this organic aggre- gate material may be an important accessory food source in inshore waters. How far such material may be formed in deeper water, where presumably bubbles are absent, is uncertain. Whatever particulate material is present could presumably serve as a surface for the adsorption of dissolved organic material. Thus the detritus may not be only relatively non-assimilable matter.

F. ZOOPLANKTON - QUANTITATIVE FOOD REQULREMENTS

There are several suggested routes, by which the reservoir of dissolved organic matter in the oceans might be transformed into particulate material, but there is little possibility yet of any quantitative assessment. Indeed, even the quantitative particulate food requirements of individual species of zooplankton are but poorly known. Few species have been accurately studied, and most investigations have centred round assessing filtration rates in filter feeders, or in measuring respiration rates to estimate metabolic requirements (cf. Raymont, 1963). An indication of the quantitative dietary needs of zooplankton arises from work on copepods, chiefly Calanus.

Despite considerable variations in filtration rate recorded by investigators, a mean rate of 70 cm3/Calanus/day appears to be generally acceptable. Experiments by Marshall and Orr (1955) using phytoplankton food labelled with 32P and W, however, have suggested rather lower values. With rates of the order of 70 cm3/day, the average phytoplankton crop in temperate waters should be sufficient to cover maintenance requirements. But at times of the year phytoplankton is scarce and it seems unlikely that all the herbivorous plankton will find enough food, not only for maintenance, but for growth and reproduction. However, we may be misled by thinking of herbivores as automatic filterers. Several workers have suggested that food may be actively sought, and Cushing (1959a) has proposed from his “encounter feeding theory” that considerably greater quantities of food may be secured. Gauld (1964) points out that some copepods (Acartia, Centropages, Temora, Pseudo- calanus and perhaps Calanus) can feed by a sweeping movement of the maxillae (“scoop net feeding”) as well as by the usual filtration method.

THE P R O D U C T I O N O F M A R I N E PLANKTON 189

The amount of food collected by these two methods may be very different, and the extent to which each meclianism is used depends in part on the type of food available. Carnivorous copepods (Anomahera, Labidocera) use the sweeping movements of the maxillae to secure their prey and this mechanism is also used by partly carnivorous species such as Temora and Centropages. Cushing ( 1964) believes that considerable superfluous feeding occurs with herbivorous copepods such as Calanus (cf. Beklemishev, 1962). Active reproduction is limited to such periods of excessive feeding. Even so, a considerable quantity of food is “wasted”. Cushing believes that very high grazing rates are typical of Calanu-s, but when there is extensive searching for limited food, egg production ceases. Petipa (1959) believes tihat the average dietary requirements of Acartia in the Black Sea, amounting to 4% of body biomass per day, cannot normally be met without the inclusion of a considerable amount of zooplankton food. Animal food plays a particularly important part during periods of activt: reproduction.

The investigations of Corner (1961) and of Cowey and Corner (1963) tend to show that sufficient food material for Calanus is present in sea water. They analysed the total amount of particulate matter in the water and then related this to the maintenance requirements. During winter, they suggest that Calanus needs to filter only 30 cm3/day, and in summer some 50 cm3/day. Marshall and Orr (1964) have listed the amounts of phytoplankton organic matter itnd the total particulate organic matter in different marine areas. Although the quantities in coastal waters are relatively high and appear to be sufficient for the requirements of copepods, the amounts in open oceans and in deep water are very much lower and would certainly seem to be inadequate for herbivorous zooplankton. Even in inshore waters the seasonal variation in total particulate organic matter is not well known. Marshall and Orr suggest that while during a spring diatom increase a great excess of food is present, it is doubtful whether in winter the amount available would cover requirements. The food requirements for a number of copepod species based on respiration rates are given. Some of the daily requirements appear to be very high; moreover far more food will be required for growth and reproduction. Further detailed metabolic studies are needed before we can measure these additional food requirements. A comparison of the metabolic needs and the body reserves for some zooplankton, however, has suggested that the requirements may be exceedingly high (Conover and Raymont, unpublished; Anraku, 1964).

VII. CONCLUSION Primary production in the oceans is mainly dependent on phytoplank-

ton, though in shallow coastal waters the important contribution of the Q.


benthic microflora and macroflora has probably been underestimated. Oceanic areas a t low latitudes may show, over short periods, high rates of primary production owing to temporary nutrient enrichment, but in general the low level of the major plant nutrients (nitrate and phosphate) in tropical and subtropical areas, with the permanent thermocline restricting vertical mixing, markedly limits annual productivity, despite the much greater depth of the illuminated zone. In temperate and sub-polar regions, although production rates vary markedly over the year owing to the great seasonal differences in depth of light penetration, the greater nutrient concentration leads to increased annual production. At high latitudes, very high rates of production may hold for short periods, but the time of abundance tends to be short. Productivity in the Antarctic is high; in the highest Arctic latitudes, however, the annual production is very low. Upwelling areas in lower latitudes show greatly increased production.

The effect of temperature on productivity is essentially indirect since its main influence is on the stabilization of the upper water layers. In a few areas salinity differences may also assist in stabilizing the upper water layers and thus may affect production. The establishment of a seasonal thermocline sharply limits production but the drop in phytoplankton crop in temperate and higher latitudes during early spring is more often due to grazing than to nutrient lack. The effect of a dis- continuity layer in reducing replenishment of nutrients from deeper layers has its main effect on phytoplankton production during the summer period. The direct regeneration of nutrients within the euphotic zone is therefore of primary importance in production over the summer period at higher latitudes; it is always of great significance at lower latitudes. Although trace elements and organic substances are required by many marine algae, there is little evidence for believing that decreased concentrations of these substances affect total production, except perhaps temporarily in some tropical oceanic areas. The varying amounts of such materials between inshore and offshore waters may, however, influence the composition of the phytoplankton population.

In general, areas of high primary production have large standing crops of algae; the temporal variations in crop, especially at higher latitudes also usually parallel the changes in production, except that heavy grazing may reduce the crdp over summer. High densities of zooplankton are found only in regions of richer phytoplankton; a sparse distribution of algal cells involves the herbivorous zooplankton in excessive searching for food so that less energy is available for growth and reproduction. Some degree of “wastefulness” in the grazing of herbivores on the phytoplankton is likely at higher latitudes and is more generally true at all latitudes in neritic regions. The “wastefulness” arises mainly from


the blooms of phytoplankton and the growth of zooplankton being somewhat out of phase. Provided the blooming of the phytoplankton is not too accelerated, however, the “wastefulness” is not excessive and in any event the partly used phytoplankton crop serves as food for deeper living zooplankton and for the benthos.

Oceanic depths have a much reduced zooplankton population. The main limitation would appear to be the amount of particulate orgahic matter available as food. While the vertical migrations of the zooplankton to different levels in the oceans carries organic particles such as faecal pellets to greater depths where they can be used by the deeper filter-feeding zooplankton, the nutritive vitlue of such particles is probably not very high. Protozoa, especial1.y ciliates, feeding on the relatively much greater quantities of dissolved organic matter in the deep oceans, either directly or via bacteria, Sorm a second food source for filter-feeders. Some bathypelagic planktonic species may feed directly on bacteria but the density of micro-organisms in the open oceans is probably never high. Organic aggregates can be formed from dissolved organic matter in the oceans and this material may serve as another source of food for the zooplankton. At moderate depths in certain warmer seas the deeper-living phytoplankton may also form a subsidiary food supply.

Carnivorous species are always prominent in deep-sea zooplankton populations; they appear to be capable of feeding on a wide variety of planktonic animals.

The precise nutritive requirements are known only for very few species of zooplankton, mainly Culanus. In inshore waters phytoplankton production is more than sufficient for zooplankton growth and reproduction over the spring and summer; during winter the total quantity of particulate organic matter is probably also sufficient for maintenance requirements, if it is assumed th,at all such organic matter can be assimilated by the animals. The requirements of oceanic and especially of deep-sea zooplankton species art? virtually unknown, and the amount of particulate matter in the open oceans, especially at great depths, appears to be very limited. Any clear ,assessment of the production of oceanic zooplankton must await metabolic studies on oceanic species.

REFERENCES Abbott, B. C. and Ballantine, D. (1957). J . Mar. 13iol. Ass. U . K . 36, 169-189.

Toxin from Gymrwdinium venqficum Ballantine Allen, E. J. andNelson, E. W. (1910). J . Mar. Biol. .tiss. U.K. 8,421474. On the

artificial culture of marine plankton organism. Anderson, G. C. (1964). fimnol. & Oceumgr. 9,284-302. The seasonal and geo-

graphic distribution of primary productivity 08 the Washington and Oregon coasts.


Anraku, M. (1964). Limnol. & Oceunogr. 9, 195-206. Influence of the Cape Cod Canal on the hydrography and on the copepods in Buzzmda Bay and Cape Cod Bay, Massechusetta. I1 Respiration and feeding.

Anraku, M. and Omori, M. (1963). Limnol. & Oceunogr. 8, 116-126. Preliminary survey of the relationship between the feeding habit and the structure of the mouth-parts of marine copepods.

Ansell, A. D., Raymont, J. E. G., Lander, K. F., Crowley, E. and Shackley, P. (1963). Limnol. & Oceanogr. 8, 184-206. Studies on the maas culture of

Ansell, A. D., Coughlan, J., Lander, K. F. and Loosmore, F. A. (1964). Limnol. & Oceanogr. 9, 334-342. Studies on the mass culture of Phaeoo!m%ylum. IV.

Antia, N. J., McAllister, C. D., Parsons, T. R., Stephens, K. and Strickland, J. D. H. (1963). Limnol. & Oceanogr. 8, 166-183. Further measurements of primary production using a large-volume plastic sphere.

Austin, T. S. and Brock, V. E. (1959). Int. Ocean. Congress Prepints, A.A.A.S. Waahington 130-13 1. Meridional variations in some oceanographic and marine biological factors in the Central Pacific.

Barker, H. A. (1935). Arch. Mikrobiol. 6, 157-181. The culture and physiology of marine dinoflagellates.

Barkley, E. (1940). 2eit.fiir Fischerei der Hilfswissen. 1 (l) , 65-156. Nahrung und Filterapparat des Walkrebschens Euphausia superba Dana.

Barnes, H. (1957). Anned Biologique 33 (1-2), 67-85. Processes of restoration and synchronisation in marine ecology. The diatom increase and the spawning of the common barnacle, Balanus balanoides (L).

Bayer, F. M. (1963). Bull. Mar. Sci. Gulf Caribb. 13, 456466. Observations on pelagic molluscs associated with the siphonophores Velella and Physalk.

Baylor, E. R. and Sutcliffe, W. H. (1963). Limnol. & Oceanogr. 8, 369-371. Dissolved organic matter in seawater as a source of particulate food.

Beklemishev, K. V. (1954). Zool. J . Inst. Oceanol. A d . Sci. U.S.S.R. 33, 1210- 1229. Feeding of some common plankton copepods in Far Eastern Sees.

Beklemkhev, C. W. (1962). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 153, 108-1 13. Superfluous feeding of marine herbivorous zooplankton.

Belser, W. L. (1959). Int. Ocean. Congresa Preprints, A.A.A.S. Washington, 908-909. Bioassay of organic materials in sea water.

Belser, W. L. (1963). “The Sea”, Vol. 2 (M. N. Hill, ed.), Ch. 9, 220-231, “Bio- assay of trace substances.” New York and London: Interscience Publishers.

Bernard, F. (1939). J . Conseil int. Explor. Mer. 14, 228-241. g’tude sur lea variations de fertilit6 des eaux m6diterran&nnes.

Bernard, F. (1953). Deep Sea Res. 1, 34-46. RBle des flagell6s calcaires dam la fertilit6 et la s6dimentation en mer profonde.

Bernard, F. (1963). I n “Marine Microbiology” (C. H. Oppenheimer, ed.), Ch. 22, 215-228. Density of flagellates and Myxophyceae in the heterotrophic layers related to environment. Springfield, Ill.: Thomas.

Bernard, F. and Lecal, J. (1960). Bull. I&. Oceanogr. Monaco. No. 1166, 1-59. Plancton unicellulaire r6colt6 dans l’oc6an Indien par le “Charcot” ( 1950) et le “Norsel” (1955-56).

Bigelow, H. B. and Sears, M. (1939). Mem. Mua. Comp. Zool. (Harvard) 54, 183-378. Studies of the waters of the continental shelf, Cape Cod to Chese- peake Bay. 111. A volumetric study of the zooplankton.

Bigelow, H. B., Lillick, L. and Sears, M. (1940). Tram. Am. Phil. SOC. 31, 140- 191. Phytoplankton and planktonic protozoa of the offshore waters of the Gulf of Maine. Part I. Numerical distribution.

Phaeodactylum. 11.


Bogorov, B. G. (1958). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 144, 117-121. Estimates of primary production in biogeographical regionization of the ocean.

B r w d , T. (1935). Hval.Skr. Nr. 10,l-173. The 0st Expedition to the Denmark Strait 1929. 11. Phytoplankton.

Braarud, T. (1958). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 144, 17-19. Counting methods for determination of the standing crop of phytoplankton.

Braarud, T. (1961). In “Oceanography”, Public. No. 67 A.A.A.S. Washington D.C. (M. Sears, ed.), 271-298. Cultivation of mrtrine organisms as a means of understanding environmental influences on populations.

Braarud, T. (1962). J . Oceanogr. Xoc. Japan, 20th Ann. Vol., 628-649. Species distribution in marine phytoplankton.

Braarud, T. and Klem, A. (1931). Haal. Skr. No. 1, 1-88. Hydrographical and chemical investigations in the coastal waters off Msre.

Brongersma-Sanders, M. (1957). I n “Treatise on Marine Ecology and Paleoe- cology”, Vol. I Ecology. Memoir 67, Geol. SOC. Am. (J. W. Hedgpeth, ed.). Mass mortality in the sea.

Bsharah, L. (1957). Bull. Mar. Sci. Gulf Caribb. ‘7, 201-251. Plankton of the Florida current. V.

Burkholder, P. R. and Sieburth, J. M. (1961). Li,nnol. & Oceanogr. 6 , 45-52. Phytoplankton and chlorophyll in the Gerlac he and Bransfield Straits of Antarctica.

Bursa, A. S. (1963). I n “Marine Microbiology” (C. €I. Oppenheimer, ed.), Ch. 58, 625-628. Phytoplankton successions in the Canadian Arctic. Springfield, Ill.: Thomas.

Cannon, H. G. (1931). Discovery Repts. 2, 435-482. On the anatomy of a marine ostracod, Cypridinc (Doloria) levw Skogsberg.

Cannon, H. G. (1940). Discovery Repts. 19, 185-244. On the anatomy of Giganto- cypria miilleri.

Clarke, G. L. (1939). Quart. Rev. Biol. 14, 60-64. The relationship between diatoms and copepods aa a factor in the productivity of the sea.

Clarke, G. L. (1940). Biol. Bull. Woods Hole 78 , 226-255. Comparative richness of zooplankton in coastal and offshore arem of thtj Atlantic.

Clowes, A. J. (1950). Investigational Report No. 12. Division of Fisheries, Union of South Africa, Pretoria. 42 pp. An introducticn to the hydrology of South African Waters.

Clowes, A. J. (1954). Investigational Report No. 16. Division of Fisheries, Union of South Africa, Pretoria. 47 pp. The South African Pilchard (Surdinops ocellata).

Collier, A. (1953). Trans. N. Amer. Wild. Conf. March 18, 463-472. The significance of organic compounds in sea water.

Collier, A. (1958). Limnol. & Oceanogr. 3 , 33-39. Some biochemical aspects of red tides and related oceanographic problems.

Collier, A., Ray, S. and Wilson, W. B. (1956). Science 124, 220. Some effects of specific organic compounds on marine organism3.

Conover, R . J. (1956). Bull. Singham Oceanogr. Coll. 15, 156-233. Oceanography of Long Island Sound, 1952-54. VI. Biology of Acartia clausi and A . tonsa.

Conover, R. J. (1960). Biol. Bull. Woods Hole 119,399 -415. The feeding, beheviour and respiration of some marme planktonic Crus tecea.

Conover, R. J. (1962). Rapp. Proc. Verb. Cons. Pwm. Int. Explor. Mer. 153, 190-196. Metabolism and growth in Calanus hyperboreua in relation to ita life-cycle.

194 J. E. 0. RAYMONT

Conover, S. A. M. (1956). Bull. Bingham Oceanogr. Coll. 15,62-112. Oceanography of Long Island Sound, 1952-54. IV. Phytoplankton.

Cooper, L. H. N. (1933). J. Mar. Bwl. Ass. U.K. 18,729-753. Chemical constituents of biological importance in the English Channel, November 1930 to January 1932. Part 11.

Corcoran, E. F. and Alexander, J. E. (1963). Bull. Mar. Sci. Gulf. Caribb. 13, 527-541. Nutrient, chlorophyll and primary production studies in the Florida Current.

Corlett, J. (1953). J. Conseil. int. Explor. Mer. 19, 178-190. Net phytoplankton at ocean weather stations “I” and “J”.

Corner, E. D. S. (1961). J. Mar. Bwl. Ass. U .K . 41, 5-16. On the nutrition and metabolism of zooplankton. I.

Costlow, J. D. and Bookhout, C. G. (1957). Biol. Bull. Woo& Hole 112, 313-324. Larval development of B&nw eburneus in the laboratory.

Costlow, J. D. and Bookhout, C. G. (1958). Biol. Bull. Woo& Hole 114, 284-295. Larval development of B&nua amphitrite war. d e n t i c u b Broch reared in the laboratory.

Cowey, C. B. (1956). J. Mar. Bwl. Ass. U.K. 35, 609-620. A preliminary investigation of the variation of vitamin B,, in oceanic and coastal waters.

Cowey, C. B. and Corner, E. D. S. (1963). J. Mar. Biol. Ass. U.K. 43, 495-611. On the nutrition and metabolism of zooplankton. 11.

Curl, H. (1962a). Limnol. & Oceanogr. 7 , 422-424. Effect of divalent sulfur and vitamin B,, in controlling the distribution of Skeletonema costatum.

Curl, H. (1962b). R q p . Proc. Verb. Cons. Perm. Int. Explor. Mer. 153, 183-189. Standing crops of carbon, nitrogen and phosphorus and transfer between trophic levels in continental shelf waters south of New York.

Curl, H. and McLeod, G. C. (1961). J. Mar. Rea. 19, 70-88. The physiological ecology of a marine diatom, Skeletonema costatum (Grev.) Cleve.

Currie, R. I. (1959). Comm. svolte 47a Riunione della S.I.P.S., 107-113. The measurement of organic production and turnover rates in the sea.

Currie, R. I. (1962). Proc. Roy. SOC. A265, 341-346. Productivity. Cushing, D. H. (1953). J. Conseil int. Explor. Mer. 19, 3-22. Studies on plankton

populations. Cushing, D. H. (19598). Piah. Invest. Lo&, Series XI 22 (6), 1-40. On the nature

of production in the sea. Cushing, D. H. (1959b). J. Conseil int. Explor. Mer. 24, 455-464. The seasonal

variation in oceanic production cw a problem in population dynamics. Cushing, D. H. et al. (1963). J . Mar. Bwl. Ass. U . K . 43, 327-389. Studies on a

C&nua patch I - V. Cushing, D. H. (1964). In “Grazing in Terrestrial and Marine Environments”

(D. J. Crisp, ed.), 207-225. The work of grazing in the sea. Oxford: Blackwell Scientific Publications.

Daisley, K. W. and Fisher, L. R. (1958). J. Mar. BwZ. Ass. U.K. 37, 683-686. Vertical distribution of vitamin B,, in the sea.

Davis, H. C. (1953). Biol. Bull. Woo& Hole 104, 334-350. On food and feeding of larvae of the American oyster, C. virgirvica.

Deevey, G. B. (1948). Bull. Binghmn Oceanogr. Coll. 12, 1-44. Zooplankton of Tisbury Great Pond.

Deevey, G. B. (1966). Bull. Bingham Oceanogr. Coll. 15, 113-155. Oceanography of Long Island Sound, 1952-54. V. Zooplankton.

Digby, P. S. B. (1953). J. Anim. Ecol. 22, 289-322. Plankton production in Scoresby Sound, East Greenland.

THE PRODUCTION O F MARINE PLANKTON 195 Digby, P. S. B. (1954). J. Anim. Ecol. 28, 298-338. Biology of the marine plank-

tonic copepods of Scoresby Sound, East Greenland. Doty, M. S. and Oguri, M. (1956). J. Conseil int. Explor. Mer. 22, 33-37. The

island mass effect. Doty, M. S. and Oguri, M. (1957). Limnol. & Oceuriogr. 2, 37-40. Evidence for a

photosynthetic daily periodicity. Droop, M. R. (1957). J . Qen. Microbiol. 16, 286-293. Auxotrophy and organic

compounds in the nutrition of marine phytoplmkton. Dunbar, M. J. (1946). J. Fish. Rea. Bd. Canada 6, 419-434. On Themisto libellula

in B a h Island coastal waters. Dunbar, M. J. (1962). J . Mar. Res. 20, 7 6 9 1 . The Life-cycle ofSagitta elegans in

Arctic and sub-Arctic Seas, and the modifying effects of hydrographic differences in the environment.

Duursma, E. K. (1961). Nether lad J . Sea Res. 1, 1-147. Dissolved organic carbon, nitrogen and phosphorus in the sea.

Edmondson, W. T. (1962). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 153, 137-141. Food supply and reproduction of zooFlankton in relation to phytoplankton population.

Einarsson, H. (1945). Dana Repts. 27, Copenhagen. Euphausiacea. I. Northern Atlantic species.

Fish, C. J. (1925). Bull. U.S. Bur. Fish. 41, 91-179. Seasonal distribution of the plankton of the Woods Hole region.

Fish, C. J. (1954). Symposium on rnarine and freshwater plankton in the Indo- Paci$c. Bangkok, 3-9. Preliminary observations on the biology of Boreo- Arctic and subtropical oceanic zooplankton pol~ulations.

Fleming, R. H. (1939). J. Conseil int. Explor. Mer. 14, 210-227. The control of diatom populations by grazing.

Fogg. G. E. (1963). Brit. Phycol. Bull. 2 , 195-205. The role of algae in organic production in aquatic environments.

Foxton, P. (1956). Discovery Repts. 28, 193-235. Sanding crop of zooplankton in the Southern Ocean.

Gaarder, T. and Gran, H. H. (1927). Rapp. Proc. V v b . Cons. Perm. Innt. Explor. Mer. 42, 1-48. Production of plankton in the CIS10 Fjord.

Gauld, D. T. (1950). Proc. Roy. SOC. Edin. 64(B), 36-64. A fish cultivation experiment in an arm of a sea loch. 111. The plankton of Kyle Scotnish.

Gauld, D. T. (1951). J. Mar. Biol. Aes. U.K. 29, 695-706. The grazing rate of planktonic copepods.

Gauld, D. T. (1964). I n “Grazing in Terrestrial ,and Marine Environments” (D. J. Crisp, ed.), 239-245. Feeding in planktonic copepods. Oxford: Black- well Scientific Publications.

Gillbricht, M. (1959). Ber. Deut. WiSs. Komm. ikreeresforsch. 15(3), 260-276. Die planktonverteilung in der Irminger See im Juni 1955.

Grainger, E. H. (1959). J. Fish. Rea. Bd. Canada. 16, 453-501. The annual oceanographic cycle at Igloolik in the Canadian Arctic. I.

Gran, H. H. (1931). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 75, 37-46. On the conditions for the production of plankton in the ma.

Grice, G. D. and Hart, A. D. (1962). Ecol. Monogr. 32, 287-309. The abundance, seasonal occurrence and distribution of the epizooplankton between New York and Bermuda.

Grmtved, J. (1952). Medd. Komm. Dan. Fisk. Havwzd. Ser. Plankton. 5(5 ) , 1-49. Investigations on the phytoplankton in the Southern North Sea in May 1947.

196 J . E. G . RAYMONT

Grontved, J. (1960). Medd. Danmarks. Fisk. Havund., N.S. 3, 55-92. On the productivity of microbenthos and phytoplankton in some Danish fjords.

Grontved, J. (1962). Medd. Danmarks. Risk. Havund., N.S. 3, 347-378. Pre- liminary report on the productivity of microbenthos and phytoplankton in the Danish Wadden Sea.

Gross, F., Marshall, S. M., Orr, A. P. and Raymont, J. E. 0. (1947). Proc. Roy. SOC. Edin. 63(B), 1-95. An experiment in marine fish cultivation. I - V.

Gross, F., Nutman, S. R., Gauld, D. T. and Raymont, J. E. G. (1950). Proc. Roy. SOC. Edin. 64(B), 1-135. A fish cultivation experiment in an arm of a sea-loch. I-v.

Guillard, R. R. L. (1963). I n “Symposium on Marine Microbiology” (C. H. Oppenheimer, ed.), Ch. 9, 93-104. Organic sources of nitrogen for mirine centric diatoms. Springfield, Ill. : Thomas.

Guillard, R. R. L. and Cassie, V. (1963). Limnol. & Oceanogr. 8, 161-165. Minimum cyanocobalamin requirements of some marine centric diatoms.

Guillard, R. R. L. and Wmgersky, P. J. (1958). Limnol. & Oceanogr. 1, 449- 454. The production of extracellular carbohydratetes by tesome marine flagellates.

Gunter, G., Williams, R. H., Davis, C. C. and Walton Smith, F. G. (1948). EwZ. Monogr. 18, 310-324. Catastrophic mass mortality of marine animals and coincident phytoplankton bloom on the west coast of Florida, Nov. 1946 to August 1947.

Gunther, E. R. (1936). Discovery Repts. 13, 109-276. A report on oceanographical investigations in the Peru Coastal Current.

Halldal, P. (1953). Hval. Skr., Nr. 38, 1-91. Phytoplankton investigations from Weather Ship M in the Norwegian Sea. 1948-49.

Hansen, V. K. (1960). Medd. Dunmarks. Fisk. Havund., N.S. 2, 1-53. Investi- gations on the quantitative and qualitative distribution of zooplankton in the southern part of the Norwegian Sea.

Hardy, A. C. and Gunther, E. R. (1936). Discovery Repts. 11, 1-456. Plankton of the South Georgia whaling grounds and adjacent waters 1926-27.

Harris, E. (1959). Bull. Bingkm Oceanogr. Coll. 17, 31-65. The nitrogen cycle in Long Island Sound.

Hart, T. J. (1934). Discovery Repts. 8, 1-268. On the phytoplankton of the south- western Atlantic and the Bellingshausen Sea, 1929-31.

Hart, T. J. (1942). Dkcovery Repts. 21, 263-348. Phytoplankton periodicity in Antarctic surface waters.

Hart, T. J. (1953). Nature 171, 631-634. Plankton of Benguela Current. Hart, T. J. and Currie, R. I. (1960). Discovery Repts. 31, 123-298. The Benguele

Current. Harvey, H. W. (1937). J . Mur. Biol. Ass. U .K . 22, 97-100. Notes on selective

feeding by Cahnus. Harvey, H. W. (1950). J . Mar. Biol. Ass. U .K . 29, 97-136. On the productionof

living matter in the sea. Harvey, H. W. (1955). “The Chemistry and Fertility of Sea Water”, 224 pp.

Cambridge University Press. Harvey, H. W., Cooper, L. H. N., Lebour, M. V. and Russell, F. S. (1935). J . Mar.

Biol. Ass. U . K . 20, 407-441. Plankton production and its control. Heinrich, A. K. (1962). J . Conseil int. Ezplor. Mer. 27, 15-24. The life histories of

plankton animals and seasonal cycles of plankton communities in the oceans. Hela, I. and Laevastu, T. (1962). “Fisheries Hydrography”, 137 pp. London:

Fishing News (Books) Ltd.

,

THE P R O D U C T I O N O F M A R I N E P L A N K T O N 197

Hentschel, E. (1933-36). Wks. Ergebn. Deut. Athr t . Exped. “Meteor” 11, 1-344. Allgemeine Biologie des Siidatlantischen Ozeens.

Hentschel, E. and Wattenberg, H. (1930). Ann. Hya‘rogr. Berlin. 58,279. Plankton und Phosphat in der Oberflaschenschicht des Sudatlantischen Ozeans.

Hoffman, C. (1956). Kieler Meeresforsch. 12, 25-36. Untersuchungen !uber die Remineralisation des Phosphors im Plankton.

Holmes, R. W. (1966). Bull. Bingham Oceanogr. Cd. 16, 1-74. The annual cycle of phytoplankton in the Labrador Sea, 1956Ell.

Holmes, R. W. (1958). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 144, 109-1 16. Surface chlorophyll “A”, surface primary production and zooplankton volumes in the eastern Pacific Ocean.

Holmes, R. W. (1962). Limnol. & Oceanogr. Sup]). to 7 , 27-28. Marine phytoplankton - areal surveys.

Hood, D. W. (1963). Oceanogr. Mar. Biol. Ann. Rev. 1, 129-155. Chemical oceanography.

Hulburt, E. M. (1962). Limnol. & Oceanogr. 7 , 307-315. Phytoplankton in the southwestern Sargasso Sea and north equatorial current, February, 1961.

Hulburt, E. M. and Rodman, J. (1963). Limnol. &, Oceanogr. 8, 263-269. Distri- bution of phytoplankton species with respect to salinity between the coast of southern New England and Bermuda.

Hulburt, E. M., Ryther, J. H. and Guillard, R,. R. L. (1960). J. Conseil int. Explor. Mer. 25, 115-128. The phytoplankton of the Sergasso Sea off Bermuda.

Jacobs, J. (1961). Limnol. & Oceanogr. 6 , 443-446. Laboratory cultivation of the marine copepod Pseudodiaptomw coronatue Williams.

Jeffries, H. P. (1962). Limnol. & 0cean)ogr. 7 , 21-31. Environmental characteristics of Raritan Bay, a polluted estuary.

Jenkin, P. M. (1937). J. Mar. Biol. Ass. U.K. 22, 301-343. Oxygen production by the diatom Coscinodiscus excentricus Ehr. in relation to submarine illumination in the English Channel.

Jespersen, P. (1924). Int. Rev. ges. Hydrobiol. CB Hydrogr. 12, 102-115. On quantity of macroplankton in the Mediterranean and Atlantic.

Jespersen, P. (1935). Dana Rept. 7, 1-44. Quantitative investigations on the distribution of macroplankton in dserent oceanic regions.

Johnson, M. W. (1963). Limnol. & Oceanogr. 8, 89-102. Zooplankton collections from the high Polar Basin with special referenm to the Copepoda.

Johnston, R. (1964). J. Mar. Biol. Ass. U . K . 44, 87-109. Sea water, the natural medium of phytoplankton. 11. Trace metals and chelation, and general discussion.

Jones, E. C. (1962). J. Conseil int. Explor. Mer. 27, 223-231. Evidence of an island effect upon the standing crop of zooplankton near the Marquesas Island, Central Pacific.

Jones, P. G. W. and Haq, S. M. (1963). J. Conseil int. Explor. Mer. 28, 8-20. The distribution of Phaeocystis in the eastern Irish Sea.

Jsrgensen, E. G. and Steemann Nielsen, E. (1961) Physiol. Plant. 14, 896-908. Effect of filtrates from cultures of unicellular algae on the growth of Staphy. lococcus aurew.

Kanazawa, A. (1961). Memo. Fac. Fish. Kagoshimz Univ. 10, 38-69. Studies on the vitamin B-complex in marine algae I.

Kain, J. M. and Fogg, G. E. (1958). J. Mar. Biol. Ass. U . K . 37, 781-788. Studies on the growth of marine phytoplankton. 11. It:ochrysis galbana. Parke.

Ketchum, B. H. (1939). Amer. J . Bot. 26, 399-407. The absorption of phosphate and nitrate by illuminated cultures of Nitmchia dosterium.


Ketchum, B. H. (1962). Rapp. Proc. Verb. Cone. Pemn. Int. Explor. Mer. 158, 142-147. Regeneration of nutrients by zooplankton.

Ketchum, B. H. and Redfield, A. C. (1938). Biol. Bull. Woods Hole. 75, 166- 169. A method for maintaining a continuous supply of marine diatoms by culture.

Ketchum, B. H., Ryther, J. H., Yentsoh, C. S. and C o d , N. (1958). Rapp. Proc. Verb. Cons. Pemn. Int. Explor. Mer. 144, 132-140. Productivity in relation to nutrients.

Kielhorn, W. V. (1952). J . Fbh. Res. Bd. Canada 9, 223-264. The biology of the surface zone zooplankton of a Boreo-Arctic Atlantic Ocean area.

Kimball, J. F., Corcoran, E. F. and Wood, E. J. F. (1963). Bull. Mar. Sci. QzLlf Caribb. 13, 574-577. Chlorophyll-containing micro-organisms in the aphotic zone of the oceans.

King, J. E. and Hida, T. S. (1957). U.S. F b h & WildlifeService, Fish. Bull. 118, 57, 365-395. Zooplankton abundance in the central Pacific, Pt. 11.

Koyama, T. (1962). J . Oceanogr. SOC. Japan, 20th Anniv. Vol. 563-576. Organic compounds in sea water.

Kreps, E. and Verjbinskaya, N. (1930). J . Consed int. Explor. Mer. 5 , 327-340. Seasonal changes in the phosphate and nitrate content and in hydrogen ion concentration in the Barents Sea.

Kreps, E. and Verjbinskaya, N. (1932). J . Conaeil int. Explor. Mer. 7 , 25-46. The consumption of nutrient salts in the Barents Sea.

Krey, J. (1961). J . Conseil int. Explor. Mer. 26, 263-280. Der Detritus in Meere. Krey, J. (1964). Kieler Meeresforsch. 20, 18-29. Die mittlere Tiefenverteilung von

Kriss, A. E. (1963). “Marine Microbiology”, 536 pp. Edinburgh: Oliver and Boyd. Krogh, A. (1934). Ecol. Monogr. 4, 430-439. Life at great depths in the ocean. Lanskaya, L. A. (1963). I n “Marine Microbiology” (C. H. Oppenheimer, ed.),

Ch. 13, 127-132. Fission rate of plankton algae of the Black Sea in cultures. Springfield, Ill. : Thomas.

Leavitt, B. B. (1935). Bwl. Bull. Woode Hole. 68, 115-130. A quantitative study of the vertical distribution of the larger zooplankton in deep water.

Leavitt, B. B. (1938). Biol. Bull. Woods Hole. 14, 376-394. The quantitative vertical distribution of macrozooplankton in the Atlantic Ocean Basin.

Lewin, J. C. (1963). I n “Marine Microbiology” (C. H. Oppenheimer, ed.), Ch. 23, 229-235. Heterotrophy in marine diatoms. Springfield, Ill.: Thomas.

Lewin, J. C. and Lewin, R. A. (1960). Can. J . Microbwl. 6 , 127-134. Auxotrophy and heterotrophy in marine littoral diatoms.

Lillick, L. C. (1940). Trans. Amer. Phil. SOC. 31, 193-237. Phytoplankton and planktonic Protozoa of the offshore waters of the Gulf of Maine. Part 11.

Lohmann, H. (1908). Wha. Meeresunters. Kiel Helgo. Abt. Kiel N .P . 10, 129-370. Untersuchungen zur Feststellung des vollstandiger Gehaltes des Meeres an Plankton.

Lohmann, H. (1911). Int. Rev. 9 ~ . Hydrobiol. & Hydrogr. 4, 1-38. ttber des Nannoplankton und die Zentrifugierung.

Loosanoff, V. L. and Davis, H. C. (1963). Advancee Mar. Biol. 1, 1-136. Rearing of bivalve molluscs.

Lucas, C. E. (1947). Bwl. Rev. 22, 270-295. Ecological effects of external metabolites.

Lucas, C. E. (1955). Pap. Mar. Biol. & Oceanogr. Suppl. Deep Sea Ree. 3, 139- 148. External metabolites in the sea.

Lucas, C. E. (1961). Ira “Oceanography” Public. No. 67, A.A.A.S. Washington,

Seston, Mikrobiomasse und Detritus im nordlichen Nordatlantik.

THE PRODUCTION O F MARINE; PLANXTON 199 D.C. (M. Sears, ed.), 499-517. Interrelationships between aquatic organisma mediated by external metabolites.

McAllister, C. D., Parsons, T. R., Stephens, K. and Strickland, J. D. H. (1961). Limnol. & Ocearwgr. 6, 237-258. Measurements of primary production in coastal sea water using a large volume plastic sphere.

Macdonald, R. (1927). J. Mar. Biol. Ass. U . K . 14, 753-784. Food and habits of Meganycdiphanea norvegica.

Mackintosh, N . A. (1934). D.iscovery Repts. 9, 67-158. Distribution of the macroplankton in the Atlantic section of the Antarctic.

Mackintosh, N. A. (1937). Discovery Repts. 16, 367412. Seasonal circulation of the Antarctic macroplankton.

Maddux, W. S. and Jones, R. F. (1964). Limnol. & Oceanogr. 9,79-86. Some interactions of temperature, light intensity, and nutrient concentration during the continuous culture of Nitzschia closterium and Telraaelmis sp.

Marak, R. R. (1960). J . Conaeil int. Explor. Mer. 25,147-157. Food habits of larval cod, haddock, and coalfish in the Gulf of Main13 and Georges Bank area.

Mare, M. F. (1940). J. Mar. Bwl. Ass. U.K. 24,461-482. Plankton production off Plymouth and the mouth of the English Channel in 1939.

Margalef, R. (1958). I n “Perspectives in Marine Biology” (Buzzati-Traverso, ed.), 323-347. Temporal succession and spatial heterogeneity in phytoplankton. Berkeley: University of California Press.

Marshall, P. T. (1958). J. Conseil int. Explor. Mer. 23, 173-177. Primary production in the Arctic.

Marshall, 8. M. (1949). J . Mar. Bwl. Ass. U.K. 28, 45-122. On the biology of the small copepods in Loch Striven.

Marshall, S. M. and Orr, A. P. (1928). J. Mar. Bio!. Ass. U.K. 15, 321-360. “he photosynthesis of diatom cultures in the sea.

Marshall, S. M. and Orr, A. P. (1930). J. Mar. Biol. Ass. U.K. 16, 853-878. A study of the spring diatom increase in Loch Striven.

Marshall, S. M. and Orr, A. P. (1948). J . Mar. 3 i o l . Ass. U.K. 27, 360-379. Further experiments on the fertilization of a soa loch (Loch Craiglin).

Marshall, S. M. and Om, A. P. (1955). “The Biology of a Marine Copepod, CaZunua finmarchicus (Gunnerus)”, 188 pp. Edinburgh and London: Oliver and Boyd.

Marshall, S. M. and Orr, A. P. (1955). Pap. Mar. Bwl. (e: Oceanogr. Suppl. Deep Sea Rea. 3, 110-114. Experimental feeding of the copepod CaZunus fZn- marchktw (Gunner) on phytoplankton cultures labelled with radioactive carbon (W).

Marshall, S. M. and Om, A. P. (1956). J. Mar. Biol. .4ss. U.K. 35,587-603. On the biology of Calanus finmarchicwr. IX. Feeding and digestion in the young stages.

Marshall, S. M. and Orr, A. P. (1964). I n “Grazing in Terrestrial and Marine Environments” (D. J. Crisp, ed.), 227-238. Grazing by copepods in the sea. Oxford: Blackwell Scientific Publications.

Mauchline, J. (1959). Proc. Roy. SOC. Edin. 67(B), 141-179. The biology of the euphausiid crustacean, Megan,y&ip?tunes m e g i c a (M. Sara).

Menzel, D. W., Hulburt, E. M. and Ryther, J. H. (1.962). Deep Sea Res. 10, 209- 219. The effects of enriching Sargasso Sea water on the production and species composition of the phytoplankton.

Menzel, D. W. and Ryther, J. H. (1960). Deep Sea Rea. 6, 351-367. The annual cycle of primary production in the Sargasso Sea off Bermuda.

Menzel, D. W. and Ryther, J. H. (1961). DeepSm Rea. 7,282-288. Annual variations in primary production of the Saxgasso Serb off Bermuda.


Menzel, D. W. and Ryther, J. H. (1961). J. Conseil int. EzpZor. Mer. 26, 250-268. Zooplankton in the Sargasso Sea off Bermuda and its relation to organic production.

Menzel, D. W. and Ryther, J. H. (1964). Limnol. & Oceanogr. 9, 179-186. “he composition of particulate organic matter in the western north Atlantic.

Menzel, D. W. and Spaeth, J. P. (1962). Limnol. & Oceanogr. 7 , 151-154. Occur- rence of vitamin BIB in the Sargasso Sea.

Moore, H. B. (1949). Bull. Bingham. Oceanogr. Coll. 12(2), 1-97. The zooplankton of the upper waters of the Bermuda area of the northern Atlantic.

Moyse, J. (1963). J. Conseil int. Explor. Mer. 28, 175-187. A comparison of the value of various flagellates and diatoms as food for barnacle larvae.

Mullin, M. M. (1963). Limnol. & Oceanogr. 8, 239-250. Some factors affecting the feeding of marine copepods of the genus Calanus.

Murray, J. W. (1963). J. Mar. Biol. Ass. U .K . 43, 621442. Ecological experiments on Foraminiferida.

Park, K., Williams, W. T., Prescott, J. M. and Hood, TI. W. (1962). Science, 198, 531-532. Amino-acids in deep-sea water.

Parsons, T. R. and Strickland, J. D. H. (1962). Deep Sea Res. 8,211-222. On the production of particulate organic carbon by heterotrophic processes in sea water.

Petipa, T. S. (1959). Trudy Sevastopol. Biol. stants. SSSR 12, 130-152. Nutrition of Acartia clausi Giesbr. and A . latisetosu Kritcs. in the Black Sea (Net. Lib. Sci. Tech. R.T.S.).

Pintner, I. J. and Provasoli, L. (1963). I n “Marine Microbiology” (C. H. Oppen- heimer, ed.), Ch. 11, 116121. Nutritional characteristics of some Chryso- monads. Springfield, Ill.: Thomas.

Pomeroy, L. R., Mathews, H. M. and Min, H. S. (1963). Limnol. & Oceanogr. 8, 50-55. Excretion of phosphate and soluble organic phosphorus compounds by zooplankton.

Proctor, V. W. (1957). Limnol. & Oceanogr. 2, 125-139. Studies of algal anti- biosis using Haematococcus and Chlamydomonas.

Provasoli, L. (1958). I n “Perspectives in Marine Biology” (Buzzati-Traverso, ed.), 385-403. Growth factors in unicellular marine algae. Berkeley: University of California Press.

Provasoli, L. (1963). I n “The Sea” Vol. 2 (M. N. Hill, ed.), Ch. 8, 165-219. Organic regulation of phytoplankton fertility. New York: Interscience Publishers.

Provasoli, L. and McLaughlin, J. J. A. (1963). In “Marine Microbiology” (C. H. Oppenheimer, ed.), Ch. 10, 105-113. Limited heterotrophy of some photosynthetic dinoflagellates. Springfield, Ill. Thomas.

Provasoli, L., McLaughlin, J. J. A. and Droop, M. R. (1957). Arch. fur Mikro- biol. 25, 392-428. The development of artificial media for marine algae.

Putter, A. (1909). “Die Ernahrung der Wassertiere und der Stoffhaushalt der Gewasser”, 168 pp. Jena: J. Fischer.

Putter, A. (1925). Archiv. fur Hydrobwl. 15, 70-117. Die Erniihrung der Cope- poden.

Raymont, J. E. G. (1959). Gmnol. & Oceanogr. 4,479-491. The respiration ofsome planktonic copepods. 111. The oxygen requirements of some American species.

Raymont, J. E. G. (1963). “Plankton and Productivity in the Oceans”, 660 pp., Oxford: Pergamon Press.

Raymont, J. E. G. and Adams, M. N. E. (1958). Gmnol. & Oceanogr. a, 119-136. Studies on the mass culture of Phaeodactylum.


Raymont, J. E. G. and Miller, R. S. (1962). Int. Rezue ges. Hydrobiol. 47,169-209. Production of marine zooplankton with fertilization in en enclosed body of sea water.

Raymont, J. E. G., Austin, J. and Linford, E. (1964). J. Conaeil int. Explor. Mer. 28, 354-363. Biochemical studies on marine zooplankton I.

Redfield, A. C. (1934). James Johnstone Memorid Vol., 176-192. On the pro- portions of organic derivatives in sea water and their relation to the composition of plankton. University of Liverpool.

Redfield, A. C., Ketchum, B. H. and Richards, F. A. (1963). In “The Sea” Vol. 2 (M. N. Hill, ed.), Ch. 2,26-77. The influence of organisms on the composition of sea water. New York: Interscience Publishers.

Reeve, M. R. (1963). J. Exp. Biol. 40, 195-205. The filter-feeding of Artemia. I. In pure cultures of plant cells.

Reid, J. L. (1962). Limnol. & Oceanogr. 7, 287-306. On circulation, phosphate- phosphorus content and zooplankton volum3s in the upper part of the Pacific Ocean.

Riley, G. A. (1942). J. Mar. Res. 5, 67-87. The relahionship of vertical turbulence and spring diatom flowerings.

Riley, G. A. (1946). J. Mar. Res. 6, 54-73. Factors controlling phytoplankton populations on Georges Bank.

Riley, G. A. (1947). J. Mar. Res. 6, 104-113. A tkeoretical analysis of the zoo- p!ankton population of Georges Bank.

Riley, G. A. (1952). Bull. Bingham Oceanogr. Coll. 13, 40-64. Phytoplankton of Block Island Sound, 1949.

Riley, G. A. (1956). Bull. Bingham Oceanogr. Coll. 115, 324-344. Oceanography of Long Island Sound, 1952-54. IX. Production anfl utilization of organic matter.

Riley, G. A. (1957). Limnol. & Oceanogr. 2, 252-270. Phytoplankton of the north central Sargasso Sea.

Riley, G. A. (1959). Bull. Bingham Oceanogr. Colt!. 17, 9-30. Oceanography of Long Island Sound, 1954-55.

Riley, G. A. (1963a). In “The Sea” Vol. 2 (M. N. Hill, ed.), Ch. 20,438-463. Theory of food-chain relations in the ocean. New York: Interscience Publishers.

Riley, G. A. (1963b). Limnol. & Oceanogr. 8 , 372-381. Organic aggregates in sea water and the dynamics of their formation and utilization.

Riley, G. A. and Bumpus, D. F. (1946). J. Mar. hes. 6, 33-47. Phytoplankton- zooplankton relationships on Georges Bank.

Riley, G. A. and Conover, S. A. M. (1956). Bull. Bingham Oceanogr. Coll. 15, 47-61. Oceanography of Long Island Sound, 1952-54. 111. Chemical Oceanography.

Riley, G. A., Stommel, H. and Bumpus, D. F. (1949). Bull. Bingham Oceanogr. Coll. 12, 1-169. Quantitative ecology of the p:ankton of the western north Atlantic.

Russell, F. S. and Colman, J. S. (1934). Qt. Barrier Reef. Expdn. Scientific Repts. B.M.(N.H.) 2, 159-176. The zooplankton. 11.

Ryland, J. S. (1964). J . Mar. Biol. A88. U . K . 44, 343-364. The feeding of plaice and sand-eel larvae in the southern North Sea.

Ryther, J. H. (1954j. Bwl. Bull. Woods Hole 106, 198-209. Ecology of phytoplankton blooms in Moriches Bay and Great South Bey, Long Island, N.Y.

Ryther, J. H. (1956). Limnol. & Oceanogr. 1, 61-70. Phot~syntheais in the ocean aa e function of light intensity.

Ryther, J. H. (1963). I n “The Sea” Vol. 2 (M. N. Hill, ed.), Ch. 17, 347-380. Geo- graphic variations in productivity. New York: Interscience Publishers.


Ryther, J. H. and Menzel, D. W. (1959). Limnol. & Ocecznogr. 4, 492-649. Light adaptation by marine phytoplankton.

Ryther, J. H. and Yentsch, C. S. (1957). Limnol. & Oceanogr. 2, 281-286. Esti- mation of phytoplankton production in the ocean from chlorophyll and light data.

Ryther, J. H. and Yentsch, C. S. (1958). Limnol. & Oceanogr. 3, 327-335. Primary production of continental shelf waters off New York.

Saijo, Y. and Ichimura, S. (1962). J . Oceanogr. Soc. Japan, 20th Ann. Vol. 687- 693. Some considerations on photosynthesis of phytoplankton from the point of view of productivity measurement.

Sewell, R. B. (1948). B . M . (Nat. Hiat.) John Murray Expdn. 1933-34 Sci. Repta. 8(3), 321-692. The free swimming planktonic Copepoda - Geographical distribution.

Shelbourne, J. E. (1953). J . Mar. Bwl. Ass. U.K. 32, 149-159. The feeding habits of plaice post-larvae in the Southern Bight.

Shelbourne, J. E. (1957). J . Mar. Biol. Ass. U .K . 36, 539-552. The feeding and condition of plaice larvae in good and bad plankton patches.

Shelbourne, J. E. (1962). J . Mar. Biol. Ass. U.K. 42, 243-252. A predator-prey size relationship for plaice larvae feeding on Oikopleura.

Shirakhi, K. and Provasoli, L. (1959). Int. Oceanogr. Congress Preprints A.A.A.S. Washington, 951-952. Growth factors as supplements to inadequate algal food for Tigriopua japonicua.

Smayda, T . J. (1963). I n “Marine Microbiology” (C . H. Oppenheimer, ed.), Ch. 27,260-274. Succession of phytoplankton and the ocean as an holoooenotic environment. Springfield, 111. : Thomas.

Smith, J. B., Tatsumoto, M. and Hood, D. W. (1960). M n o l . & Oceanogr. 5, 425-431. Carbamino carboxylic acids in photosynthesis.

Sorokin, J. I. (1964a). J . Conaeil int. Explor. Mer. 29, 41-60. On the primasy production and bacterial activities in the Black Sea.

Sorokin, J. I. (1964b). J . Conaeil int. Explor. Mer. 29,25-40. A quantitative study of the microflora in the central Pacific Ocean.

Steele, J. H. (1956). J . Mar. Biol. Ass. U .K . 35, 1-33. Plant production on the Fladen Ground.

Steele, J. H. (1958). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 144, 79-84. Production studies in the northern North Sea.

Steele, J. H. (1962). Limnol. & Oceanogr. 7 , 137-150. Environmental control of photosynthesis in the sea.

Steele, J. H. and Baird, I. E. (1961). Limnol. & Oceanogr. 6, 68-78. Relations between primary production, chlorophyll and particulate carbon.

Steele, J. H. and Baird, I. E. (1962). Limnol. & Oceanogr. 7 , 42-47. Further relations between primary production, chlorophyll and particulate carbon.

Steele, J. H. and Menzel, D. W. (1962). Deep Sea Rea. 9, 39-49. Conditions for maximum primary production in the mixed layer.

Steem- Nielsen, E. (1935).’ Medd. K m m . Danmrka Fbk-Havund. Ser. Phnkton, 3 Nr. 1, 1-93. The production of phytoplankton at the Faroe Isles, Iceland, E. Greenland and in the waters around.

Steemann Nielsen, E. (1937). J. Conaeil int. Explor. Mer. 12, 147-153. On the relation between the quantities of phytoplankton and zooplankton in the sea.

Steemann Nielsen, E. (1940). M&. Komm. Danmrka Fhk-Havund. Ser. Plankton, 3 Nr. 4, 1-56. Die Produktionsbedingungen des Phytoplanktons im tfber- gengsgebiet zwischen der N o d und Ost-see.

SteemannNielsen, E. (1961). Medd. K m . Danmarka F‘isk-Haw&. Ser. P b n h ,


5 Nr. 4, 1-114. The marine vegetation of the lsefjord - A study of ecology and production.

Steemann Nielsen, E. (1954). J. Conseil int. Explor. Mer. 19,309-328. On organic production in the oceans.

Steemann Nielsen, E. (1958a). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 144, 92-95. A survey of recent Danish meammments of the organic productivity in the sea.

Steemann Nielsen, E. (1958b). J. Conseil int. Explor. Mer. 23,178-188. The balance between phytoplankton and zooplankton in the sea.

Steemann Nielsen, E. (1960). Physiol. Plant. 13, 348-357. Dark fixation of CO, and measurements of organic productivity with remarks on chemo-synthesis.

Steemann Nielsen, E. (1962a). Physiol. Plant. 15, 161-171. Inactivation of the photochemical mechanism in photosynthesis 8 3 a meana to protect the cells against too high light intensities.

Steemann Nielsen, E. (1962b). Rapp. Proc. Verb. Cfons. Perm. Int. Explor. Her. 153, 178-181. The relationship betwoen phytoplankton and zooplankton in the sea.

Steemann Nielsen, E. (1963). In “The Sea” Vol. 2 (M. N. Hill, ed.), Ch. 7, 129-164. Productivity definition and measurement. New ‘York: Interscience Publishers.

Steemann Nielsen, E. (1964a). J. EwZ. 52 (Suppl.), 119-130. Recent advances in measuring and understanding marine primary production.

Steemann Nielsen, E. (1964b). Medd. Danmarks. Fisk-Ham&. N.S. 4, 31-77. Investigations of the rate of primary production a t two Danish light-ships in the transition area between the North Sea and the Baltic.

Steemann Nielsen, E. and Aabye Jenuen, E. (1957). Galatheu Rept. 1, 49-136. Primary oceanic production. The autotrophic production of organic matter in the oceans.

Steemann Nielsen, E. and Hamen, V. K. (1959). PhysiOZ. Plant. 12, 353-370. Light adaptation in marine phytoplankton populations and its interrelation with temperature.

Steemann Nielsen, E. and Park, T. S. (1964). J. 9oneeiZ int. Explor. Mer. 29, 19-24. On the time course in adapting to low light intensities in marine phytoplankton.

Sverdrup, H. V. (1953). J. Conseil int. Explor. Me,.. 18, 287-295. On conditions for the vernal blooming of phytoplankton.

Sverdrup, H. V. and Allen, W. E. (1939). J. Mar. RIM. 2, 131-144. Distribution of diatoms in relation to the character of water mawes and currents off southern California.

Telling, J. F. (1960). LimnoZ. & Ocemnogr. 5, 62-77. Comparative laboratory and field studies of photosynthesis by a marine planktonic diatom.

Tatsumoto, M., Williams, W. T., Prescott, J. M. and Hood, D. W. (1961). J. Mar. Res. 19, 89-95. Aminoacids in samples of surface sea water.

Teixeira, C. (1963). Bol. Inst. Oceanogr. Univerdzde de Sao Paul0 13, 53-60. Relative rates of photosynthesis and standing stock of the net phytoplankton and nannoplankton.

Teixeira, C. and Kutner, M. B. (1963). Bol. Inst. Gcemwgr. Univerdade de Sao Paul0 12, 101-124. Plankton studies & a man,grove environment. I.

Tranter, D. J. (1962). Auat. J. Mar. Freshw. Reo. 13, 106-142. Zooplankton abundance in Australian waters.

!t’ranter, D. J. and Newell, B. S. (1963). Deep Sea RM. 10, 1-9. Hnrichment experiments in the Indian Ocean.


Vaccaro, R. F. (1963). J. Mar. Res. 21, 284-301. Available nitrogen and phosphorus and the biochemical cycle in the Atlantic off New England.

Vinogradov, M. E. (1962a). Deep Sea Rea. 8,251-258. Quantitative distribution of deep-sea plankton in the western Pacific and its relation to deep-water circulation.

Vinogradov, M. E. (1962b). Rapp. Proc. Verb. Cons. Perm. Int. Explor. Mer. 153, 116119. Feeding of deep-sea zooplankton.

Vishniac, H. S. and Riley, G. A. (1961). Linznol. & Oceanogr. 6,36-41. Cobalamin and thiamine in Long Island Sound; patterns of distribution and ecological significance.

Walne, P. R. (1963). J. Mar. Biol. Ass. U.K. 43, 767-784. Observations on the food value of seven species of algae to the larvae of Ostrea edulia. 1. Feeding experiments.

Wangersky, P. J. (1952). Science 115, 685. Isolation of ascorbic acid and rhamno- sides from sea water.

Wiborg, K. F. (1948a). Rep. Norweg. Fish & Mar. Inveat. 9(3), 1-27. Investige- tions on cod larvae in coastal waters of northern Norway.

Wiborg, K. F. (194813). Rep. Norweg. Fish & Mar. Invest. 9(4), 1-17. Some observations of the food of cod (Gadus callarias L.) of the 0-11-group from deep water and the littoral zone in northern Norway and f o m deep water at Spitzbergen.

Wiborg, K. F. (1949). Rep. Norweg. Fish & Mar. Invest. 9(8), 1-27. Food of cod of 0-11 group from deep water in some fjords of northern Norway.

Wiborg, K. F. (1954). Rep. Norweg. Fish & Mar. Invest. 11(1), 1-246. Investi- gations on zooplankton in coastal and offshore waters of western and north- western Norway.

Wickstead, J. H. (1958). J. Conseil int. Explor. Mer. 23, 341-353. A survey of the larger zooplankton of Singapore Straits.

Wickstead, J. H. (1963). Proc. 2001. SOC. London 141, 577-608. Estimates of total zooplankton in the Zanzibar area of the Indian Ocean with a comparimn of the resultg with two different nets.

Wimpenny, R. S. (1936). Fiah. Invest. areat Britain Ser. 11, 15(3), 1-53. The distribution, breeding and feeding of some important plankton organisms of the south-west North Sea in 1934, Pt. I.

Wimpenny, R. S. (1938). J. Conseil int. Explor. Mer. 13, 323-336. Diurnal variation in the feeding and breeding of zooplankton related to the numerical balances of the zoo- phyto-plankton community.

Wimpenny, R. S. (1958). Rapp. Proc. Verb. Cons. Perm. Int. Explm. Mer. 144, 70-72. Carbon production in the sea at the Smith’s Knoll light-vessel.

Wood, E. J. F. (1963a). In “Marine Microbiology” (C. H. Oppenheimer, ed.), Ch. 3, 28-39. Ecology of algae, protozoa, fungi and viruses. Springfield, €ll.: Thomas.

Wood, E. J. F. (1963b). I n “Marine Microbiology” (C. H. Oppenheimer, ed.), Ch. 28, 275-286. Some relationships of phytoplankton to environment. Spri@eld, Ill.: Thomas.

Wood, E. J. F. (1963~). Oceanogr. Mar. Biol. Ann. Rev. 1, 197-222. Heterotro- phic micro-organisms in the oceans.

Yentsch, C. S. and Ryther, J. H. (1959). J. Conseil int. Explor. Mer. 24, 231-238. Relative signScance of the net phytoplankton and nanoplankton in the waters of Vineyard Sound.

Yentsch, C. S. and Vaccaro, R. F. (1958). Limnol. & Oceanogr. 3, 443-448. Phytoplankton nitrogen in the oceans.

THE PRODUCTION O F MARINE: PLANKTON 205

Zenkevitch, L. (1963). “Biology of the Seas of the U.S.S.R.”, 955 pp. London:

Zenkevitch, L. A. and Birstein, J. A. (1956). DeepSea Reg. 4,5P64. Studies of the

Zobell, C. E. (1946). “Marine Microbiology”, 240 rip. Waltham, Mass.: Chronica

Allen & Unwin.

deep-water fauna and related problems.

Botanica Co.

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