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FACTORS OF PHYTOPLANKTON PRODUCTION: II

The relation of plants to the physical-chemical and biological properties has been touched upon in the foregoing discussion outlining the factors that control phytoplankton production. It remains to enlarge upon and examine more closely how some of these factors operate in nature. This examination will be organized in reference to (a) photosynthesis of phytoplankton, (b) plant nutrients and vertical circulation of water, (c) horizontal ocean currents, and (d) temperature.

Photosynthesis of Phytoplankton

The intensity of light decreases gradually with depth; yet for the purpose of biological investigations it is convenient to consider the sea as divided vertically into three zones with respect to the amount of light that is present. The depths given are approximations and vary with latitude and season.

1. The euphotic zone, which is abundantly supplied with light sufficient for the photosynthetic processes of plants. This zone extends from the surface to 80 or more meters. All of the eulittoral zone lies within this layer.

2. The disphotic zone, which is only dimly lighted and extends from about 80 to 200 or more meters. No effective plant production can take place in this zone, and the plants found here have mostly sunk from the layer above.

3. The aphotic zone, the lightless region below the disphotic zone. In the deep sea it is a very thick layer in which no plants are produced and the animal life consists only of carnivores and detritus feeders.

Until the relationship between rate of photosynthesis and light intensity at different wave lengths is more thoroughly understood than at present, it will be necessary to restrict discussion to the relationship between rate of photosynthesis and total light intensity in the sea as expressed in energy units or in units of illumination.

When using energy units the light intensity is expressed in ergs per unit surface and unit time, for example, ergs/cm²/sec; or in gram calories or joules per unit surface and unit time (1 g cal = 4.18 × 10⁷ ergs, 1 joule = 10⁷ ergs). The penetration of radiant energy in the sea was discussed in chapter IV (p. 104). It was stated there that no direct measurements are available of the energy which under different conditions reaches different depths below the surface, but that these amounts could be computed from observations of the extinction coefficients for radiation of different wave lengths and from the intensity of the radiation of stated wave lengths reaching the sea surface (table 27, figs. 21, 22). In all experiments in which the intensity of light has been examined in conjunction with studies of photosynthesis, the energy at different levels has

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been computed on such a basis. The light which penetrates to any considerable depth in the sea falls within a narrow band of the spectrum between approximate wave lengths of 0.45 μ and 0.60 μ, corresponding to light in the blue-to-yellow range. In marine plants, photosynthesis takes place within this part of the spectrum, for which reason the photosynthesis can be expected to stand in a fairly definite relation to the total energy.

In a number of published reports on photosynthesis in the sea, light intensity is expressed in units of illumination, that is, in units based on the power of light to produce visual sensation. Illumination units such as 1 meter-candle = 1 lux = 0.093 foot-candle have been widely used, and it is therefore necessary to explain their relation to the energy units. Because the unit of illumination is directly based on the reaction of the human eye, a mechanical equivalent of the illumination unit can be established only at a specified wave length. At moderate illumination the maximum sensitivity of the human eye lies at a wave length of 0.56 μ, and at this wave length the “luminous equivalent” has been established (Smithsonian Tables, 1933) at

There exists no simple relation, however, between the total energy of radiation of different wave lengths and the corresponding illumination in luxes, the reason being that the human eye is not at all sensitive to infrared radiation and is only slightly sensitive to radiation in the violet part of the spectrum. More than half of the radiation from sun and sky which reaches the sea surface falls in the infrared, and the eye is not very sensitive to a great portion of the remaining half, so that the luminous equivalent as defined above has to be multiplied by a factor of about 0.15 in order to give the illumination in luxes corresponding to a given intensity of the radiation in energy units. In the sea the infrared part of the radiation is absorbed in the upper few centimeters and, owing to the selective absorption in the visible part of the spectrum, the energy which penetrates to greater depths becomes more and more concentrated at wave lengths to which the human eye has its greatest sensitivity. Consequently, the factor by which the luminous equivalent must be multiplied in order to give the illumination in luxes increases with depth, reaching a value of approximately 0.75 at depths where the incident energy is reduced to 1 g cal/cm²/hour or less.

It is not possible to give any table by means of which the energy reaching a certain depth can be converted into units of illumination, because the conversion factors will depend upon the quality of the light. Thus, in turbid coastal water and in the clearest oceanic water the same amount of energy is found at the depths of 10 and 100 m, respectively (table 27), but at 10 m in the coastal water the maximum intensity lies

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at a wave length of 0.55 μ, whereas at 100 m in the oceanic water the maximum intensity is at a wave length of 0.48 μ. At these intensities the maximum sensitivity of the human eye will be at about 0.55 μ, and the illumination at 10 m in the coastal water would therefore be greater than at 100 m in the clear oceanic water, in spite of the energies being equal.

Table 92 has been prepared in order to show approximately corresponding values of energy and illumination at different depths and in different types of water. For the sake of simplicity the intensity of the radiation penetrating the surface has been selected at 100 g cal/cm²/hour, corresponding approximately to the radiation from sun and sky with the sun at zenith. The illumination at the surface is then about 120,000 luxes. The illumination decreases more slowly with depth than does the energy, but it is realized that the values in the table do not correspond exactly to each other. They give only the approximate relationship and can serve in obtaining a rough estimate of the energy if the illumination is stated, or vice versa.

The effect of light (somewhat modified by the effect of temperature) on photosynthesis can be illustrated by an experiment in which a series of suitable clear glass bottles are filled with sea water containing a substantial phytoplankton population and are submerged in the day time at various depths in the euphotic zone. It will be found that at a few meters below the surface the oxygen content of the water will increase as a result of the photosynthetic activities of the plants within the bottles.

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With increasing depth and accompanying diminution of light intensity, the amount of oxygen produced becomes gradually less until a depth is reached where the respiration of the plants exactly balances the oxygen produced through photosynthesis, so that no free oxygen is given off to the water. The amount of oxygen used by the plants in respiration during the experimental period is determined by a similar accompanying series of plankton samples in bottles covered by dark cloth to exclude any light for photosynthesis. The amount of oxygen consumed from the water in these bottles gives a measure of the respiration at the respective depths. Adding this figure to the amount of oxygen produced in the exposed bottles gives the total amount of oxygen produced in photosynthesis.

When the temperature decreases with increasing depth, the rate of respiration decreases. As long as the light intensity is so high that it does not limit the rate of photosynthesis, this rate also falls somewhat with falling temperature, but at low light intensities the effect of temperature

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on photosynthesis is negligible. A typical assimilation experiment is given in table 93. In this experiment samples of mixed plankton from the surface layer were lowered to different depths in covered or exposed bottles. The oxygen consumption in the covered bottles was therefore due to the total respiration of the plants and the animals and bacteria included in the sample. No oxygen was produced in the exposed bottles at depths greater than about 27 m, and the total production of oxygen disappeared at a depth of about 44 m. If the bottles had contained pure cultures of plants, production of oxygen in the exposed bottles would have taken place to a depth somewhere between these two limits (p. 933).

The photosynthesis depends on the light intensity, and the light intensity at which oxygen production and oxygen utilization are equal is therefore called the compensation point, or the compensation light intensity. The illumination at this point is “the minimum intensity at which the plant could survive in nature and [is] still too low for any crop increase” (Jenkin, 1937). The more pronounced effect of lowered temperature on the rate of respiration as compared with the effect on the rate of photosynthesis leads to a slight lowering of the compensation point with decreasing temperature, at least in certain higher algae (Spoehr, 1926).

It is obvious that the compensation point is determined by physiological characteristics of the plants and may, therefore, be somewhat different for different species, just as the optimum light intensity is not the same for all species. The compensation point is independent of the time during which photosynthesis and respiration have been measured if the oxygen production per unit time remains proportional to the light intensity and the oxygen consumption per unit time remains constant. On these assumptions, the oxygen production dP in the short time interval dt equals aIdt, where a is a constant and I is the light intensity, and the oxygen consumption dR equals bdt where b is another constant. The compensation point, I_c, is defined by

The values of oxygen production P and consumption R in the time T are The average light intensity in the time T is Therefore, if P = R, it follows that

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that is, the compensation point equals the average light intensity during a period of time in which oxygen production and consumption balance. The conclusion is correct on the assumptions which were made, but measurements in the field will not lead to exact results unless the light intensity remains low during the experiment, because only then is the production of oxygen proportional to the light intensity.

The two factors a and b which have been introduced here are in general not determined, but measurements of the difference between production and consumption are made at different light intensities and the compensation point is found by interpolation. Since the compensation point depends upon the ratio b/a, it follows that it depends on temperature if photosynthesis and respiration are influenced differently by the temperature.

The depth at which the compensation point is found is called the compensation depth. This depth evidently varies with the season of the year, the time of day, the cloudiness, and the character of the water. In the experiment quoted in table 93, the compensation depth lies between 27 m and 44 m. For a given locality one can introduce such terms as daily compensation depth with a clear sky, daily compensation depth with an overcast sky, average annual compensation depth, and so on. With a clear sky the compensation depth will in a given locality reach its maximum value at noon and will rise to the surface shortly before sunset. The average daily compensation depth is less than the compensation depth at noon, except at the North Pole.

The diatoms and many other algae thrive best in somewhat subdued light, but the optimum light intensity is not the same for all species. For example, Schreiber (1927) found the optimum for the diatom Biddulphia mobiliensis to be 1600 luxes, and for the green flagellate Carteria sp. over 3200 luxes. Some diatoms are able to grow in much reduced light. This has been shown in nature by Vanhoeffen for arctic species found growing under the ice in March. From Schreiber's results with Biddulphia we learn that high illumination does not necessarily increase the rate of photosynthesis, since the rate of multiplication was proportional to light intensity only at the intermediate illuminations 200 to 400 luxes. That this is quite generally true is indicated by the habit exhibited by many diatoms of grouping the otherwise scattered chromatophores into knots when exposed to strong light. In this way they afford mutual protection during such periods of unusual exposure as might occur when being swept by ascending currents to the very surface on bright days. This condition whereby the chromatophores are concentrated or collected into a group is known as a systrophe, and was described by Schimper (Karsten, 1905). For the diatom Coscinodiscus excentricus this has been found to occur at a light intensity of about 9.6 g cal/cm²/hour, p. 781. That diatom photosynthesis falls off

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in bright light at the surface is shown by field-assimilation experiments of Marshall and Orr (1928) with “persistent diatom cultures.” A “persistent” culture is one consisting of only a single species of diatom, but may contain also bacteria and a few other small organisms such as flagellates (Allen and Nelson, 1910). These investigators concluded that the compensation depth in inshore waters in the latitude of Loch Streven, Scotland, in summer is at 20 to 30 m and in winter at some level close to the surface. Gran (1927) also found that the optimum light conditions for diatoms in northern waters are not at the surface but at a depth of 5 m. Gaarder and Gran (1927) determined that the balance point between photosynthesis and respiration in “raw plankton” samples (mixed culture of composite plankton collection which may contain some animals) occur at a depth of 10 m in Oslo Fjord during March. These authors show that auto-oxidation and bacterial oxidation are important factors to be considered in studies of phytoplankton respiration. Other field observations with raw plankton indicate that a balance of photosynthesis and respiration occurs at a depth of about 17 m in Passamaquoddy Bay during midsummer (Gran and Braarud, 1935), and in certain Puget Sound bays during the summer the compensation depth for raw plankton lies between 10 and 18 m (Gran and Thompson, 1930). The shallowness of the compensation depth in Puget Sound perhaps resulted partly from absorption by the rich diatom plankton which prevailed. The most rapid photosynthesis, as indicated by oxygen production, in this experiment was at a depth of 1 m. The great number of diatoms produced in the upper few meters thus formed a screen preventing normal penetration of light to the population at greater depths.

Assimilation experiments with raw plankton samples can be carried on only if the diatom population is sufficiently dense that the metabolic activities provide differences in oxygen content and pH values above the limits of experimental error of the method. Experiments with persistent cultures have the advantage that they make possible field-assimilation experiments even at seasons when in nature the phytoplankton is at a minimum. The absence of small planktonic animals and the possible control of bacterial populations in such cultures eliminates a source of error in computing oxygen utilization. On the other hand, the diatoms in persistent cultures may represent selective species with slightly different light optima and may therefore not be typical of the mixed population of raw cultures.

The considerable variation found for the depth of compensation of oxygen production and utilization by phytoplankton results from variations in latitude, season, weather, and turbidity, all of which influence the depth of submarine illumination. Theoretically, it should be possible to determine the depth of optimum diatom production for a given area during the growing season by a study of the vertical distribution of

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oxygen, since the maximum oxygen produced in situ represents the depth of optimum light conditions for photosynthesis, provided, other factors essential to growth are uniform in the water mass. During a diatom maximum of five-day duration, the oxygen content may increase by as much as 2.2 ml/L. However, vertical circulation of the water, solution of oxygen from the air, and consumption of oxygen by animal and bacterial respiration makes this a rather uncertain index. The occurrence of the maximum diatom population below the level of maximum oxygen or below the experimentally determined compensation depth indicates that the plants were not produced at that level but have sunk there. For instance, it has been pointed out that the finding of diatom maxima at 40 to 80 m by Schimper (Karsten, 1905) in the Antarctic on the Valdivia could be explained only as being due to sinking, since no effective photosynthesis can occur in these latitudes below 50 m. Actually, such a population must represent a disintegrating one originally produced near the surface. Diatoms do, of course, carry on some photosynthesis at considerably greater depths than the depth of compensation, but more energy is used than is stored and the plants must finally reach a state where they succumb when the stored-up energy is exhausted.

Not only is the quantity of light a factor to be considered, but so also is the quality. It is well known that as sunlight enters the sea the intensity is reduced, but there is moreover a differential absorption, certain light rays being absorbed before others. The red component of light is removed in the first few meters of water, while the blue light penetrates to much greater depths (p. 106). Therefore, diatoms in nature have their greatest growth at depths where the red component is much reduced; rich growths are found at depths (15 to 20 m) where only blue and green light prevail. A realization of this has led to experiments on the effect of light intensities selectively reduced.

In experimental cultures, using Nitzschia closterium, a diatom much used in culture experiments, Stanbury (1931) concluded that the precise wave length is not so important as the amount of energy transmitted.

Assuming that the total energy in all wave lengths within the visible spectrum provides the best measure of available energy for photosynthesis of diatoms, Jenkin (1937), working in the English Channel, computed the available energy in joules or gram calories at various depths and correlated these values with the amount of oxygen produced by Coscinodiscus excentricus in submerged experimental bottles at the various depths tested. The results indicate that with an energy flux less than 7.5 joules, or 1.8 g cal/cm²/hour, the oxygen production is directly proportional to the energy and the utilization of the available energy is about 7 per cent. With an energy flux greater than the above, the photosynthesis is gradually inhibited. Systrophe takes place at an

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energy flux of about 40 joules, or 9.6 g cal/cm²/hour. At the compensation point the figures are 0.55 joule, or 0.13 g cal/cm²/hour. In Gullmar Fjord, Sweden, the compensation light intensity for mixed plankton with some animals included was found to be about 400 luxes (about 0.07 g cal/cm²/hour) (Pettersson et al, 1934). In the clear waters of the English Channel the compensation depth was found to be about 45 m during summer.

In certain sessile shallow-water diatoms adapted to a depth of only a few centimeters the maximum oxygen production occurs at higher energy values, that is, 60 g cal/cm²/hour or 80,000 luxes (Curtis and Juday, 1937).

Diatoms tend to show chromatic adaptation when grown under different components of light, assuming colors that are complementary to those under which they are grown. They thus tend to become yellow-green when grown in red and yellow light, and dark brown in green and blue light. For benthic green algae the red component of light is essential to healthy growth, while brown algae and, especially, red algae characteristic of deep water are adapted to carry on photosynthesis with the red component absent or reduced. We have seen also (p. 295) that, in keeping with this, the order of vertical distribution of the benthic marine algae is greens, browns, and reds, from shallow to deeper water. The quantity of chlorophyll present in these classes of algae is also diminished in the same order (Lubimenko and Tikhouskaia, 1928). The depth at which these benthic algae can grow is also directly correlated with the depth of submarine illumination. In northern latitudes the maximum depth is about 40 to 50 m, whereas in the clear waters of the Mediterranean it is said to be over 100 m. It has been suggested (Klugh, 1930) that certain pigments present in plants growing some distance below the surface may act as photosensitizers to the chlorophyll, enabling it to function with less light intensity.

Plant Nutrients and Vertical Circulation of Water

The inorganic substances required by plants are commonly spoken of as “plant nutrients.” These constitute the raw materials or building blocks out of which the plants, with the aid of sunlight, build up organic compounds entering into their cell structure. The growing plants can obtain these raw materials only from the sea water in which they live. This must therefore be looked upon as a dilute nutrient medium containing all of the elements necessary for plant growth. The concentrations of the nutrient salts are remarkably small; yet a concentration of 1 mg of phosphorus to 10001 of water, for example, is sufficient to produce a vigorous growth of diatoms if other factors are favorable. This is facilitated partly by the very minute size of most phytoplankton organisms and may be illustrated by comparing one plant 1 mm³ in size with a

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thousand plants each 0.001 mm³ in size. Krogh (1934) has calculated that there is a thousandfold advantage for the latter with respect to absorption of nutrients in dilute solution. This advantage results from (1) a tenfold aggregate increase in surface area of the smaller plants and (2) a hundredfold better condition for diffusion of salts to these surfaces. The latter is due to the fact that owing to the microscopic size of the smaller plants the full concentration of nutrients is maintained immediately outside the cell membrane.

The mineralized nutrient elements are not uniformly distributed in the sea, however, and they undergo cycles during which there are periods of delay between the available mineralized state and the unavailable organically bound state of the nutrients. This leads to fluctuations in the intensity of plant production both in space and in time. The production of marine phytoplankton is nature's greatest demonstration of hydroponics, or water culture. The operation of the whole system in detail in the sea is different in many respects, however, from the operation of experimental hydroponic tanks. For example, there is a difference in the population; as we have learned, the floating plants of the sea are not specialized with aerial portions for utilization of CO₂ and elimination of O₂; and roots are not provided for intake of mineral nutrients; neither are there elaborate vascular systems to transport fluids and food. All of the metabolic processes of the marine phytoplankton are carried on within the individual cells which are always submerged beneath the water surface. This universality means that the whole plant must receive light, and the specializations, as already discussed, are along lines designed to maintain the plants in the upper lighted portions of the sea. In the sea the mineral nutrients are not added from without as needed; they have accumulated from the land over eons of time and are stored mainly in the deeper dark-water layers where they are not accessible to autotrophic plants and from whence they must be transported by water movements to replenish the supply periodically exhausted in the productive lighted zone. For discussion of the forces causing this transport see chapter XIII.

It is well known that with return of sunshine and increased temperatures during spring in the temperate and higher latitudes there is a phenomenal outburst of phytoplankton growth in the surface waters. Even the most causal observer is impressed with the brown-green color that is imparted to the waters of coastal areas and over banks during these periods of diatom “bloom.” The production may go on at varying intensities during the summer and frequently becomes augmented again in the autumn. But during the winter months, and sometimes at other seasons as well, there is a dearth of plants and the waters again become deeper blue in color. Similar conspicuous changes in water color occur when one leaves the rich coastal waters and proceeds to the barren open

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sea (fig. 214). It has been said that “blue is the desert color of the sea,” and this is indeed true of vast ocean stretches where phyto- and zooplankton are at a minimum and the water is not otherwise discolored and turbid with inanimate dissolved or suspended material (p. 89). The seasonal and spatial differences in color of coastal waters we know to be due in large measure to the greater or lesser amounts of various types of plankton organisms present in the surface waters, but what is the combination of factors controlling the time and distribution of this fertility? Many details are still unknown, but it is clear that with sufficient sunlight the combination of the nutrient cycles and vertical circulation of the water are dominant causes.

Brandt's theory that phosphates and nitrates may constitute limiting factors in phytoplankton production has found proof in investigations of subsequent workers (Marshall and Orr, 1927, Schreiber, 1927, Gran, 1930, Hentschel and Wattenberg, 1930, and others). At the initiation of vernal phytoplankton production these salts are relatively abundant in the euphotic layer, but as production proceeds the quantity gradually falls off until it can no longer maintain a large population, and the organisms diminish in number or disappear from the water.

Here Nathansohn's theory forms a complement to Brandt's theory in the explanation of irregularities in distribution and periodic fluctuations in phytoplankton production. (See p. 901 for control through organic factors.) Nathansohn (1906) suggested that the nutrient salts must disappear from the lighted surface layers owing to the fact that they are consumed by the plants and that they must therefore accumulate in the deep sea through sinking of living or dead bodies, both plant and animal, constantly settling towards the bottom. The store of nutrients thus accumulated in the deep water through the dissolution of these bodies is, in time, returned to the euphotic layer through diffusion and vertical circulation of the water.

With improvements of methods in chemical analysis it has, indeed, been shown that usually phosphate concentrations do increase with

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depth, indicating a utilization at the surface and a tendency to storage in the deeper water layers. This withdrawal of nutrients from the surface and the resultant accumulation in the deeper layers where they cannot be of direct use to plants owing to the absence of sunlight does not in general represent a permanent loss to the biological cycle. In the terrestrial environment there is constantly a small loss of nutrients as the dissolved salts are carried to the sea in runoff from the land. The sea therefore constantly gains in its resources in proportion to what the land loses. Some nutrients are lost annually from the sea in the formation of stable residues such as humus and through removal of fisheries products, but even these must eventually find their way back to the sea. This runoff from land supplies phosphates, nitrates, and other nutrients to the surface layers of the sea in the coastal regions, but the main replenishment comes from the supply present in the deeper water. Circulation of the water by upwelling, turbulence, diffusion, or convection is the physical agency by which the return is accomplished.

Upwelling. The upwelling of subsurface water in which nutrient salts are brought back to the lighted layers is reflected in large diatom production along the California coast (Moberg, 1928, Sverdrup and Allen, 1939; fig. 215), along the western South American coast through the mechanism of the Peruvian Coastal Current (Gunther, 1936), in regions of divergence along the equatorial countercurrents, and along

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the west coast of Africa (Hentschel, 1928). On the basis of the extensive Meteor investigations, Hentschel demonstrated a relatively much heavier phytoplankton production along the West African coast where marked upwelling is known to take place than along the east coast of South America, except at the southeastern tip where the influence of the Falkland Current is operative. Further, it is shown that the most markedly fertile areas or independent maximal regions along the African coast have tongues of gradually diminishing total plankton density extending outward from the coast corresponding to the main water movements that flow away from the coast, as is indicated by the outward extension of the isotherms (fig. 216).

Not all surface currents show this tendency to unusually rich fertility indicated by the above great coastal populations and the seaward tonguelike extensions. In seeking an explanation we find that the upwelling along the African coast has brought to the surface nutrient-rich water, fertilizing the illuminated euphotic layer. The plants respond with a luxuriant growth, which diminishes in intensity as the nutrients are gradually consumed by the population in the waters as they move to greater and greater distances away from the coast and from the regions of upwelling. Figure 217 shows how closely the distribution of phosphates coincides with the areas shown by direct examination of plankton catches to be fertile in phytoplankton.

The distribution of phosphates as shown in fig. 218, which represents a vertical section from the coast of Africa across the Atlantic to the coast of South America at lat. 9°S, also illustrates how nutrient-rich water is nearer the surface on approaching the African coast. The water with more than 1 μg-atom/L (30 mg/cm³) rises to within about 40 m of the surface, whereas on the South American coast water of nutrient concentration greater than this is not found above about 1000 m. It must be borne in mind that not only phosphates, but also other nutrients needed for plant life that have been regenerated in the deep waters from sinking bodies of organisms produced in the upper layers, are conveyed from the

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enormous unfailing nutrient reservoir of the deep. It has already been pointed out that there is a fairly constant nitrate-phosphate ratio.

Regions of Divergence and Convergence. Regions of divergence are defined as those regions where surface water masses of the ocean flow away from each other or away from the coast so that water from the deep must rise, as a feature of upwelling, to replace them. It appears that such areas, whether at the coast or in the open sea, are productive of phytoplankton; this condition is exemplified in the South Atlantic Congo tongue of cold water which extends far out to sea from the region of the Congo River (Hentschel, 1928). Conversely, regions of convergence are areas where surface waters meet and sink. Such areas are relatively barren of plants, the waters having been impoverished by earlier exhaustion of the nutrients.

The hydrographic features of these two types of water movements are discussed on p. 140, and graphically shown in fig. 198, p. 710, for a Carnegie section across the equatorial currents of the Pacific. Here are two parallel regions of divergence between which lies a region of convergence associated with the Equatorial Countercurrent. When the Carnegie plankton volumes from H. W. Graham's analysis (1941) are compared with the hydrography of this section, we find that the relative volumes of general plankton, which must reflect phytoplankton production, show greater concentrations at stations 157 and 151 which lie within the regions of divergence. This is brought out in fig. 219, where the upper diagram shows the relative plankton volumes (precipitated in special bottles) in centimeters per mile of haul, and the lower diagram shows the vertical water movements and selected isolines for phosphate. For greater detail, see fig. 198.

Turbulence. The effect of renewal of plant nutrients from the deeper water as the result of turbulence and accompanying diffusion is demonstrated especially in such areas as the Bay of Fundy and Puget Sound, where strong tidal currents flowing over uneven bottom and through tortuous passages maintain a relatively homogeneous water

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from the surface to considerable depths. In Puget Sound the surface layers are rich in phosphates, showing an average of about 2.0 μg-atoms/L (62 mg PO₄-P), and the phytoplankton is in general rich from May to October (Thompson and Johnson, 1930, Phifer, 1933). Lower values for phosphates are found in the Bay of Fundy, although the maximum values are relatively high, but the phytoplankton production is restricted for other reasons, as explained below. In the English Channel, where the store of nutrients is relatively low, the turbulence may lead to a depletion of nutrients clear to the bottom during the season of phytoplankton production.

As far as renewal of plant nutrients is concerned, upwelling and turbulence are similar in that they are more or less continuous throughout the year with some variation resulting from periodic changes in the direction or intensity of the winds (cf. p. 725) or from stabilization resulting

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from influx of fresh water or from summer increase in temperature, both of which lead to a stratification of the waters of the euphotic layer.

Where turbulence and upwelling are sufficiently vigorous to involve the euphotic layer, there may always be present a ready supply of nutrients to support at least a moderate plankton production. Under such conditions the cessation of production must result from other factors than depletion of nutrients. During the winter season the controlling factors in some latitudes may be the reduction of light or temperature. The cessation of reproduction during a portion of the year may well represent a period of rest induced by a change in conditions, at least for neritic species.

Stabilization. During recent years there has been a realization that for maximum production a certain degree of vertical stability is required within the euphotic layer. In areas of excessive turbulence this stability is wanting, with the result that, although nutrients and other factors may be optimal, only a moderate production of phytoplankton takes place because the descending currents withdraw a portion of the diatom stock into the deeper water where there is not sufficient light for photosynthesis. Ascending currents may bring some of these back to depths of adequate light. The length of time spent below the euphotic layer would then determine the extent of loss, if any, to total production. The complex problem introduced by turbulence may be stated as mainly one of balancing the beneficial factor against the deleterious factor: ascending currents constantly conveying nutrients from deeper water against descending currents withdrawing a portion of the population to suboptimal lighting conditions. The depth of turbulence and the thickness of the euphotic layer are important in this connection. An example of the beneficial effect is seen when comparing areas in the Gulf of Maine and the Bay of Fundy (Bigelow, 1926, Gran and Braarud, 1935). In the open Gulf, marked stratification due to summer heating leads to the exhaustion of nutrients in the euphotic zone with a subsequent drop in phytoplankton production. Over Georges Bank, however, a fairly rich diatom plankton is maintained during the summer owing to the turbulence of water flowing over the bank.

The deleterious effect is illustrated in parts of the Bay of Fundy where, in June, surface areas rich in nutrients, 0.3 μg-atom/L PO₄-P (10 mg PO₄-P per m³) and up to 4 μg-atoms/L NO₃-N (60 mg NO₃-N per m³) at a depth of 1 m, resulting from turbulence, were nevertheless poor in plankton because of the combination of turbulence and low transparency. Diatoms were fewer than 500 cells per liter in the most affected areas. The largest populations were found in areas of moderate stratification. Two months later some stabilization had occurred with the advance of summer, but the most turbulent areas still showed high nutrients and a small population of about 7000 or fewer diatoms per

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liter, as compared with 551,000 in nearby areas with a well-defined thermocline between 10 and 25 m.

Convection. In regions where there are marked seasonal changes in temperatures between winter and summer, the changes are of great importance not only because of the effect of temperature directly upon the rate of metabolism but also because of its indirect effect in the renewal of nutrients to the surface layers. This method of renewal is characteristic of fresh-water lakes, but is also very important in the sea, especially in the higher latitudes. The phenomenon is, of course, dependent upon the surface waters cooling to a point where their density becomes sufficient to cause them to sink and be replaced by upward movement of lighter and incidentally nutrient-rich waters from below. Similar effects result from pronounced evaporation and must contribute essentially to the maintenance of phytoplankton in the open tropical seas and in isolated seas like the Mediterranean. In areas where vertical circulation results from convection currents, the biological implications are somewhat different than those resulting when nutrient renewal is brought about through the agency of upwelling or turbulence. Except as discussed later, renewal of surface waters by convection is a seasonal rather than a continuous process. The replenishment of elements essential to plants occurs during autumn and winter, with the result that the euphotic layer is richly fertilized in readiness for diatom growth as soon as sufficient sunshine becomes available in spring and as soon as other favorable living conditions are attained. A period of intense growth then ensues, resulting in depletion of nutrients, and since no general renewal can take place until autumn such areas typically experience a marked summer minimum in diatom production following the spring maximum. There is usually a secondary autumnal maximum before the gradually diminishing light reaches a point too low for effective photosynthesis. The regularity of this system may be disturbed by wind-induced turbulence sufficient to cause an upward transport of nutrientladen water from deeper layers, or by fertilization of the surface layers with nutrients brought down from land by rivers. Thus there may be alternating maxima and minima of greater or lesser duration and intensity throughout the whole growing season.

In boreal waters, when the spring production of diatoms has come to a low ebb owing to marked stratification and near exhaustion of nutrients, the role of organic production may be taken over in a diminished degree by the dinoflagellates, especially members of the genus Ceratium. These organisms, owing to their low nutrient requirements and slow rate of growth (daily increase under summer conditions of only 30 to 50 per cent as opposed to 360 per cent in the diatom Chaetoceros curvisetum) can develop at lower nutrient salt concentrations than can diatoms, and they may therefore continue to propagate in impoverished waters.

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As a further aid to utilization of the last vestiges of nutrients, the dinoflagellates, owing to their motility, are capable of adjusting themselves in some degree to optimum conditions.

Horizontal Ocean Currents

As an outcome of the phytoplankton collections taken by the Challenger from the various seas of the world, it appeared that in general no essential differences existed between the pelagic flora of different seas; but later, as a result of the more detailed plankton work of the German Plankton Expedition, Schütt concluded that different ocean currents are inhabited by characteristic types of floating plants.

Cleve (1900) was of the opinion, after studying extensive plankton collections from many separate areas, that plankton species endemic to separate geographic areas (each with its own set of environmental conditions) are transported from these areas by water currents to remote regions, depending upon the hydrographic conditions prevailing. Accordingly, the procedure of investigation should be first, to determine the geographic distribution of the separate species and to learn the conditions of life required by the principal plankton associations. Then, according to the theory, the origin of various water masses could be determined by a biological analysis of the waters to ascertain the type of plankton organisms they support. Cleve recognized a number of plankton communities with dominant types characteristic of separate ocean regions wherein the water has certain uniform characteristics with respect to the physical characters, but the hope of utilizing the diatom plankton types as indicators of water origin has not been fully realized. The nature of the life history of diatom populations, their prompt response by increase or decrease to fluctuating conditions of nutrients and other variable environmental factors, must make them of less value as direct indicators of ocean currents than are the planktonic animals with longer, more tenacious lives. Certain species of Ceratium have proved of special value in characterizing water masses, for example, the fluctuating flow of Arctic and Atlantic waters around Newfoundland (p. 865).

The diatom plankton types of Cleve are of great significance, however, as biological types (p. 793), each with different requirements of life which make them respond in succession to changes of season as living conditions become favorable to their specific needs.

From the strictly biological aspect, we are especially interested in the dispersal of species that is brought about by means of ocean currents. The widespread distribution of most species is evidence in itself of the operation of this type of dispersal. Many species are common to widely separate areas where living conditions are similar during at least a portion of the year. The diatom Asterionella japonica was not recorded from the waters of Romsdalsfjord, Norway, during investigations covering the

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period 1898–1900, but subsequently it appeared there, apparently carried to the region by currents (Gran, 1929). Ostenfeld (1909) has reported, on the basis of collections made cooperatively through the International Council for the Study of the Sea, that Biddulphia sinensis, originally an Indo-Pacific species, was accidentally introduced in 1903 into the North Sea off Hamburg and from there spread with ocean currents along the Danish and Norwegian coasts as far as Bergen.

It is not uncommon to find small numbers of neritic diatoms that have been carried far seaward with outgoing currents. They may even reproduce for a time by fission but they gradually become abnormal, with weakly silicified shells and diminutive in size; some may form resting spores which drift about. Just what are the oceanic factors that are unfavorable to neritic species is not clearly known. It may be a matter of nutrition or salinity, though, with respect to the latter, many neritic species are doubtless euryhaline.

The most popularly known drift of marine plants is that of the higher alga Sargassum. Although naturally an attached littoral plant, Sargassum may be torn from its moorings along the shore and float far to sea with the currents. Under these conditions it thrives vegetatively but is unable to reproduce except by fragmentation. Its tendency to accumulate in the slowly flowing cyclonic circulation in the North Atlantic has given the name Sargasso Sea to that relatively quiet halistatic area. Commonly, other littoral seaweeds and animals live attached to or among the branches and gas-filled floats of the Sargassum.

Temperature

Because of the close association of temperature with other factors, we have already had numerous occasions to refer to it in the course of discussion. It is certainly one of the most important of physical factors. However, it is not easy to generalize and designate any one factor as being more important than any other in a complex natural environment where all of the numerous known factors operate simultaneously. According to Liebig's law of the minimum, production is limited by the factor occurring in minimal quantity. This factor is obviously not the same for each circumstance. Hence, actually, the factor occurring in minimal quantity, whatever it may be, is temporarily the most important factor. It becomes the so-called “limiting factor” which has been defined as “any of the direct factors which is not optimal at the conditions present in a water mass, viz., without any change of the other factors.”

The rate of metabolism, hence the rate of growth and reproduction of any given species, is regulated by temperature. Just what will be the required range of temperature is dependent upon the species, but the warmest as well as the coldest waters of the sea are able, when other external factors are favorable, to produce a characteristic type of flora

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adapted to the conditions. The separate species are either eurythermic or stenothermic, depending upon whether their tolerance to temperature range is great or small. Different genera and different species within a genus may indicate a temperature preference, as shown by the following maximal growth periods for certain species in the Gulf of Maine at the surface temperatures indicated (Gran and Braarud, 1935):

Neritic species of the higher latitudes are also durothermic with respect to low temperatures during resting stages. These resting stages are very resistant to extreme temperatures and have been found to be viable even though they have spent unfavorable periods frozen solidly in ice.

We may conclude, then, that one great influence of temperature is in determining the character, that is, the composition, of species that will develop in any one region at various periods of the year. In temperate latitudes it is possible, depending on season and other conditions, for both high-latitude and subtropical species to grow provided either that “seed” can be carried in by currents at the proper season or that durothermic resting stages can survive the “off” season and germinate again with return of the growing season.

In this way Cleve's geographical diatom types, namely, arctic, boreal, temperate, and tropical, are explained not as having been produced in and carried from these separate areas but rather as having their metabolic requirements adjusted to temperatures characterizing these regions. During seasons of unfavorable temperatures the stock of separate types is maintained as resting-spores or resistant individuals with potentialities of quick response upon the return of their specific temperature tolerance, the different species succeeding each other in order according to their requirements.

Perhaps one of the most far-reaching influences of temperature is indirect through its effect on the viscosity of the water. We have had frequent need to mention how vitally important it is that the open-sea plants be kept within the euphotic layer. The degree of viscosity or internal friction of the water is vital to passively floating organisms with a specific gravity greater than the water in which they live. Variations

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in salinity have only a small influence on viscosity, and owing to the small variations in salinity, except near shore, viscosity is not materially affected from this cause; but a change in temperature from 25°C to 0°C is sufficient to double the viscosity. With this in mind, we see how important it is to phytoplankton suspension when a transition or thermocline with a marked temperature gradient occurs within the euphotic zone. The rate of sinking at the transition layer may be sufficiently retarded to allow an accumulation of plants that would otherwise not have occurred owing to reduction of stock by sinking, with the subsequent slowing up of production that accompanies such withdrawal of stock (p. 772).

Winter and summer variations which occur in the structure of certain species are attributed to the temperature variations of the seasons in areas where there is great temperature range, but temperature differences in higher and lower latitudes have the same effect, consequently summer forms of high-latitude species may occur in the warmer seas or vice versa. The structural differences are concerned mainly with adaptations leading to a better adjustment to the floating existence. The summer or warm-water forms have thinner shells and are of more slender build. A classical example is given in the diatom Rhizosolenia semispina (fig. 70), wherein a temperate form (semispina) and an arctic form (hebetata), once regarded as separate species, may originate one from the other or wherein opposite ends of a single cell may even show characteristics of both. The form hebetata is now regarded as a primitive resting stage of the form semispina.

In concluding this discussion it should be emphasized that even though the conditions with respect to light, temperature, nutrients, and so forth may be favorable to diatom production, yet no spontaneous population development can take place if previous conditions with respect to any factor have left the water sterile of vegetative plants or of resistant resting spores of species capable of taking advantage of the return of good conditions. This may explain in some instances the dearth of phytoplankton in offshore situations where the great depth of water prohibits the ready return of resting stages common to species of neritic waters. The phenomenal outbursts of diatoms in arctic regions coincident with the spring melting of ice have been explained as probably being associated with the rapid germination of spores that have been locked in the ice and are released through melting. It is known that these regions simulate biological conditions of coastal areas and the population is largely neritic. In investigating oceanographic conditions at a line of stations through Barents Sea from the coast northward to the Arctic ice, Kreps and Verjbinskaya (1930) found in spring that the early vernal flares of diatoms were confined to coastal waters and to waters near the Arctic ice, while between these and at some distance from

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shore in branches of the North Cape Current of Atlantic water, the population was poor although nutrients were high. In the Arctic waters near the front of melting ice both nutrients and diatoms were abundant.

The stimulation of phytoplankton growth commonly observed to be coincident with the mixing of two bodies of water with different characteristics may also result from an inoculation of a sparse population living under poor conditions into more favorable waters which have lacked spores suitable to take advantage of the good physical-chemical environment.

Population control through biological factors, such as animal consumption, is discussed in chapter XVII.