FACTORS OF PHYTOPLANKTON PRODUCTION: I
In the study of plankton, the production is generally understood as being the amount of organic matter produced by the phytoplankton under a unit area of sea surface or in a unit volume of water during a given
The principal factors controlling productivity have been reviewed by Braarud (1935) and we follow his scheme with some modifications in outlining the analysis of the direct and indirect factors. Under the heading of direct factors are included (a) direct primary factors that operate directly on the growth and proliferation of the individual alga, and (b) direct secondary factors that directly affect the population density and, therefore, the total production which is possible in a given period of time.
Direct Primary Factors of Reproduction and Growth
The Energy Factors. In the presence of carbon dioxide and water, plants are able by virtue of their pigments to intercept the sun's radiant energy required by them in the manufacture of compounds of carbon. The chemical change is expressed in simple form by the equation 6CO2 + 6H2O → C6H12O6 + 6O2. This process of carbon assimilation is an endothermic reaction, wherein the energy absorbed is derived from the light and the resultant product contains more energy than was present in the reactants CO2 and H2O. This energy, stored in the complex organic substance of the plant, becomes the source of chemical energy for life processes, directly for those of the plant and of herbivorous animals and indirectly for those of carnivorous animals, and also for the heterotrophic bacteria and other saprophytic forms.
It is important to note that the by-product of carbon assimilation is free oxygen. The process therefore becomes a source of an appreciable portion of the dissolved oxygen in the water and, consequently, is of great moment in the general metabolism of the sea, in the respiration of organisms, and in oxidation of organic and inorganic substances.
Since oxygen is always used in the respiration of the algae, the free supply dissolved in the water is drawn upon for metabolic processes during periods of low light intensity or when the plants have sunk to a depth at which the light intensity is below the minimum required for oxygen production by photosynthesis to balance oxygen consumption by respiration. The depth where light intensity is just sufficient to bring about this balance is known as the compensation depth (cf. p. 779).
Factors of Food Supply. The utilization of carbon dioxide is directly associated with the process of photosynthesis and is briefly discussed above. It is sufficiently abundant in the sea at all times, either as a dissolved gas or as a fixed constituent of the bicarbonates, to meet the requirements of the plants; it is, therefore, apparently never a limiting factor in phytoplankton production in the sea, for as rapidly as it is consumed by the plants a supply becomes available by the hydrolysis of the bicarbonates (p. 192). It has been estimated by Moore (in John-stone, Scott, and Chadwick, 1924) that in the Irish Sea 20,000 to 30,000 tons of carbon dioxide per cubic mile of sea water are passed through the biological cycle annually.
Although carbon dioxide cannot be considered a limiting factor in plant production, it is an item of far-reaching biological significance. In the final analysis the carbon compounds of all living creatures of the sea, from protozoa to the higher animals, come directly from the carbon dioxide in the sea.
Under dissolved nutrient salts we include the mineral salts that have been shown to influence and at times limit or control the production of phytoplankton, namely, the nitrogen and phosphorus, and also, to a more uncertain degree, iron and other trace elements. The control of growth is expressed in Liebig's law of the minimum, which states that growth is limited by the factor that is present in minimal quantity.
In the early studies of phytoplankton, Brandt (1899) suggested that diatom growth must be regulated by the nutrient substances that the diatoms utilize in the lighted waters of the sea. He anticipated the importance of compounds of nitrogen and phosphorus as substances which, according to Liebig's law, might be limiting factors. With the improvements of analytical methods by Atkins and Harvey, it has been shown beyond doubt that Brandt's theory was correct. Various investigators have demonstrated that phytoplankton organisms may assimilate different compounds of nitrogen (cf. p. 915), not only nitrates but also nitrites and ammonia (Schreiber, 1927, Braarud and Föyn, 1931, Harvey, 1933, ZoBell, 1935). Of these, nitrates are the most important, and in waters of temperate and arctic latitudes they accumulate during the winter and form the main nitrogen supply for spring diatom growth (Cooper, 1937).
The utilization of nitrates and phosphates in the synthesis of organic substance proceeds at an approximately parallel rate so that, although both may become markedly reduced by plants, the ratio of the two approaches fifteen atoms of nitrogen to one atom of phosphorus, with some deviation called the “anomaly of the nitrate-phosphate ratio,” perhaps dependent upon stages in the nitrogen cycle, a more rapid bacterial regeneration of phosphates, and the history of the particular body of water. In keeping with this there is an agreement in the ratio
Although the two elements discussed above have been shown to be vital to plant production, yet in nature the diatom population has been known to decrease while these nutrients were still present in sufficient quantity to support production. In these instances the limiting factors must be looked for elsewhere.
Gran (1931) believed that low concentrations or lack of iron might be a factor in limiting plant growth at times, especially for neritic species. From experiments, this seems probable (Harvey, 1937), and Thompson and Bremner (1935) have recorded a reduction in the quantity of iron in sea water coincident with heavy diatom production.
There are still other elements that occur in minute quantities in sea water or as traces in the analysis of plants, but since the status of these in the economy of the plant is as yet uncertain, they will not be dealt with in this general survey. Manganese, for example, has been shown to influence the growth of the diatom Ditylum (Harvey, 1939).
Silicates, used in the formation of the siliceous shells of diatoms and of certain other organisms, show seasonal fluctuations and also vertical distribution correlated with phytoplankton activity (Atkins, 1926, Harvey, 1928). Yet there is no evidence that reduction of silicon ever becomes a limiting factor. However, data from areas especially rich in silicon show a degree of utilization of this element by diatoms that would exceed the total supply available if applied to areas of low silicon (p. 261).
Accessory Growth Factors. It is becoming increasingly evident that the nutritional requirements for a lively diatom growth include substances not referred to in the above consideration. In experimental cultures utilizing artificial sea water, Allen (1914) found that the diatom Thalassiosira gravida would not grow unless small quantities of natural sea water or extracts of the marine alga Ulva were added. The accessory growth substance added with the sea water and the alga is not known. More recently Harvey (1939) has shown that even natural sea water enriched with nitrate, phosphate, and iron may lack the growth substances necessary for the continuous production of the marine diatom Ditylum brightwelli. The experiment indicates also that there are complementary substances, neither of which function well without the other. Some diatoms, for example Nitzschia closterium, apparently do not need the accessory substances although their presence stimulates growth. It is thought that diatoms like Nitzschia may be able by their own activity to make the organic accessory required. The accessory substances are
The above will serve to illustrate in part the complex problems involved in the explanation of phytoplankton nutrition.
Factors Influencing Metabolism. The rate of metabolism is much accelerated with rise in temperature. According to van't Hoff's law the increase is two to three times for each 10° rise in temperature within favorable limits. Very little is known regarding the optimum temperature conditions for the various phytoplankton species. However, it is known that various species may be attuned to a given temperature range. The species with common temperature requirements constitute biological groups which, if cold-water loving, may thrive in the Arctic in summer and in lower latitudes only during colder seasons. The growing season for a cold-water group may thus shift toward the Equator as winter approaches, and that for a warm-water group poleward with the approach of summer.
The salinity of the water is important in maintaining the proper osmotic relationship between the protoplasm of the organism and the water. The extent to which osmotic relationships can vary is dependent upon the species. Very little study has been made on the osmotic relations of diatoms, but the diatom Ditylum apparently does not act as an ordinary osmotic system (Gross, 1940). Some diatoms, especially neritic forms, have a tolerance for a rather wide range of salinity and are known as euryhaline forms, while the oceanic forms are usually stenohaline, that is, capable of enduring only small changes in salinity. Changes in this factor operative mainly in estuarine or in inshore situations. The variations in salinity operate mainly as a selective agency determining the composition or types of species that make up the population rather than on the fertility of the region.
The hydrogen-ion concentration or pH of sea water is generally maintained within narrow limits owing to the buffer effect of the dissolved salts (p. 202), hence its range of variations at most, perhaps, has only a moderate influence as a limiting factor for phytoplankton. However, during periods of high diatom production a marked rise in pH does occur as a result of the rapid utilization of carbonic acid by the plants during photosynthesis. On such occasions an excessive rise might tend to act as a natural check on further proliferation of some species, although this has not been shown for diatoms. Gail (1920) found that growth of the brown benthic alga Fucus evanescens is much inhibited at the high pH
Direct and Indirect Secondary Factors Influencing Population Density
We have already described the methods of reproduction characteristic of the plankton algae. These methods, which involve mainly simple cell division, are highly efficient and under optimal nutritional and metabolic conditions result in building up by geometric progression an excessively dense population. Any factor, then, that disturbs this progression has a far-reaching effect on the total numbers that can be produced in a given period of time.
By way of illustration, Braarud shows in a hypothetical example the difference between two identical populations of 500 cells per liter after nine cell divisions, when one population suffers no loss between successive cell divisions, while the other is assumed to experience a net loss of 10 per cent between the successive divisions. The undisturbed population would have increased at the end of the given time to 256,000 cells per liter, whereas the other at the same time would have only 99,159 cells per liter. The total withdrawal in cells would be only 12,343, but these plus their potentiality to produce yet other cells in the given time would amount to 144,498 cells per liter, in other words, the difference in increase between the two initial populations of 500 cells per liter at the end of nine cell divisions.
Just how much time would elapse during nine cell divisions in nature is dependent upon the living conditions and the species involved. The rate of division is dependent, of course, upon the direct primary factors mentioned above. In culture experiments (Gran, 1933) in the sea at Woods Hole it was found that population increases corresponded to seven divisions in three days for Chaetoceros compressus, six divisions in five days for the oceanic species Rhizosolenia alata, and five to six divisions in three days for other species. It has been estimated by Harvey et al (1935) that diatoms divide at a rate of once each 18 to 36 hours.
In nature, the number of cells lost between successive divisions would not remain constant even when resulting from consumption by a uniform population of filter-feeding animals, for there is some evidence that the rate at which these animals filter water remains the same whether or not the water is thinly or thickly populated with plankton food (p. 901). Harvey et al also show that during periods of abundant food the grazing plankton animals consume more than they are able to digest and void pellets of only partially digested diatoms.
Consumption. Since the phytoplankton is the main pasturage of the sea, it is very heavily drawn upon by the countless numbers of herbivorous plankton animals living within or periodically invading the euphotic zone. This has long been recognized as a foregone conclusion (Hensen, 1887, Lohmann, 1908),
The planktonic copepods are doubtless the chief diatom grazers, and due to their vast numbers they must exact an exceedingly heavy toll. In examining the digestive tracts of copepods, Dakin (1908) found that diatoms were the most abundant organisms present, especially species of Thalassiosira and Coscinodiscus. Species of Peridinium were next in importance. Esterly (1916), in direct examination, also found evidence of phytoplankton grazing, there being included in the digestive tract diatoms, dinoflagellates, and coccolithophores. Lebour (1922), Marshall (1924), and others have also shown that diatoms are important in the diet of copepods.
In addition to the copepods there are also large numbers of other small animals, especially the larval stages of benthic invertebrates, that graze directly upon the phytoplankton. For example, larval annelids are voracious feeders and, when abundant, may diminish materially the diatom population. Lohmann, working at Kiel, calculated that during the course of a year the increase in volume of pelagic plants was 30 per cent daily. Hence, that fraction of the plant population could be consumed daily by grazers without endangering the plant stock, if no other loss occurred.
The unevenness of phytoplankton distribution both in space (horizontally and vertically) and in time may reflect relative intensity of grazing rather than control through nutrient or physical conditions of the water, and actually more organic production may have taken place in areas only moderately rich in plants at any given time (p. 901).
Sinking. Even though diatoms are especially adapted to a floating existence, the suspensory organs and analogous structures usually operate only to retard sinking and not as a complete counter to the constant pull of gravity. Therefore, many individuals of the population tend to sink below the euphotic zone and may be considered as being withdrawn from the reproducing population as completely as if consumed by animals in the euphotic zone, unless before death they are fortuitously returned to the lighted waters by ascending water movements. According to the definition of compensation values (pp. 778 and 779), when the depth to which the plants have sunk is characterized by light with intensity below the “compensation point,” theoretically they would be considered as having become, at least temporarily, nonproducers for the twenty-four hours considered. It is probable, however, that the slowly sinking specimens have an adaptability enabling them to carry on photosynthesis sufficiently to reproduce slowly at a lower illumination than is indicated for experimental cultures at the compensation point. Harvey (1939) found a “physiological state” in Ditylum which indicated an adaptability to
In connection with the velocity of sinking, temperature becomes an important indirect factor influencing production owing to its marked effect on viscosity. A marked discontinuity layer, providing a sharp temperature decrease within the euphotia layer, is an important feature in maintaining the plants in the productive layer, since viscosity is inversely proportional to temperature and the rate of sinking is inversely proportional to viscosity.
Vertical Transport. Some of the points discussed in relation to sinking will be equally applicable in the factor of vertical transport. We learn from the discussion of turbulence (p. 471) that water particles within a water mass are not at rest but may be shifted in various directions. Passive microscopic objects, such as diatoms, caught in these shifts are transported along with the water. But as far as transport is concerned, we are interested here mainly in the vertical component of turbulence. If this vertical component is confined to the transportation of particles up or down within the euphotic layer, its effect on the production will be of no great significance, although it is of importance in maintaining a “seed” supply in the euphotic layer. If, however, the movement involves a transport of water from the productive layer downward into darker layers, it will have a deleterious effect on production in so far as it carries with it a certain portion of the phytoplankton population. This deleterious effect may be partly compensated for by a return of normally sinking plants to the lighted zone by ascending currents, but the time spent below optimum light conditions must constitute a loss.
Indirect Factors. The indirect factors of productivity also belong to the secondary group and operate simultaneously with them, in most instances also with the direct primary factors. Temperature, for instance, modifies the rate of metabolism, while at the same time it regulates the viscosity, and the vertical temperature gradient tends to reduce active turbulence. On the other hand, turbulence, upwelling, or convection currents are essential to the return of nutrients to the euphotic layer; thus the effect on the population is very complicated.
Among the more obvious of indirect factors of productivity may be listed water movements of various kinds, stability of waters within the euphotic layer, discharge of rivers, meteorological conditions, bathymetric conditions, and geographic position. The separate indirect factors exert their influence on productivity through the effect on the direct factors, and also on the other indirect factors. As a result, a complex of forces is constantly at play to increase or to decrease the total production during shorter or longer periods of time.