SCOPE 13 - The Global Carbon Cycle

ABSTRACT

Total annual primary production of aquatic ecosystems, comprising phytoplankton, coastal macrophytes, coral reefs, and freshwater production, is estimated at 45.8 x 10¹⁵ g C. A critical evaluation of methods used for measuring primary photoplankton productivity is given, from which it is concluded that the estimate for primary production by phytoplankton must be adjusted to yield an annual production rate of 43.5 x 10¹⁵ g C. Phytoplankton production appears to be 95% of total primary production in the oceans. The small areas of coastal macrophytes, salt marshes, and estuaries contribute 3.18% of the global aquatic primary production. Also, coral reefs, although very productive, occupy too small an area to contribute significantly to aquatic primary production only 0.65%. On the basis of present knowledge of phytoplankton physiology and evaluation of radiocarbon measurement of primary production, higher yields of oceanic phytoplankton production can be expected in the future.

10.1 INTRODUCTION

Unicellular algae (phytoplankton) are initially responsible for primary production, i.e. fixation of CO₂ or HCO₃ in seas and oceans. These include diatoms, dinoflagellates and coccolithophores. Cellular division occurs at least once in 24 hours, so growth is rapid and is controlled chiefly by the availability of nutrients, especially nitrogen and phosphorus and light, as well as by grazing of herbivores.

The significance of light has been studied by means of theoretical calculations on primary production in seas and oceans, taking light as the controlling factor. Such work has been carried out by Ryther (1959), Russell-Hunter (1970) and Vishniac (1971). The results of these calculations clearly show that, with the amount of light available, primary production in seas and oceans should be at least 5 to 10 times greater than determined by direct measurements. Evidently, factors other than light limit plankton growth.

In a marine environment, carbon dioxide or bicarbonate will not be a limiting factor, as only about 1% of the inorganic carbon in sea-water is utilized. Inorganic carbon can only be a limiting factor if used exclusively in the undissociated form (Fogg, 1975b).

Grazing, especially by zooplankton, stabilizes the phytoplankton population over a short period of time, Over longer periods, i.e. during a plankton bloom, there is an increase in the zooplankton population. A high grazing pressure by zooplankton stimulates phytoplankton growth, due to the nutrients liberated by the grazers (Strickland 1972).

Temperature can only be a regulating factor if both light and nutrients are in excess. Enzymic, non-photochemical processes then predominate, and overall carbon synthesis has the high Q₁₀ value (greater than 2) characteristic of enzymic reactions. Behaviour varies greatly between species, and great adaptation is possible (Strickland, 1958).

Nutrients, especially nitrogen, are the most significant limiting factor in great parts of the oceans. Algae can store amounts of phosphate and nitrate beyond their needs (Steemann Nielsen, 1953; Fogg, 1975b), but nitrogen and phosphorus, and to a lesser extent silicon, are the principal limiting factors for marine phytoplankton populations. In addition to these nutrients, certain trace metals can be considered as limiting factors, for example iron in the Sargasso Sea (Fogg, 1975b).

The availability of nutrients to the phytoplankton is determined by hydrographic factors. An early evaluation of the importance of hydrography for primary production on a global scale was given by Sverdrup (1955). He published a world map based entirely on hydrography data. Polar and boreal regions were considered as moderately productive and large parts of the oceans in the'lower latitudes were considered as having a low productivity, except in areas near the equator. This global picture has since been confirmed by investigations on primary productivity (Steemann Nielsen, 1963; Ryther, 1963; Strickland, 1965; Koblentz-Mishke et al., 1970).

At lower latitudes, specifically in subtropical regions, open-ocean water contains a low concentration of nitrogen (about 0.010.02 mmol/l) and phosphorus (about 1015% of the nitrogen value). As a consequence, these areas have a low primary production (about 30 g C/m² year). In anticyclones the water column has a high stability, an absence of silt, low amounts of algae, and very little water movement.

In higher latitudes (4060^°), light incidence is reduced during winter, the water is more turbid, and turbulent mixing carries the algae to depths 5-10 times the thickness of the euphotic layer. As a result, primary production stops almost completely. In spring, stratification develops and a plankton bloom is initiated, exhausting the nutrients in the euphotic zone in a matter of a few weeks. This is followed by a period of reduced primary productivity. In autumn, new mixing periods alternate with stable periods, and a smaller secondary bloom occurs.

At high latitudes, the Arctic Ocean has a very low production (l g C/m² year; Bunt, 1971), since this region is covered with pack ice nearly the whole year. In contrast, the ocean around Antarctica is the world's most fertile sea. Upwelling at some distance from the edge of the antarctic continent results in a high nutrient concentration. In spite of intense turbulence, low temperatures, and a short summer season, about 100 g C/m² year are produced.

On a more regional scale, hydrographic factors can greatly influence the rate of production. The most important of these is coastal upwelling, which is caused, in part, by trade winds. On the west side of the continents, especially off the coast of Africa and South America, the surface coastal waters are driven off-shore and are replaced by waters from greater depths (a few hundred metres) which are far richer in nutrients, thus causing high primary productivity.

High primary productivity can also be found in equatorial waters. In the eastern part of the Atlantic and Pacific Oceans, a clearly higher primary productivity takes place in the region along the equator due to the trade winds, which also induce upwelling.

In estuaries, a `food trap' occurs resulting from a circulation caused by a surface stream flowing seaward, and a bottom current flowing in the opposite direction. As a consequence, estuaries often have a very high primary productivity, which persists during the whole year in low latitudes.

In order to obtain reliable estimates on primary production in lakes and oceans, a critical evaluation of the techniques used in measuring primary production is given first.

10.2 A CRITICAL EVALUATION OF METHODS USED IN MEASURING PRIMARY PRODUCTIVITY

Several methods can be used for the measurement of primary production; accuracy depends primarily on the sensitivity of the method. Primary production can be measured by the amount of oxygen released during photosynthesis. Oxygen concentration is usually measured by the Winkler titration; which has a sensitivity of 0.15 mg O₂/l (Hall and Moll, 1975) to 0.02 mg O₂/l (Strickland, 1965; Golterman, 1975).

When oxygen production exceeds 0.5 mg O₂/l, polarographic determinations can be used (Hall and Moll, 1975). The subtraction of a dark-bottle value rests on the assumption that respiration in the dark is the same as in the light. This certainly has not been proved. Because of its rather low sensitivity, this method cannot be employed for primary production measurements in seas and oceans, except in coastal regions. However, it is used for the measurement of primary production of coral reefs. Accuracy can be affected by the presence of organic material.

Primary production can also be measured by determining the amount of functional chlorophyll present. Chlorophyll is extracted with acetone and determined spectrophotometrically or fluorometrically. Unfortunately, investigators do not agree as to how photosynthesis can be derived from chlorophyll estimates, because chlorophyll can have varying photosynthetic activity, depending on age, availability of nutrients, water temperature and season (Hall and Moll, 1975).

Adaptation to light intensity occurs; at minimal light intensities there is more chlorophyll in the cells than at high light intensities. The algae need 20 to 40 hours to adapt to a change in light intensities. The fact that chlorophyll concentrations in the seas and oceans vary by a factor of more than 1000, and those of primary production less than 50 (per volume) (Fogg, 1975b), leads us to conclude that measurement of primary productivity by means of chlorophyll concentration is not to be recommended.

The radiocarbon method is presently the most widely used to measure primary production in seas and oceans and was first introduced by Steemann Nielsen (1952). This technique involves the addition of a small amount of radioactive NaHCO₃ to a sea-water sample, and measures the amount of carbon taken up by the cells after a defined incubation time. It can measure far smaller levels of primary production than previous methods. Measurements can be made in situ, incubating the samples in the same depth from which they were taken, or on board a ship. Here the amount of light for each sample is adjusted, with the aid of filters, to the level at its original depth.

Owing to differences in the techniques used by various investigators employing the radiocarbon method, different results can be obtained. Soviet investigators use a standardized technique, but investigators from western countries use individually adapted methods, making it very difficult to compare the data. Many investigators do not give a description of their techniques which would make intercalibrations possible. A standardization of techniques for measuring primary production is necessary.

In view of differences in the radiocarbon techniques used and quantitative uncertainties, the relevant technical and physiological factors pertaining to these techniques will be briefly discussed here.

In principle, any measurement of a water sample in a closed glass bottle, even when carried out in situ, will not guarantee a primary production value which reflects that of the water of the site of collection. The absence of turbulence, which influences the amount of nutrients, light, excretion products, and CO₂, could conceivably change primary production inside the bottle. Furthermore, the glass surface of the bottle is a substrate for bacteria and some algal species, which grow rapidly under these circumstances. This difficulty can be overcome by using relatively brief incubation periods (24 hours). By exposing water samples from greater depths to direct sunlight, a light shock may occur, which should be prevented. A few investigators have used blue filters, instead of neutral ones, in incubations performed aboard a vessel. A comparison reveals that about 60% more light passes through blue filters relative to neutral filters (Kiefer and Strickland, 1970); appropriate corrections should be made.

The bicarbonate standard solutions can show differences of up to 9% in radioactivity (Ward and Nakanishi, 1971), which requires a check of each standard solution prior to analysis. In addition, bicarbonate standard solutions may contain a small amount of labelled organic matter with up to 0.01% of total radioactivity, an amount high enough to affect data on extracellular excretion products in tropical seas. Standard solutions can be purified by exposure to ultaviolet radiation, which decreases organic matter content appreciably (Williams et al., 1972). Investigators do not always correct for the rate of assimilation of ¹⁴CO₂, which is 6% below that of natural CO₂ (Golterman, 1975).

The best way to stop photo assimilation is filtration immediately after incubation. Halting the reaction by placing the bottles in the dark complicates the issue, because of carbon fixation in the dark (Sharp, 1977). A slightly improved method is to add some formalin to the bottles. However, this kills the plankton cells and can cause the release of soluble organic substances.

Filtration of the phytoplankton cells can lead to cell rupture, which results in lower activity of the cells, as indicated on a GeigerMüller counter or with liquid scintillation. Breakage of cells occurs particularly when large volumes are filtrated (Arthur and Rigler, 1967), or when high filtration pressure is applied. Different results have been reported with changes in filter pressure. Smith (1975) found no differences with filtration pressures in the 01292 mm Hg range. In contrast, Herbland (1974) found a sharp increase in dissolved, labelled organic substances with filtration pressures from 75 to 250 mm Hg; at pressures exceeding 250 mm Hg, values remained constant. Apparently, the effect of filtration pressure in cell rupture depends on the species of algae and their respective growth stage.

A. second disadvantage of filtration rests on the fact that filters can retain organic substances and inorganic carbonate, yielding deceptively high values for cellular primary production and too low values for extracellular excretion (Nalewajko and Lean, 1972). According to Berman (1973), fixation of organic matter on filters is not a serious problem. Fixation of inorganic carbonate on the filter can be remedied by `fuming' the filter in HCl vapour.

When keeping dried filters in vacuo, in desiccators prior to radioactivity measurements, 21% (Ward and Nakanishi, 1971, 1973) or a mean of (30% 2.950.7%, Wallen and Geen, 1968) loss of radioactivity occurs. These losses occur almost entirely in the first 24 hours. The percentage depends on the species composition of the phytoplankton.

Following filtration, the low-molecular products, which are released by the cells during incubation, are determined. The labelled bicarbonate is removed by acidifying and aerating the filtrate. Smith (1975) demonstrated that in order to remove all labelled bicarbonate, the pH of the filtrate should be below 2.53; at this pH, the loss of organic matter by evaporation or decomposition is very small. Several investigators who have worked on extracellular excretion have not paid attention to this effect (Fogg et al., 1965; Horne et al., 1969; Samuel et al., 1971; Choi, 1972). According to Smith (1975) an aeration time of 10 minutes should be long enough under the right conditions; CO₂ gas is more effective for aeration than air.

The disadvantages of filtration led Schindler et al. (1972) to omit filtration altogether, and to measure the whole sample by direct acidification and aeration. Using this technique, it is not possible to distinguish between the amounts of carbon fixed in the cells and those excreted extracellularly.

In addition to technical difficulties, differences in primary production estimates can result from the influence of physiological and environmental factors. In measuring primary production in seas and oceans, various species of algae can react differently according to varying environmental conditions. Growth phases (lag, log, stationary or scenescent phase) can be different for various algal species. All this can have a pronounced effect on primary production measurements.

Usually, it is assumed that no significant primary production occurs at levels below a light intensity of 1% of that in surface water. However, Venrick et al. (1973) showed that in the central Pacific, and especially near the axes of the Central Pacific Gyres, maximal chlorophyll concentrations can occur below a 1% light level during the summer, when the water is stratified at this level. These findings may imply that primary production levels are significantly higher in very oligotrophic regions than has previously been supposed.

Doty and Oguri (1957) have reported that primary production of natural phytoplankton populations exhibits a distinct diurnal rhythm, which appears to be dependent on latitude. The ratio between maximum and minimum primary production per day ranged from 10 at the equator to close to 1 at a latitude of about 75^° N or 75^° S, respectively (Doty, 1959). This diurnal rhythm in primary production is caused by a variation in photosynthetic capacity which is largely independent of chlorophyll concentration or biomass. Little is known on diurnal variation in respiration (Sournia, 1974). A correction can be made for diurnal variations, by taking sample times at the intersection of the diurnal curve and the mean production per hour for each geographical position.

The diurnal rhythm can be described as analogous to the yearly variation in oceanic primary production. In polar regions, there is only one plankton bloom in the short summer, and in temperate regions there are blooms in spring and autumn, whereas in subtropical and tropical regions there are no distinct blooms. This does not imply that there are no variations in primary production in these regions over the year, but that the variations are quite small. Seasonal patterns are determined by several factors and their interaction is very complex and not well understood. There are only a few studies of primary production covering a whole season. The ratio between the yearly maximum and minimum production does not differ much from that of the diurnal production rhythm.

Since the radiocarbon method was introduced by Steemann Nielsen (1952), different opinions have been expressed on the results: do they give `net' primary production (Ryther, 1956), `gross' primary production (Fogg, 1963), or does the value lie between these extremes (Steemann Nielsen and Hansen, 1959)? It is not known whether all fixed carbon comes from newly assimilated CO₂ or partly from older respired carbon; CO₂ from respiration can be used again for photosynthetic fixation before being released. Unless incubation occurs within a rather short time, a value close to net primary production is found. The assumption is usually made that the radiocarbon method approximately reflects net primary production.

Many investigators have reported that algal cells excrete labelled organic substances during incubation (Hellebust, 1965). A list of the different substances excreted has been given by Hellebust (1974). The most significant factors influencing extracellular excretion of algae are: (i) the amount of light: (ii) the cell density (Fogg and Watt, 1965); (iii) the growth phase of the algal cells; and (iv) stresses, for example salinity variations. Some investigators (Ryther et al., 1971; Sharp, 1977) doubt whether extracellular excretion occurs in healthy plankton cells; others, for exampe Fogg (1975b, 1977), are convinced that healthy cells excrete. Sharp (1977) mentions shortcomings in measuring techniques; he stresses the necessity for a careful statistical evaluation of results. In the author's opinion, Sharp's claim that extracellular excretion does not occur in healthy cells is not convincing, although his methodological recommendations should be followed by investigators working in this field.

In addition to the influence of excess light (Ignatiades and Fogg, 1973), cell density is an important factor in extracellular excretion. The highest percentage of extracellular excretion occurs in populations living in oligotrophic waters and the lowest in those present in eutrophic waters (Thomas, 1971; Anderson and Zeutschel, 1970; Choi, 1972; Berman and Holm-Hansen, 1974).

The growth phase of the algal cells also influences the amount of extracellular excretion. As a rule, all circumstances which prevent cell division, but permit photoassimilation, result in the excretion of a large part of the synthesized compounds (Hellebust, 1974).

Another problem in measuring primary production is dark fixation of carbon. Dark fixation probably involves heterotrophic activity (bacteria), as well as changes in the algal physiological pathways, but investigations on this have so far been inconclusive. Golterman (1975) supposed that growing algal cells need -ketoglutarate and oxaloacetate from the Krebs cycle when forming proteins. For the regeneration of these substances pyruvate is needed, which is formed during photosynthesis by means of the WoodWerkman reaction. Since this reaction does not fix chemical energy, unlike the photosynthetic carbon fixation, it should not play a role in net carbon fixation. With the introduction of the radiocarbon method, Steemann Nielsen (1952) observed that for an incubation time of four hours, dark fixation yielded 13% of light fixation; he argued that this amount had to be subtracted from the light fixation. Most investigators have subtracted, dark fixation from photoassimilation, some have neglected it, while others have assumed that it only involves an insignificant part of total carbon fixation.

Whether one subtracts or not, dark fixation can have consequences for the assessment of primary production rates, especially in oligotrophic areas. The ratio of dark fixation to light fixation is strongly related to cell density. Dark fixation in oligotrophic waters can exceed that in eutrophic waters by tenfold (Morris et al., 1971). According to Burris (1977) dark fixation can vary from 9.7 to 77% of total carbon fixation. Also, the Share of dark fixation in the total carbon fixation increases with decrease of light intensity. At very low light levels, dark fixation can be higher than photosynthesis (Gerletti. 1968).

Pollution can affect the growth of marine phytoplankton, especially in coastal areas. It has been demonstrated that heavy metal ions can retard the growth of phytoplankton cells (Jensen and Rystad, 1974; Jensen et al., 1976; Overnell, 1976), and germanic acid has a similar effect (Thomas and Dodson, 1974). Algal cells can, however, show a certain adaptation to pollutants over a period of 2040 days. Plankton cells can, in time, adapt to high concentrations of a number of pollutants (Stockner and Antia, 1976).

10.3 PRIMARY PRODUCTION IN AQUATIC ENVIRONMENTS 

10.3.1 Coastal Areas and Estuaries

In the coastal zones of seas and oceans, at least five different biotic components can be distinguished, each of which contributes to primary production: (i) macroalgae, (ii) marine angiosperms, (iii) phytoplankton, (iv) benthic diatoms, and (v) purple bacteria. Important groups of the first biotic component are the brown macroalgae such as rockweeds (Fucales) and kelps (Laminariales, e.g. Laminaria and Macrocystis), the red rockweeds (e.g. Chondrus) and the green macroalgae (e.g. Ulva, Enteromorpha). Kelps, in particular, are very efficient primary producers. Marine angiosperms such as eelgrass (Zostera marina L.), salt marsh cord grass (Spartina alterniflora Loisel) and turtle grass (Thalassia testudinum König) can significantly affect primary production. In addition to macrophytes, phytoplankton production can be high in coastal areas due to eutrophication. Benthic diatoms have also been found to contribute significantly to primary production in shallow waters. Photosynthetic purple bacteria may be another contributing source. However, no production estimates of these bacteria are known and, therefore, they will not be dealt with here.

Primary production of macroalgae in coastal areas is best known for the brown and red seaweeds of rocky coasts. Values for the productivity of green seaweeds from sandy coasts and estuaries are lacking, because these weeds are often not attached to a substrate.

Giant kelps (e.g. Macrocystis) are dominant along the coast of North America and on the southern half of the globe (Australia, New Zealand, South America, and South Africa). Various Laminaria species are dominant along the coasts of the North Atlantic (New England, Canada, northwestern Europe). Kelp forests are limited to cooler seas; above 20 ^°C, growth and vitality are limited (Pearse and Gerard, 1977); this is also true for rockweeds. The geographical distribution of the rockweeds is about the same as that of the kelps (Mann, 1972a).

Ryther (1963) indicated that seaweeds in the coastal zone might have a primary production amounting to one-tenth of the estimates of the ocean's phytoplankton production. Recent research on large kelps has shown that these seaweeds have a very high productivity, with a possible annual increase in the biomass by a factor of 5 (rockweeds) to 15 or more (kelps) (Blinks, 1955; Lüning, 1969; Mann, 1972a,b; Mann and Chapman, 1975) (Figure 10.l).

In kelps (Laminaria sp., Ascophyllum sp.), this can be explained as follows: although at low light intensities photosynthesis is almost independent of temperature, at high light intensities photosynthesis, as well as respiration, are strongly controlled by temperature. In this way, a seasonal adaptation of respiration occurs: with decreasing temperature, respiration declines faster than photosynthesis. In summer and autumn, an intensive photosynthesis enables storage of carbohydrates, which are used for growth in winter and spring. A long day-length in summer, at high latitudes, compensates for low light intensities. Besides the algae, photosynthesis is saturated at a light level of about one-third of full sunlight (Kanwisher, 1966).

Figure 10.1 The range of net annual primary production (g C/m² year) of the major marine macrophyte systems, compared with some terrestrial communities (quoted from Odum, 1971):1. Medium-aged oak-pine forest, New York II. Young pine plantation, England III. Mature rain forest, Puerto Rico IV. Alfalfa field, United States. (Mann, 1973. Reproduced by permission of the American Association for the Advancement of Science) 

In winter and spring, circumstances are favourable for growth, because high nutrient concentrations are available due to low plankton concentrations, and a high light transmission occurs in the water column (Mann, 1973; Mann and Chapman, 1975). No influences of geographic latitude on kelp production have been found (Parke, 1948; Kain, 1971).

Photosynthesis of giant kelps (Macrocystis sp.) adapt progressively to lower temperatures without loss of assimilation capacity (Mann and Chapman, 1975).

In rockweeds (Fucus sp.), seasonal fluctuation in storage products are much less marked than in kelps. There is little winter growth in rockweeds and storage products are provided directly by a high photosynthesis level during the summer. Storage products are mainly needed for respiration during the winter (Healey, 1972; Mann, 1973; Mann and Chapman, 1975).

The new data on kelp production allows total primary production of these plants to be recalculated on a global scale. The kelp beds have been mapped by Chapman, as given by Mann (1973) (Figure 10.2). From the work of MacFarlane (1952), Walker (1954), Mann (1972a) and Zenkevich (1963), estimates can be made of kelp biomass per km coastline in Nova Scotia (Canada), Scotland, and the West Murmansk coast., These areas yield amounts of about 1.350 t (wet weight) per km coast line. From a map of coastal land forms of the world (McGill, 1958), and using coastal lengths of countries as published by Karo (1956), the length of all coastlines where kelp beds are expected total 58 774 km. On the basis of maps given by Walker (1954) for kelp beds in Scotland, MacFarlane (1952) for Nova Scotia (Canada), and Zobell (1971) for California, it can be estimated that about 30 000 km coastline have significant kelp beds. Assuming a productivity to biomass ratio (P/B) of 10 (Mann, 1972b, 1973) the yearly production of kelps is 0.392 x 10¹⁵ g wet weight, corresponding to 0.022 x 10¹⁵ g C.

Figure 10.2 The distribution of Laminaria (L), Macrocystis (M) and Eklonia (E) in quantities sufficient for exploitation. The 20 ^°C isotherms are for summer in the northern and southern hemispheres, respectively. (Mann, 1973; after Chapman, 1960). Reproduced by permission of the American Association for the Advancement of Science)

No coastal length data were available for rockweeds. According to Mann (1972a) fucoids have the same geographical area as kelps. Biomasses of rockweeds per km coastline have been given by MacFarlane (1952) and Mann (1972a). An average of 300 t fresh weight per km coastline was estimated. The production of Fucus, Ascophyllum and other rockweeds is given as 5001000 g C/m² year (Mann and Chapman, 1975). This gives a P/B of about 5. The yearly production of biomass given by Blinks (1955) gives a P/B which agrees with this value.

The yearly production per km thus amounts to 1500 t wet weight. On a global scale, this amounts to 0.088 x 10¹⁵ g wet weight. Assuming that dry weight is 25% of wet weight and that 30% of dry weight is carbon (Mann, 1972a), annual production of rockweeds is 0.0073 x 10¹⁵ g C.

Another calculation of the production of benthic macroalgae on a global scale can be made, based on estimates of the standing crop of seaweed resources of the world, given by Naylor (1976). For red seaweed, a world standing crop of 2660 x 10⁹ g is reported (wet weight), and for brown seaweed, 14 600 x 10⁹ g (wet weight). According to the results summarized by Lüning (1969) and Mann (1972a), it is concluded that 15% of the total mass of brown seaweed are rockweeds. Assuming dry weight to be 25% of wet weight in rockweeds and 15% in kelps, and 30% of dry weight to be carbon (Mann, 1972a), the annual production of red weeds can be calculated as 1000 x 10⁹ g C, brown weeds as 820 x 10⁹ g C, adding up to 0.00 182 x 10¹⁵ g C, and kelps as 0.0056 x 10¹⁵ g C.

Compared with other calculations, the production of kelps and rockweeds shows a difference by a factor of 4. No estimate of the importance of extracellular excretion of photosynthesized compounds of brown or red weeds can presently be made, because of conflicting data presented by Moebus and Johnson (1974), and Sieburth (1969).

Another biotic element which contributes to coastal zone primary production is benthic diatoms, which can be at least as productive as the phytoplankton of coastal waters. Table 10.1 gives a compilation of measurements, derived from Cadeé and Hegeman (1974b). For one benthic diatom (Phaeodactylum tricornutum) a rather low amount of extracellular excretion of photosynthetic products has been demonstrated (Chapman and Rale, 1969).

Phytoplankton can have a higher productivity in coastal waters than in other shelf areas, due to eutrophication by rivers and human environmental influence. Table 10.2, derived from Woodwell et al. (1973), Gieskes and Kraay (1975), and Cadeé and Hegeman (1974a), gives a summary of production estimates.

Table 10.l Productivity of benthic diatoms. (After Cadeé and Hegeman, 1974b. Reproduced by permission of the Netherlands Institute for Sea Research)

Area	Annual production	Source
	g C/m2 year
Salt marsh, Georgia (U.S.A.)	200	Pomeroy (1959)
Danish fjords	116	Grøndved (1960)
Danish Wadden Sea	115178	Grøndved (1962)
False Bay	143226	Pamatmat (1968)
Ythan estuary	31	Leach (1970)
Southern New England	81	Marshall et al. (197 1)
Western Dutch Wadden Sea	60140	Cadée and Hegeman (1974b)

Another biotic element are angiosperms growing in coastal marshes, intertidally or submerged, which are known to have a high primary productivity. Dominant genera in coastal marshes are Zostera, Spartina, and Thalassia. At least six species of Spartina are C₄ plants, which might explain their high production efficiency in the physiologically `dry' salt marsh environment (see Chapter 8, this volume). In Table 10.3, some production values are given for these important genera.

Table 10.2 Productivity of coastal phytoplankton. (After Woodwell et al., 1973. Reproduced by permission of National Technical Information Service, U.S. Dept. of Commerce, Springfield, Virginia)

Locality			Annual productivity
			g C/m2 year
Denmark, Islefjord			260430
The Netherlands, North Sea coastal water			160180
Nova Scotia			190
British Columbia			450
The Netherlands, Wadden Sea			100120
State of Washington, Columbia River, north			152
river mouth			88
ocean beyond river			61
river plume			60
State of New York, Long Island Sound			205
Hempstead Bay			395
shallow water off New York			160
continental shelf			120
continental slope			100
State of North Carolina, coastal water			52
State of Georgia, coastal water			547
State of Mississippi, coastal water			228
State of Louisiana, Barataria Bay			170
India, Cochin backwater			124

Table 10.3 Productivity of intertidal or submerged marine angiosperms

Release of dissolved organic matter by marine angiosperms seems to be rather low (Brylinski, 1977; Penhale and Smith, 1977). The real problem in making primary production estimates for coastal waters and estuaries is that there are production estimates for the different plants, but there are no estimates for the surface area they occupy. A reasonable estimate can only be made for salt marsh production in the United States.

Reimold (1977) estimated salt marshes along the Atlantic coast of the United States to occupy a total of 589 480 ha. MacDonald and Bardour (1974) calculated the salt marsh area of the U.S. Pacific coast to be 30 800 ha. Chapman (1960) estimated a total salt marsh area of about 4 900 000 ha in the U.S.A., i.e. 1 420 000 in the Gulf of Mexico and about 3 009 200 ha in Alaska. On the basis of Turner's review (1976) of the primary productivity of salt marsh angiosperms along the Atlantic coast of the U.S.A., and MacDonald's (1977) for the Pacific coast, a total primary production of between 720 and 1081 x 10⁹ g C/year could be calculated for the Atlantic coastal marshes; between 1988 and 5538 x 9 g C/year for the Gulf coastal marshes; between 40 and 154 x 10⁹ g C/year for the Pacific coastal marshes; and between 120 and 1444 x 10⁹ g C/year for Alaska coastal marshes.

A map of the world distribution of salt marshes has been given by Chapman (1977), and an approximate coastal length of the salt marsh area can be determined from this source. The world production of salt marshes is estimated to be between 0.02 and 0.03 x 10¹⁵ g C/year, excluding root production and epiphyte production.

Woodwell et al. (1973) made a calculation for primary production of coastal marshes of the world, including mangroves, taking root production, benthic algal and epiphytic production, phytoplankton production and production of submerged angiosperms into account, but excluding benthic diatoms. The results are somewhat higher than those given in Tables 10.2 and 10.3. Woodwell et al. (1973) assumed an area of 0.35 x 10⁶ km² for coastal marshes of the world. Furthermore, they assumed three equal areas with productivities of 450, 1125 and 2250 g C/m² year. From this they calculated an annual coastal marsh production of 0.49 x 10¹⁵ g C.

For the global production of the open-water regions of estuaries, Woodwell et al. (1973) assumed an average net primary production of 675 g C/m² year and an area of open water of l.4 x 10⁶ km². The world production of open-water estuaries would then be 0.92 x 10¹⁵ g C/year. Total estuary production, including the marshes, would then be 1.41 x 10¹⁵ g C/year.

The total production of the coastal zone can be obtained by the summation of total estuary production and production of kelp and rockweeds, which then includes all biotic elements: l.44 x 10¹⁵ g C/year.

10.3.2 Seas and Oceans 

Much effort has been made to determine primary production in seas and oceans, especially since Steemann Nielsen (1952) introduced the radiocarbon method, opening the possibility of measuring primary production in oligotrophic regions. Most investigations are regional and local, and because of differences in the techniques used, a comparison of results and final integration to a general picture of marine primary production is very difficult.

In this review, only those publications are considered in which the authors have made their own calculations, and not publications in which estimates have been copied from other publications. Tables 10.4 and 10.5 give a number of production estimates for the global oceans and individual oceans.

Riley (1946) obtained his estimates by measuring the oxygen content of water samples. This method does not give reliable results in oligotrophic waters (compare Section 10.2) and Riley's estimate is certainly far too high. Steemann Nielsen (1953) used the radiocarbon technique for the first time on a voyage around the world. His data were chiefly from tropical and subtropical waters, with little data from temperate and polar regions. For this reason his global estimate is somewhat low.

 Table 10.4 Annual primary production in the world's oceans

Production
in 1015 g C		Source
126		Riley (1946)
15		Steemann Nielsen (1953)
20		Ryther (1969)
23		Koblentz-Mishke et al. (1970)
44		Bruevich and Ivanenkov (1971)
60	80	Sorokin (1973)
31		Platt and subba Ran (1975)

Table 10.5 Annual primary production by phytoplankton, individual oceans

Ryther (1969) divided the oceans into three regions: open ocean, coastal zone, and upwelling areas, with estimated mean primary production values of 50, 100, and 300 g C/m² year respectively. From this data, he calculated a total oceanic primary production of 20 x 10¹⁵ g C/year.

Koblentz-Mishke et al. (1970) made a statistical distribution of all published data, and distinguished five production groups: <100; 100150; 150250; 250500; >500 mg C/m² day. Each group represents a maximum in the distribution curve. They calculated a primary production of 23 x 10¹⁵ g C/year for the oceans, which they considered to be low. They also made a map (Figure 10.3) of oceanic primary production.

Bruevich and Ivanenkov (1971) considered the values of Steemann Nielsen (1953) and Koblentz-Mishke et al. (1970), on oceanic primary-production, to be too low because of errors inherent in the radiocarbon method. Moreover, by summing primary production per unit volume throughout the photosynthetic layer, Koblentz-Mishke et al. did not sufficiently account for the fact that, in tropical regions of the ocean, half of the production occurs in the lower parts of the photic layer. Bruevich and Ivanenkov (1971) revised the data of Koblentz-Mishke et al. (1970), by assuming that primary production is twice as high in the oligotrophic zones of the oceans, four times as high in the transition zones, and 30% higher in the medium- and high-productivity zones. This revision yielded a primary production for world ocean of 44 x 10¹⁵ g C/year.

Sorokin (1973) also distinguished five regions of productivity; internal seas, temperate ocean waters, tropical waters (continental shelf and open ocean), and polar and subpolar regions. His estimate is more than twice that of the other authors, because he assumed that the radiocarbon method, on the whole, underestimates primary production by a factor of 1.52. In addition, the other investigators sample, not at the minima and maxima of plankton distribution, but at specific underwater light intensities, which correspond to the transmission values of available neutral light filters. The zones of maximal plankton concentration can thus easily be missed by this procedure.

Figure 10.3 Distribution of primary production in the world oceans. (From Degens and Mopper, 1976; after Koblentz-Mishke et al., 1970. Reproduced with permission from Chemical Oceanography, Vol. 6 (2nd edn.). eds. J. P. Ripley and R. Chester. Copyright by Academic Press Inc. (London) Ltd.)

Platt and Subba Rao (1975) distinguished shelf regions, upwelling areas, and coastal waters. By arranging data for the individual ocean, they derived a total production of 31 x 10¹⁵ g C/year.

The most recent estimates presented in Table 10.4 may be too low, partly as a result of shortcomings in the radiocarbon method and partly because of hydrographical and physiological factors. A survey of these factors has been given in Section 10.2 and some adjustments will be made below.

The damage to plankton cells by filtration is quite variable and is dependent on the algal species involved; no correction can be given here.

Dark fixation could be important in primary production measurements, especially in lower levels of the photic zone or in oligotrophic seas. In cases where dark fixation has not been subtracted from values for photosynthesis, a significant upward correction should be applied to primary production, especially in oligotrophic seas. However, because the process of dark fixation is not well known, and inasmuch as only a few measurements of dark fixation have been carried out in the marine environment, no corrections will be made here.

Another observation important for primary production in oligotrophic waters has been made by Venrick et al. (1973). These authors reported that production below the 1% light level can account for 720% of total primary productivity. Since only a few observations were made, many more experiments should be carried out before an upward correction for primary production can be justified.

Wallen and Geen (1968), and Ward and Nakanishi (1971 and 1973) showed that keeping plankton filters in a vacuum desiccator for one day causes a radioactivity loss of 2030%. This fact had not"been considered prior to 1968. The use of a desiccator was recommended, however, in the widely employed standard method of Strickland and Parsons (1968). Thus, in the author's opinion, an upward correction of 20% for primary production values is justified for world phytoplankton primary productivity.

Extracellular excretion is an important part of photosynthetic production, especially in oligotrophic waters. To adjust for this contribution, values for primary productivities (expressed in mg C/m² day) and extracellular excretion (expressed as a percentage of total primary production) were combined from four authors (Anderson and Zeutschel, 1970; Ryther et al., 1971; Berman and Holm-Hansen, 1974; Smith et al., 1977). The curve between the sets of data was determined by means of the least squares method. With the aid of this relation, an overall correction of 20.3% was found for extracellular excretions, summing corrections for the five different production types distinguished by Koblentz-Mishke et al. (1970).

By applying the two corrections given above to the total production estimate of Koblentz-Mishke et al. (1970), a new total annual production value of 32.29 x 10¹⁵ g C is found. When the estimate of Platt and Subba Rao (1975) is corrected in the same way, an annual primary production of 43.48 x 10¹⁵ g C is derived.

In their publication, Koblentz-Mishke et al. (1970) already stated that their value, 23 x 10¹⁵ g C/year, might be low, due to use of the radiocarbon method and also because the area of the highly productive inshore region may have been underestimated. Consequently, they believed that 2530 x 10¹⁵ g C/year might be a more accurate figure. Platt and Subba Rao (1975) gave an estimate of 31 x 10¹⁵ g C/year. On the basis of the previous discussion, it is concluded that the corrected estimate of 43.5 x 10¹⁵ g C/year is the best approximation of primary production in seas and oceans.

10.3.3 Coral Reefs

Reef-building corals (hermatypical corals) live between the latitudes of 30^° N and 30^° S, occupying an area of 190 x 10⁶ km². Coral reefs occur only in the western regions of the oceans, since trade winds transport surface water westward and upwelling in the eastern parts causes lower water temperatures. Coral reefs and atolls are found mainly in the Indo-Pacific and the Caribbean (Stoddard, 1969). Three types of coral reefs can be distinguished: the atol, the barrier reef, and the fringe reef.

Corals are Anthozoa (Scleractinia), carnivorous animals which catch small animals with their polyps. However, they are also associated with zooxanthellae, which are essentially autotrophic dinoflagellates. These algae are near the surface of the coral tissues, which enables them to photosynthesize. The zooxanthellae supply organic carbohydrate and nitrogen compounds to their host (Lewis and Smith, 1971). Because corals need light for their zooxanthellae, they occur mostly at depths of less than 40 m. Porter (1976) showed from morphological data that all hermatypical corals are dependent on zooxanthellae, as well as on zooplankton. The surface : volume ratio and polyp diameter are measures of the relative importance of each of the two respective feeding methods. Coral reefs are rich biocenoses which include other primary producers, for example calcareous algae (Yonge, 1968).

Because of low primary production in the surrounding ocean water, coral reefs as such are highly self-sufficient biocenoses. Zooplankton, which finds shelter on the reef during the day, rises at night and is then caught by the tentacles of the corals. Also, benthic blue algae, which can fix nitrogen, occur on the reefs (Mague and Holm-Hansen, 1975; Wiebe et al., 1975).

Coral reefs show a high primary production, of approximately 15008000 g C/m² year gross production. In an experimental respirometer, pieces of coral gave lower productivities, of approximately 12002500 g C/m² year. Various production estimates, determined on the reefs in situ and in respirometers, are given in Table 10.6. These primary production rates are far higher than those in the surrounding ocean water, which range from 20 to 40 g C/m² year.

No estimate of the total surface of coral reefs in the world could be found in the literature. However, a calculation was made on the basis of five admiralty maps, which were selected to be representative for the coral reef region. The total length of coral reefs was measured for each reef category, and with the estimates of coral reefs as given by Chave et al. (1972), the surface area of each reef category actually covered with corals and calcareous algae could be determined. The total coral reef surface area was calculated. For the total ocean area where coral reefs occur (190 x 10⁶ km²), a coral surface of 112 341 km² was found. A total gross primary production of coral reefs of 0.47 x 10¹⁵ g C/year, and a net primary production of 0.30 x 10¹⁵ g C/year were obtained.

10.3.4 Freshwater Production

On a global scale, the amount of fresh water present in lakes and rivers is only 0.02% of the total water mass on earth (see Chapter 12, this volume, Fig. 12.l). The surface area is only 0.2% of the earth's total surface. Although phytoplankton production in fresh water generally has a markedly higher level than in the sea, it forms only a small part of total aquatic primary production.

Table 10.6 Primary productivity of coral reefs

		Gross primary	Net primary
		production	production
Source	Location	g C/m2 year	g C/m2 year
l. Production of whole reef communities
Sargent and Austin	Rongelapp Atoll	1460
(1949)	(N. Marshall Isl.)
Sargent and Austin	same location	1500	190
(1954)
Odum and Odum	Eniwetok Atoll	3504	2044
(1955)
Kohn and Helfrich	N. Kapaa Reef	3000	1400
(1957)		2900	511
Gordon and Kelly	Mokuoloe Island	7300
(1962)	Kaneohe Bay	not an autotroph reef
	Oahu, Hawaii
Quasim and	Reef in Arab Sea	4494	3618
Sankaranarayanan	(10° N 72° E)
(1970)
Smith (1973)	Eniwetok Atoll	3241	2190
	Hawaii	7358	6307
Smith and Marsh	Eniwetok Atoll	4380	2190
(1973)	Hawaii	8497	6307
Wanders (1976)	Curacao	5650	2330
2. Measurements with	respirometer.
Kanwisher and	Plantation Key,	2303	528
Wainwright (1967)	Florida, U.S.A.
Marsh (1970)	Eniwetok Atoll	1261	946
(only algae)	Kaneohe Bay,
	Hawaii
Litter (1973)	Hawaii	2495	2080
(only algae)

The measurement of primary production in fresh water meets many of the difficulties reported for the marine environment (compare Section 10.2). There are great differences among lakes, even among those in the same region, with regards to nutrient level and the degree of eutrophication. Apart from nutrients, three other important factors in freshwater production can be mentioned. Firstly, fresh water can have a high `background' colour, or turbidity, which will impede penetration of the available light. Secondly, with increasing population density, self-shading ultimately limits production. Thirdly, there is a clear trend of declining photosynthesis capacity per unit population with increasing population density (Talling, 1975).

Brylinski and Mann (1973) made a statistical analysis of the influence of various biological and non-biological variables on the primary production in 43 lakes and 12 reservoirs. These lakes are in latitudes from 10^° N to 75^° N, from sea level to an altitude of 2500 m. Considering production over the whole latitudal range, variables related to solar energy input have a greater influence on production (56% of variation) than nutrient-related variables (less than 15% of variation). When only those lakes and reservoirs located in temperate latitudes (39^° N to 55^° N) are considered, nutrient-related variables are more important. In both cases, geomorphological differences have little influence on productivity per unit area.

For productive lakes or ponds, production is approximately 1000 g C/m² year; values higher than 2500 g C/m² year are exceptional in natural lakes. In shallow lakes, production is limited by sediments, which are resuspended by wind-induced turbulence. An average plankton cell spends then a large fraction of its time in darkness. Few detailed studies have been made on respiration of algal cells. The impression is that, in fresh water, respiration losses can be more important in decreasing net photosynthetic production than in the sea.

A total carbon balance for one small temperate zone lake, Lake Lawrence, Southwestern Michigan, U.S.A., was made by Wetzel and Rich (1973). Freshwater primary production in different parts of the world is given in Figure 10.4. The relationship between primary production and various nutrient concentrations is illustrated in Table 10.7

Figure 10.4 Diagram comparing freshwater gross primary productivity (g C/m² year) of a number of sites with some data for ecosystems (quoted by Odum, 1971). A: coastal water (New York), B: young pine plantation (England), C: large flowing spring (Florida), D: mature rain forest (Puerto Rico). (From Brylinski and Mann, 1973. Reproduced by permission of the American Society for Limnology and Oceanography)

Table 10.7 Some general characteristics of lakes of various trophic status. (After Likens, 1975. Reproduced by permission of the Springer Verlag New York Inc.)

	Primary	Phytoplankton
	productivity	biomass	Chlorophyll-a	Total	Total
Trophic status	mg C/m2 day	mg/C m3	mg/m3	P (g/l)	N (g/1)
ultraoligotrophic	50	50	0.010.5	15	1250
oligotrophic	50300	20100	0.3-3
oligomesotrophic				5-10	250600
mesotrophic	2501000	100300	215
mesoeutrophic				10-30	5001100
eutrophic	600-8000	300	10-500
hypereutrophic				30-5000	50015000
dystrophic (humic)	50600	50200	0.110	110	1500

Primary production in various lakes based on Likens (1975), Schindler and Holmgren (1971), and Cadée and Hegeman (1974) is given in Table 10.8. According to Likens (1975), freshwater primary production of the world can best be calculated from the largest lakes (Lake Baikal and the Great Lakes), which account for 31% of the earth's surface fresh water.

The total area of inland waters is 2 x 10⁶ km². Combining macrophyte, periphyton, and phytoplankton productivity, the mean net production of lakes and rivers is about 200 g C/m² year, giving a net annual production of about 0.4 x 10¹⁵ g C.

As with marine phytoplankton primary production, this estimate can be corrected for loss of radioactivity on filters and for extracellular excretion (compare section 10.3.2). Applying these corrections, an annual freshwater primary production of 0.58 x 10¹⁵ g C is obtained.

Table 10.8 Primary productivity of some individual lakes, given in g C/m² year

10.3.5 Total Primary Production and Total Biomass in Aquatic Ecosystems

The relative importance of primary production in all aquatic ecosystems is given in Table 10.9 for different categories. For coastal areas, the highest production estimates as derived for seaweeds and salt marshes are used.

The results clearly indicate the dominant role played by oceanic phytoplankton in total aquatic primary production. The coastal zone provides only 3.13% of total primary production, but is of great importance with respect to the evaluation of human resources. Coral reefs account for only a small portion of the total primary productivity, for reasons of their restricted areal distribution. The total aquatic primary production given here is greater than that of other recent estimates. Future research, especially on oceanic phytoplankton, will probably result in even higher estimates than those given here.

Table 10.9 Primary production in lakes, seas, and oceans

Much work has been done by Russian investigators on the living biomass in seas and oceans, and the estimates presented here have been derived mostly from Russian sources (Tables 10.10 and 10.11).

Table 10.10 Biomass of plants and animals in the oceans

Table 10.11 Total biomass in seas and oceans, given in 10¹⁵ g C

	Plant	Animal
Source	biomass	biomass	Total
Bogorov (1967)*	0.153	2.925	3.078
Bazilevich et al. (1970)	0.077
Whittaker and Likens (1973)	1.760	0.449	2.209
Zenkevich et al. (1960)*		0.900
*From Moiseev (1969)

Comparing the Russian estimates with those of Whittaker and Likens, a striking feature is that the plant biomass of the latter is much higher than the Russian one, whereas a reverse picture emerges for the animal biomass. When the estimates of plant and animal biomass are compared, an inverted food pyramid can be seen, when using the Russian sources.

10.4 AQUATIC PRIMARY PRODUCTION AS A PART OF THE GLOBAL CARBON CYCLE

10.4.1 Sedimentation of Organic Carbon from the Photic Zone

Approximately 50% of the total amount of carbon dioxide originating from combustion of fossil fuels is retained in the atmosphere. The other half, and an unknown amount of carbon dioxide from clearcutting and burning of forests, is assumed to have gone into the oceans (Dyrssen, 1972).

Primary production could provide a `sink' for at least a part of that carbon, by means of sedimentation. Nearly the whole primary production is recycled in the upper 200 m of the oceans, but there is always a relatively small percentage that escapes recycling and sinks together with dead zooplankton to the sea floor. That percentage depends on the primary production values, the growth phase of the phytoplankton, the rate of grazing by zooplankton, and the intensity of remineralization by bacteria. In Table 10.12 some estimates from the literature are given.

A large part of this material is decomposed or metabolized underway, and only a minor part of it is deposited at the bottom of the sea. According to Lisitzin (1972), at a depth of 5000 m only 0.021% of the original amount of material reaches the bottom. Degens and Mopper (1976) state that 6.68.6% of the sinking primary production should actually reach the bottom; Garrels and Perry (1974) estimate this value to be only 0.01 % of total primary production.

Table 10.12 Percentage of total primary production sinking to deeper sea levels and to the bottom

10.4.2 Influence of Climatic Changes on Aquatic Primary Production

The direct influence of temperature changes on primary production in the oceans is probably not great, if those temperature changes occur gradually over a long period of time. Unicellular algae show a good adaptation to different temperatures, as for example in the Antarctic seas, where a relatively high primary^- production occurs in spite of low summer temperatures. Even under ice cover, there is a certain amount of primary production (Bunt, 1968; Bunt and Lee, 1970).

According to Bryson (1974), two forms of climatic changes can be distinguished: long-term changes (over about two centuries) when an ice age can start, implying a mean temperature change of 46 ^°C; and Holocene temperature changes, which can start within a few decades and imply far lower temperature changes. For example, in the period 1920 to 1940 the mean temperature of the northern hemisphere rose by about 0.5 ^°C. Observations on the biomass and the primary production in the oceans and their variations with time are few, and generally do not cover long periods. Tont (1976) has reported observations in the biomass of diatoms on the Californian coast (La Jolla) since 1928. Russell et al. (1971) mentioned observations on nutrients and zooplankton in the English Channel since 1924 and primary production measurements since 1964. Robinson (1970) and Reid (1977) reported observations on phytoplankton biomass in the North Sea and the North Atlantic, measured with continuous plankton recorders towed by merchant ships. The observation periods began in 1948 and 1958 respectively. This is probably too short a period to detect any reaction to climatic changes.

Russell et al. (1971) reported an abundance of zooplankton and relatively high phosphate concentrations from 1924 to 1931, followed by a period with low phosphate concentrations and little phytoplankton until 1965. Thereafter, a higher phosphate level occurred, which involved more zooplankton due to a rise of primary production. These changes are assumed to result from an amelioration in the climate in the North Atlantic, which brought about a change in the circulation of the North Sea. As the Atlantic water went farther north, a decrease of pressure from the North Sea water through the English Channel resulted. Cooper (1955) gave a theory which supposed that cold water in the North Atlantic, as a result of cold winters, flows down in the form of great boluses, which generate waves that can cover large distances. When these waves meet continental slopes, strong vertical mixing can occur. Normal vertical mixing, caused by temperature and wind, should bring these water masses to the surface. These processes are effective when a series of cold Arctic winters follow each other. Changes in primary production in the English Channel could be linked to climatic variations.

The reports of Robinson (1970) and Reid (1977) showed results that are far less clear, due possibly to the shorter observation periods. Robinson (1970) showed clearly geographical differences in the seasonal cycle of the phytoplankton, at the time when bloom starts, the amount of algal cells, and the length of the period. The onset of blooms was strongly correlated with the beginning of the stabilizing of the water column in spring. Reid (1977) observed a strong decrease in diatoms, Ceratium and phytoplankton, in general north of 59^° N over the past 10 years. South of this latitude, a decrease of diatoms was also observed, but there was no change in Ceratium, and an increase in phytoplankton, perhaps due to microflagellates which escape detection by continuous plankton recorders. Reid (1977) attributed the observations in the southern North Sea to an amelioration in the climate of the North Atlantic Ocean which occurred since 19701977. Tont (1976) observed a correlation between diatom blooms in the sea near California and upwelling caused by the California current coming from high latitudes with nutrient-rich water. When currents from the west prevailed with warmer water, high salinity, and few nutrients, diatom blooms were significantly reduced. According to Tont (1976), the rate of insolation was not the controlling factor, since diatom blooms occur with low insolation.

Generally, the assumption is justified that a warming-up of the earth's climate will not directly affect primary production in the oceans, but indirectly, by changing the hydrographic circumstances. For example, a longer period of stratification could mean a lower primary production in that part of the oceans (see Chapter 1, this volume). Also, a change in the direction of sea currents and wind belts could affect the upwelling zones near the continents, with consequences on, primary production.

REFERENCES

Anderson, G. C. and Zeutschel, R. P. (1970) Release of dissolved organic matter by marine phytoplankton in coastal and offshore areas of the Northeast Pacific Ocean. Limnol. Oceanogr. 15, 402-407.

Arthur, C. R. and Rigler, F. H. (1967) A possible source of error in the ¹⁴C method of measuring primary productivity. Limnol. Oceanogr. 12, 121-124.

Bazilevich, N. J., Rodin, L. Ye., and Rozov, N. N. (1970) Geographical aspects of biological productivity. In: Papers of the Fifth Congress of the Geographical Society U.S.S.R., Leningrad. Sov. Geogr. Rev. Transl. 12, 293-317 (1971). 

Berman, T. (1973) Modification in filtration methods for the measurement of inorganic ¹⁴C uptake by photosynthetizing algae. J. Phycology 9. 327-330. 

Berman, T. and Holm-Hansen, O. (1974) Release of photoassimilated carbon as dissolved organic matter by marine phytoplankton. Mar. Biol. 28, 305-310. 

Blinks, L. R. (1955) Photosynthesis and productivity of littoral marine algae. J. Mar. Res. 14, 363-373.

Bolin, B. (1970) The carbon cycle. Scient. Amer. 223(3), 124-132.

Bruevich, S. V. and Ivanenkov, V. N. (1971) Problems of the chemical balance of the world ocean. Okeanologiya 11, 835-841.

Brylinski, M. (1977) Release of dissolved organic matter by some marine macrophytes. Mar. Biol. 39, 213-220.

Brylinski, M. and Mann, K. H. (1973) An analysis of factors governing productivity in lakes and reservoirs. Limnol. Oceanogr. 18, 1-14.

Bryson, R. A. (1974) A perspective of climatic change. Science 184, 753-/60. 

Bunt, J. S. (1968) Some characteristics of microalgae isolated from Antarctic sea ice. Antarctic Res. Ser. 11, 1-14.

Bunt, J. (1971) Microbial production in Polar regions. In: Hughes, D. E. and Rose, A. H. (eds.) Microbes and Biological Productivity, 333-354. Cambridge University Press, Cambridge, London, New York, Melbourne.

Bunt, J. S. and Lee, C. C. (1970) Seasonal primary production in Antarctic Sea Ice at McMurdo Sound in 1967. J. Mar. Res. 28, 304-320.

Burris, J. E. (1977) Photosynthesis, photorespiration and dark respiration in eight species of algae. Mar. Biol. 39, 371-379.

Cadée, G. C. and Hegeman, J. (1974a) Primary production of phytoplankton in the Dutch Wadden Sea. Neth. J. Sea Res. 8, 240-259.

Cadée, G. C. and Hegeman, J. (1974b) Primary production of the benthic microflora living on tidal flats in the Dutch Wadden Sea. Neth. J. Sea Res. 8, 260-291.

Chapman, V. J. (1960) Salt Marshes and Salt Deserts of the World, 1-392. Leonard Hill, London, and Interscience, New York.

Chapman, V. J. (1977) Introduction. In: Chapman, V. J. (ed.), Ecosystems of the World. 1. Wet Coastal Ecosystems, 1-30. Elsevier Scientific Publishing Company, Amsterdam, Oxford. New York.

Chapman, G. and Rae, A. C. (1969) Excretion of phytosynthate by a benthic diatom. Mar. Biol. 3, 341-351.

Chave, K. E., Smith, S. V. and Roy, K. J. (1972) Carbonate production by coral reefs. Mar. Geol. 12, 123-140.

Choi, C. L. (1972) Primary production and release of dissolved organic carbon from phytoplankton in the Western North Atlantic Ocean. Deep-Sea Res. 19, 731-735. 

Cooper, L. H. N. (1955) Hypotheses connecting fluctuations in Artic climate with biological productivity of the English Channel. Papers in marine biology and oceanography, suppl. of Deep Sea Res. 3, 212-223.

Degens, E. T. and Mopper, K. (1976) Factors controlling the distribution and early diagenesis of organic material in marine sediments. In: Riley, J. P. and Chester, R. (eds), Chemical Oceanography, 2nd ed., vol. 6, 60-114. Academic Press, London, New York, San Francisco.

Doty, M. S. (1959) Phytoplankton photosynthetic periodicity as a function of latitude. J. Mar. Biol. Ass. India  l, 66-68.

Doty, M. S. and Oguri, M. (1957) Evidence for a photosynthetic daily periodicity. Limnol. Oceanogr. 2, 37-40.

Dyrssen, D. (1972) The changing chemistry of the oceans. Ambio 1, 20-25.

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

Fogg, G. E. (1975a) Biochemical pathways in unicellular plants. In: Cooper, J. P. (ed.), Photosynthesis and Productivity in Different Environments, 437-457. Cambridge University Press, Cambridge, London, New York, Melbourne.

Fogg, G. E. (1975b) Primary productivity. In: Riley, J. P. and Skirrow, G. (eds), Chemical Oceanography, 2nd ed., vol. 2, 385-453. Academic Press, London, New York, San Francisco.

Fogg, G. E. (1977) Comment: excretion of organic matter by phytoplankton. Limnol. Oceanogr. 22(3), 576-577.

Fogg, G. E., Nalewajko, C., and Watt, W. D. (1965) Extracellular products of phytoplankton photosynthesis. Proc. R. Soc. B162, 517-534.

Fogg, G. E. and Watt, W. D. (1965) The kinetics of release of extracellular products of photosynthesis by phytoplankton. Mem. Ist. Ital. Idrobiol. 18 (suppl.), 165-174.

Garrels, R. M. and Perry, Jr., E. A. (1974) Cycling of carbon, sulfur and oxygen through geologic time. In: Goldberg, E. D. (ed.), The Sea, vol. 5, 303-336. J. Wiley and Sons, New York, London, Sydney, Toronto.

Gerletti, M. (1968) Dark bottle measurements in primary production studies. Mem. Ist. Ital. Idrobiol. 23, 197-208.

Gieskes, W. W. C. and Kraay, G. W. (1975) The phytoplankton spring bloom in Dutch coastal waters of the North Sea. Neth. J. Sea Res. 9, 166-196.

Golterman, H. L. (1975) Physiological Limnology. An Approach to the Physiology of Lake Ecosystems. Elsevier Scientific Publishing Company, Amsterdam, Oxford, New York.

Gordon, M. S. and Kelly, H. M. (1962) Primary production of an Hawaiian coral reef: a critique of flow respirometry in turbulent waters. Ecology 43, 473-480.

Hall, C. A. S. and Moll, R. (1975) Methods of assessing aquatic primary production. In: Lieth, H. and Whittaker, R. H. (eds), Primary Production in the Biosphere, 19-55. Springer-Verlag, Berlin, Heidelberg, New York.

Healy, F. P. (1972) Photosynthesis and respiration of some Arctic seaweeds. Phycologia 11, 267-271.

Hellebust, J. A. (1965) Excretion of some organic compounds by marine phytoplankton. Limnol. Oceanogr. 10, 192-206.

Hellebust, J. A. (1974) Extracellular products. In: Stewart, W. D. P. (ed.), Algal Physiology and Biochemistry, 838-863. University of California Press, Berkeley and Los Angeles.

Herbland, A. (1974) Influence de la dépression de filtration sur la mesure simultanée de l'assimilation et de l'excrétion organique de phytoplancton. Cah. ORSTOM, Sér. Océanogr. 12, 173-177.

Horne, A. J., Fogg, G. E., and Eagle, D. J. (1969) Studies in situ of the primary production of an area of inshore Antarctic sea. J. Mar. Biol. Ass. U.K. 49, 393-405.

Ignatiades, L. and Fogg, G. E. (1973) Studies on the factors affecting the release of organic matter by Skeletonema costatum (Greville) Cleve in culture. J. Mar. Biol. Ass. U.K. 53, 937-956.

Jensen, A. and Rystad, B. (1974) Heavy metal tolerance of marine phytoplankton. l. The tolerance of three algal species to zinc in coastal sea water. J. Exp. Mar. Biol. Ecol. 15, 145-157.

Jensen, A., Rystad, B., and Melson, S. (1976) Heavy metal tolerance of marine phytoplankton. 2. Copper tolerance of three species in dialysis and batch cultures, J. Exp. Mar. Biol. Ecol. 22, 249-257.

Kain, J. M. (1971) The biology of Laminaria hyperborea. VI. Some Norwegian populations. J. Mar. Biol. Ass. U.K. 51, 387-408.

Kanwisher, J. W. (1966) Photosynthesis and respiration in some seaweeds. In: Barnes, H. (ed.), Some Contemporary Studies in Marine Science, 407-420. George Allen and Unwin Ltd., London.

Kanwisher, J. W. and Wainwright, S. A. (1967) Oxygen balance in some reef corals. Biol. Bull. Mar. Biol. Lab., Woods Hole 133, 378-390.

Karo, H. A. (1956) World coastline measurements. Int. Hydrogr. Rev. 33, 131-140.

Kiefer, D. and Strickland, J. D. H. (1970) A comparative study of photosynthesis in seawater samples incubated under two types of light attenuator. Limnol. Oceanogr. 15, 408-412.

Kirby, C. J. and Gosselink, J. G. (1976) Primary production in a Louisiana Gulf Coast Spartina alterniflora marsh. Ecology 57, 1052-1059.

Koblentz-Mishke, O. J., Valkovinsky, V. V., and Kabanova, J. G. (1970) Plankton primary production of the world ocean. In: Wooster, W. S. (ed.), Scientific Exploration of the South Pacific. Nat. Acad. Sci., Washington.

Kohn, A. J. and Helfrich, P. (1957) Primary productivity of a Hawaiian coral reef. Limnol. Oceanogr. 2, 241-251.

Lewis, D. H. and Smith, D. C. (1971) The autotrophic nutrition of symbiotic marine coelenterates with special reference to hermatypic corals. l. Movement of phytosynthetic products between the symbionts. Proc. R. Soc. B178, 111-129.

Likens, G. E. (1975) Primary production of inland aquatic ecosystems. In: Lieth, H. and Whittaker, R. H. (eds), Primary Production of the Biosphere, 185-202. Springer-Verlag New York Inc.

Lisitzin, A. P. (1972) Sedimentation in the World Ocean. Soc. Econom. Palaeont. Mineral., Spec. Pub. 17, l-218.

Litter, M. M. (1973) The productivity of Hawaiian Fringing-Reef Crustose corallinaceae and an experimental evaluation of production methodology. Limnol. Oceanogr. 18, 946-952.

Lüning, K. (1969) Standing crop and leaf area index of the sublittoral Laminaria species near Helgoland. Mar. Biol. 3, 282-286.

MacDonald, K. B. (1977) Plant and animal communities of Pacific North American salt marshes. In: Chapman, V. J. (ed.), Ecosystems of the World. 1. Wet Coastal Ecosystems, 167-191. Elsevier Scientific Publishing Company, Amsterdam, Oxford, New York.

MacDonald. K. B. and Bardour, M. G. (1974) Beach and salt marsh vegetation of the North American Pacific Coast. In: Reimold, R. J. and Queen, W. H. (eds), Ecology of Halophytes, 175-233. Academic Press, London, New York, San Francisco.

MacFarlane, C. (1952) A survey of certain seaweeds of commercial importance in Southwest Nova Scotia. Can. J. Bot. 30, 78-97.

McGill, J. T. (1958) Map of the coastal land forms of the world. Geogr. Rev. 48, 402-405.

Mague, T. H. and Holm-Hansen, O. (1975). Nitrogen fixation on a coral reef. Phycologia 14, 87-92.

Mann, K. H. (1972a) Ecological energetics of the sea-weed zone in a marine bay on the Atlantic Coast of Canada. I. Zonation and biomass of seaweeds. Mar. Biol. 12, l-10.

Mann, K. H. (1972b) Ecological energetics of the sea-weed zone in a marine bay on the Atlantic Coast of Canada. II. Productivity of the seaweeds. Mar. Biol. 14, 199-209..

Mann, K. H. (1973) Seaweeds: their productivity and strategy for growth. Science 182, 975-981.

Mann, K. H. and Chapman, A. R. O. (1975) Primary production of marine macrophytes. In: Cooper, J. P. (ed.), Photosynthesis and Productivity in Different Environments, 207-223. Cambridge University Press, Cambridge, London, New York, Melbourne.

Marsh, J. A. (1970) Primary productivity of reef-building calcareous red algae. Ecology 51, 255-263.

Menzel, D. W. (1974) Primary productivity, dissolved and particulate organic matter, and the sites of oxidation of organic matter. In: Goldberg, E. D. (ed.), The Sea, 2nd ed., vol. 5, 659-678. J. Wiley and Sons, New York, London, Sydney, Toronto.

Moebus, K. and Johnson, K. M. (1974) Exudation of dissolved organic carbon by brown algae. Mar. Biol. 26, 117-125.

Moiseev, P. A. (1969) The living resources of the world ocean. Moscow. (Eng. trans: Israel Program of Scientific Translations Ltd., Jerusalem 1971.)

Morris, J., Yentsch, C. M., and Yentsch, C. S. (1971) Relationship between light CO₂ fixation and dark CO₂ fixation by marine algae. Limnol. Oceanogr. 16, 854-858.

Nalewajko, C. and Lean, D. R. S. (1972) Retention of dissolved compounts by membrane filters as an error in the ¹⁴C method of primary production measurement. J. Phycol. 8, 37-43.

Naylor, J. (1976) Production, trade and utilization of seaweeds and seaweed products. FAO, Fish. Techn. Pap. No. 159.

Nienhuis, P. H. and Bree, B. H. H. de (1977) Production and ecology of eelgrass (Zostera marina L.) in the Grevelingen estuary, The Netherlands, before and after the closure. Hydrobiologia 52, 55-66.

Odum, E. P. (1974) Energetics and ecosystems. In: Reimold, R. J. and Queen, W. H. (eds), Ecology of Halophytes, 599-602. Academic Press, London, New York, San Francisco.

Odum, H. T. and Odum, E. P. (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol. Monogr. 25, 291-320.

Overnell, J. (1976) Inhibition of marine algal photosynthesis by heavy metals. Mar. Biol. 38, 335-342.

Parke, M. (1948) Studies on British Laminariaceae. l. Growth in Laminaria saccharina (L.) Lamour. J. Mar. Biol. Ass. U.K. 27, 651-709.

Pearse, J. S. and Gerard, V. A. (1977) Kelp forests. In: Clark, J. (ed.), Coastal Ecosystem and Management 645-649. J. Wiley and Sons, New York, London, Sydney, Toronto.

Penhale, P. A. and Smith, W. O. (1977) Excretion of dissolved organic carbon by eelgrass (Zostera marina) and its epiphytes. Limnol. Oceanogr. 22, 400-408.

Platt, T. and Subba Rao, D. V. (1975) Primary production of marine microphytes. In: Cooper, J, P. (ed.), Photosynthesis and Productivity in Different Environments, 249-280. Cambridge University Press, Cambridge, London, New York, Melbourne.

Porter, J. W. (1976) Autotrophy, heterotrophy and resource partitioning in Caribbean reef-building corals. Am. Nat. 110, 731-742.

Quasim, S. Z. and Sankaranarayanan, V. N. (1970) Production of particulate organic matter by the reef on Kavaratti Atoll (Laccadives). Limnol. Oceanogr. 15, 574-578.

Ranwell, S. D. (1966) World resources of Spartina townsendii (Sensu lato) and economic use of Spartina±marshland. J. App. Ecol. 4, 239-256.

Reid, P. C. (1977) Continuous plankton records: changes in the composition and abundance of the phytoplankton of the Northeastern Atlantic Ocean and North Sea, 1958-1974. Mar. Biol. 40, 337-339.

Reimold, R. J. (1977) Mangals and salt marshes of eastern United States. In: Chapman, V. J. (ed.), Ecosystems of the World. 1. Wet Coastal Ecosystems. Elsevier Scientific Publishing Company, Amsterdam, Oxford, New York, 157-166.

Riley, G. A. (1946) Factors controlling phytoplankton polulation on George's Bank. J. Mar. Res. 6, 54-73.

Robinson, G. A. (1970) Continuous plankton records: variation in the seasonal cycle of phytoplankton in the North Atlantic. Bull. Mar. Ecol. 6, 333-345. 

Russell, F. S., Southward, A. J., Boalch, G. T., and Butler, E. J. (1971) Changes in biological conditions in the English Channel off Plymouth during the last half century. Nature 234, 468-470.

Russell-Hunter, W. D. (1970) Aquatic Productivity, 1-306. Collier-Macmillan Limited, London.

Ryther, J. H. (1956) Photosynthesis in the Ocean as a function of light intensity. Limnol. Oceanogr. 1, 61-70.

Ryther, J. H. (1959) Potential productivity of the sea. Science 130, 602-608. 

Ryther, J. H. (1963) Geographic variations in productivity. In: Hill, M. N. (ed.), The Sea, vol. 2, 347-380. J. Wiley and Sons, New York, London.

Ryther, J. H. (1969) Photosynthesis and fish production in the sea. Science 166, 72-76.

Ryther, J. H., Menzel, D. W., Hulburt, E. M., Lorenzen, C. J., and Couvin, N. (1971) The production and utilization of organic matter in the Peru coastal current. Investigacion pesq. 35, 43-59.

Samuel, S., Shah, N. M., and Fogg, G. E. (1971) Liberation of extracellular products of photosynthesis by tropical phytoplankton. J. Mar. Biol. Ass. UK 51, 793-798.

Sargent, M. C. and Austin, T. S. (1949) Organic productivity of an atoll. Trans. Am. geophys. Un. 30, 245-249.

Sargent, M. C. and Austin, T. S. (1954) Biologic economy of coral reefs. Prof. Pap. U.S. Geol. Surv. 260E, 293-300.

Schindler, D. W. and Holmgren, K. S. (1971) Primary production and phytoplankton in the experimental lakes area, Northwestern Ontario, and other low-carbonate waters, and a liquid-scintillation method for determining ¹⁴C activity in photosynthesis. J. Fish. Res. Bd Can. 28, 189-201.

Schindler, D. W., Schmidt, R. V., and Reid, R. A. (1972) Acidification and bubbling as an alternative to filtration in determining phytoplankton production by the ¹⁴C method. J. Fish. Res. Bd Can. 29, 1627-1731.

Sharp, J. H. (1977) Excretion of organic matter by marine phytoplankton: do healthy cells do it? Limnol. Oceanogr. 22, 381-399.

Sieburth, J. McN. (1969) Studies on algal substances in the sea. III. The production of extracellular organic matter by littoral marine algae. J. Exp. Mar. Biol. Ecol. 3, 290-309.

Smith, S. V. (1973) Carbon dioxide dynamics: a record of organic C production, respiration and calcification in the Eniwetok reef flat community. Limnol. Oceanogr. 18, 106-120.

Smith, S. V. and Marsh, J. A. (1973) Organic carbon production on the windward reef flat of Eniwetok Atoll. Limnol. Oceanogr. 18, 953-961.

Smith, W. O. (1975) The optimal procedures for the measurement of phytoplankton excretion. Mar. Sci. Communications. 1, 395-405.

Smith, W. O., Barber, R. T., and Huntsman, S. A. (1977) Primary production off the coast of northwest Africa: excretion of dissolved organic matter and its heterotrophic uptake. Deep Sea Res. 24, 35-47.

Sorokin, Yu. I. (1973) The primary production of the seas and oceans. General Ecology, Biocenology, Hydrobiology, vol. 1 (Biology series), 3-35. (Eng. trans.: G. K. Hall and Co., Boston, Mass., U.S.A., 1974.)

Sournia, A. (1974) Circadian periodicities in natural populations of marine phytoplankton. Adv. Mar. Biol. 12, 325-389.

Steemann Nielsen, E. (1952) The use of radioactive carbon (¹⁴C) for measuring organic production in the sea. J. Cons. Perm. Int. Explor. Mer 18, 117 -140.

Steemann Nielsen, E. (1953) On organic production in the oceans. J. Cons. Perm. Int. Explor. Mer 19, 309-328.

Steemann Nielsen, E. (1963) Productivity, definition and measurement. 2. Fertility of the oceans. In: Hill, M. N. (ed.), The Sea, vol. 2, 129-164. J. Wiley and Sons, New York, London.

Steemann Nielsen, E. and Hansen, V. K. (1959) Light adaptation in marine phytoplankton polulations and its interrelation with temperature. Physiologia Pl. 12, 353-370.

Stockner, J. G. and Antia, H. J. (1976) Phytoplankton adaptation to environmental stresses from toxicants, nutrients, and pollutants a warning. J. Fish. Res. Bd Can. 33, 2089-2096.

Stoddard, D. R. (1969) Ecology and morphology of recent coral reefs. Biol. Rev. 44, 433-498.

Strickland, J. D. H. (1958) Solar radiation penetrating the ocean. A review of requirements, data and methods of measurements, with particular reference to photosynthetic productivity. J. Biol. Bd Can. 15, 453-493.

Strickland, J. D. H. (1965) Production of organic matter in the primary stages of the marine food chain. In: Riley, J. P. and Skirrow G. (eds), Chemical Oceanography, vol. l, 477-610. Academic Press, New York.

Strickland, J. D. H. (1972) Research on the marine planktonic food web at the institute of marine resources: a review of the past seven years of work. Oceanogr. Mar. Biol. Ann. Rev. 10, 349-414.

Strickland, J. D. H. and Parsons, T. R. (1968). A practical handbook of seawater analysis. Fish. Res. Bd. Canada Bull. 167, l-311.

Sverdrup, H. U. (1955) The place of physical oceanography in oceanographic research. J. Mar. Res. 14, 287-294.

Talling, J. F. (1975) Primary production of freshwater macrophytes. In Cooper, J. P. (ed), Photosynthesis and Productivity in Different Environments, 225-247. Cambridge University Press, Cambridge, London, New York, Melbourne.

Thayer, G. W. and Adams, S. M. (1975) Structural and functional aspects of a recently established Zostera marina community. In: Cronin, L. E. (ed.), Estuarine Research, Vol. 1: Chemistry, Biology and the Estuarine System, 518-540. Academic Press, London, New York, San Francisco.

Thomas, J. P. (1971) Release of dissolved organic matter from natural populations of marine phytoplankton. Mar. Biol. 11, 311-323.

Thomas, W. H. and Dodson, A. N. (1974) Inhibition of diatom photosynthesis by germanic acid. Separation of diatom productivity from total primary productivity. Mar. Biol. 27, 11-19.

Tont, S. A. (1976) Short-period climatic fluctuations: effects on diatom biomass. Science 194, 942-944.

Turner, R. E. (1976) Geographic variations in salt marsh macrophyte production: a review. Contr. Mar. Sci. 20, 47-68.

Venrick, E. L., McGowan, J. A., and Mantyla, A. W. (1973) Deep maxima of photosynthetic chlorophyll in the Pacific Ocean. U.S. Fish. Wildl. Serv., Fish. Bull. 71, 41-52.

Vishniac, W. (1971) Limits of microbial production in the oceans. In: Hughes, D. E. and Rose, A. H. (eds), Microbes and Biological Productivity, 355-366. Cambridge University Press, Cambridge, London, New York, Melbourne.

Wallen, D. G. and Geen, G. H. (1968) Loss of radioactivity during storage of ¹⁴C labelled phytoplankton on membrane filters. J. Fish. Res. Bd Can. 25, 2219-2224.

Walker, F. T. (1954) Distribution of Laminariaceae around Scotland. J. Cons. Perm. Int. Explor. Mer 20, 160-166.

Wanders, J. B. W. (1976) The role of benthic algae in the shallow reef of Curacao (Netherlands Antilles). l. Primary productivity in the coral reef. Aquat. Bot. 2, 235-270.

Ward, F. J. and Nakanishi, M. (1971) A comparison of GeigerMüller and liquidscintillation counting methods in estimating primary productivity. Limnol. Oceanogr. 16, 560-563.

Ward, F. J. and Nakanishi, M. (1973) A comparison of liquid scintillation and GeigerMüller estimates of primary productivity in an in situ experiment. J. Fish. Res. Bd Can. 30, 708-711.

Wetzel, R. G. and Rich, P. H. (1973) Carbon in freshwater systems. In: Woodwell, G. M. and Pecan, E. V. (eds), Carbon and the Biosphere. AEC Symposium Series 30, 241-263, NTIS U.S. Dept. of Commerce, Springfield, Virginia.

Whittaker, R. H. and Likens, G. E. (1973) Carbon in the biota. In: Woodwell, G. M. and Pecan, E. V. (eds), Carbon and the Biosphere. AEC Symposium Series 30, 221-240, NTIS U.S. Dept. of Commerce, Springfield, Virginia.

Wiebe, W. J., Johannes, R. E., and Webb, K. L. (1975) Nitrogen fixation in a coral reef community. Science 188, 257-259.

Williams, P. J. LeB., Berman, T., and Holm-Hansen, O. (1972) Potential sources of error in the measurement of low rates of plankton photosynthesis and excretion. Nature New Biology 236, 91-92.

Wong, G. T. F., Brewer, P. G., and Spencer, D. W. (1976) The distribution of particulate iodine in the Atlantic Ocean. Earth Planet. Sci. Lett. 32, 441-450.

Woodwell, G. M., Rich, P. H., and Hall, C. A. (1973) Carbon in estuaries. In: Woodwell, G. M. and Pecan, E. V. (eds), Carbon and the Biosphere. AEC Symposium Series 30, 221-239, NTIS U.S. Dept. of Commerce, Springfield, Virginia.

Yearbook of Fisheries Statistics 1974; Fishery Commodities. FAO, Rome, 1975.

Yonge, C. M. (1968) Living corals. Proc. R. Soc. B169, 329-344.

Zenkevich, L. (1963) Biology of the Seas of the USSR, 1-955, George Allen and Unwin Ltd., London.

Zieman, J. C. (1975) Quantitative and dynamic aspects of the ecology of turtle grass, Thalassia testudinum. In: Cronin, L. E. (ed.), Estuarine Research, Vol. 1. Chemistry, Biology and the Estuarine System, 541-562. Academic Press, London, New York, San Francisco.

Zobell, C. E. (1971) Drift seaweeds on San Diego County beaches. In: North, W. J. (ed.), The Biology of Giant Kelp Beds in California, 1-273, Verlag J. Cramer.