SCOPE 13 - The Global Carbon Cycle
10
|
Primary Production in Aquatic Environments
|
|
C. G. N. DE VOOYS |
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.) | |
|
|
|
|
|
|
|
|
|
115178 | |
|
|
|
|
143226 | |
|
|
|
|
|
|
|
|
|
|
|
|
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 |
|
|
|
|
|
|
|
260430 | |
|
|
|
The Netherlands, North Sea coastal water | |
|
160180 | |
|
|
|
|
|
|
|
|
|
|
|
|
|
The Netherlands, Wadden Sea | |
|
100120 | |
|
|
|
State of Washington, Columbia River, north | |
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
State of New York, Long Island Sound | |
|
|
|
|
|
|
|
|
|
shallow water off New York | |
|
|
|
|
|
|
|
|
|
|
|
|
|
|
State of North Carolina, coastal water | |
|
|
|
|
State of Georgia, coastal water | |
|
|
|
|
State of Mississippi, coastal water | |
|
|
|
|
State of Louisiana, Barataria Bay | |
|
|
|
|
|
|
|
|
|
Table 10.3 Productivity of intertidal or submerged
marine angiosperms
|
|
|
|
|
|
|
|
|
|
|
|
|
Spartina townsendii (sensulato) | |
|
|
|
Spartina alterniflora Loisel | |
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
4.5-540 |
Thayer and Adams (1975) |
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
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
|
|
|
Primary production in 1015 g C
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
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
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
l. Production of whole reef communities | |
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
(10° N 72° E) |
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|