ENCYCLOPEDIA OF ENVIRONMENTAL SCIENCE AND ENGINEERING - AQUATIC PRIMARY PRODUCTION pdf

113 Primary productivity in aquatic systems, like the same process in terrestrial environments, provides the base of the food web upon which all higher levels of an ecosystem depend. Biological productivity is the increase in organic material per unit of area or volume with time. This addi- tion of organic matter is the material from which the various plant and animal communities of an ecosystem are made, and is dependent on the conversion of inorganic matter into organic matter. Conversion is accomplished by plants through the photosynthetic process. Plants are therefore considered to be the primary producers , and in an aquatic ecosystem these plants include algae, bacteria, and some- times higher plants such as water grasses and water lil- lies. Primary productivity , the first level of productivity in a system, can be measured as the rate of photosynthesis, addition of biomass per unit of time (yield), or indirectly by nutrient loss or a measure of respiration of the aquatic community. METHODS OF STUDY Standing crop refers to the part of biological production per unit area or per unit volume that is physically present as biomass and that is not lost in respiration. Standing crop measurements over a period of time give an indirect mea- sure of productivity in terms of yield. Plankton, microscopic floating plants and animals, can be collected in a plankton net and may be counted under a microscope or weighed. Aquatic biologists have used standing crop measurements to estimate productivity longer than any other method (e.g. Lohman, 1908). This method is still also used for periphyton (attached algae) or rooted plants. Only within the past few decades have biologists pro- gressed from merely counting numbers of organisms to calculating biomass, and more recently, to expressing bio- mass yield. Fishery biologists, like farmers, for many years have measured fish productivity in terms of tons produced per acre of water surface per year. Calculating biomass and biomass yield is an important step forward since changes in standing crop reflect the net effect of many biological and physical events and therefore are not directly proportional to productivity. For example, the standing crop of a phyto- plankton community may be greatly diminished by preda- tion and water movement, while photosynthetic rates of the survivors may remain high. The measurement of plant pigments such as chlorophyll a is also a standing crop measurement that is frequently used and may now be done through remote sensing by aircraft or satellites. UPTAKE OF NUTRIENTS Another early attempt at measuring the rate of production in aquatic ecosystems was to measure the inorganic nutrients taken up in a given system and to calculate the amount of biological production required to absorb this amount. Atkins (1922, 1923) studied the decrease in carbon dioxide and phosphate in measuring production in the North Sea, and Steel (1956), also working in the North Sea, estimated the annual cycle of plant production by considering changes in the inorganic phosphate in relation to vertical mixing of the water mass. Many biologists consider phosphorus to be a difficult element to study in this respect because organisms often store it in excess of their requirements for optimum growth. Measuring nutrient uptake in an indirect method of deter- mining the rate of productivity in an aquatic ecosystem and is influenced by various other biological activities. Nevertheless, it has been important in the development toward more precise measurements of the dynamic aquatic ecosystem. MEASUREMENTS OF OXYGEN AND CARBON DIOXIDE The net rate at which the phytoplankton community of a given ecosystem incorporates carbon dioxide may be esti- mated in moderately to highly productive aquatic environ- ments by direct measurement of the short-term fluctuations in the dissolved oxygen it produces. The calculations are based on the assumption that a mole of oxygen is released into the environment for each mole of carbon dioxide reduced in photosynthesis. This method precludes the necessity of enclosing the phytoplankton in a bottle. If measurements are made at regular hourly intervals over a 24-hour period, the average hourly decrease in oxygen during times of darkness when no photosynthesis is occurring can be determined. It is assumed that respiration removes this amount of oxygen each hour throughout the day thus giving a measure of the gross rate at which the community incorporates carbon dioxide. AQUATIC PRIMARY PRODUCTION © 2006 by Taylor & Francis Group, LLC 114 AQUATIC PRIMARY PRODUCTION An analogous method exists for recording fluctuations in carbon dioxide. The pH meter, which measures acidity, has been suc- cessfully employed to measure these carbon dioxide changes in the aquatic ecosystem since the removal of carbon dioxide from the water for photosynthesis is accompanied by a pro- portional rise in pH. This pH shift has been used to estimate both photosynthesis and respiration. The sea and some fresh waters are too buffered against changes in pH to make this method useful in all environments, but it has been employed with success in lakes and for continuously monitoring the growth of cultures. Carbon dioxide may also be directly measured by standard volumetric or gasometric techniques. Although carbon dioxide and oxygen can be measured with relative precision, the overall precision of productiv- ity measurements made by these techniques is not generally great because of uncertainties in the corrections for diffu- sion, water movements, or extended enclosure time. Some of the oxygen produced by higher aquatic plants may not be immediately released thus causing a lag period in the evolu- tion of oxygen into the environment. The primary advantage this method has over the more sensitive 14 C method is the added benefit of an estimate of community respiration. Some of the uncertainties of the previous method can be reduced by enclosing phytoplankton samples just long enough in glass bottles for measurable changes in the con- centration of oxygen and carbon dioxide to occur, but not long enough for depletion of nutrients or the growth of bac- teria on the inside bottle surface. This method is called the light and dark bottle method. The name is derived from the fact that identical samples are placed in a transparent “light bottle” and an opaque “dark bottle.” Gross and net produc- tivity of the plankton community from which the samples were taken can be estimated by calculating the difference in the oxygen content between the two bottles after a predeter- mined period of incubation and with that present initially. Productivity determinations that are dependent on mea- surements of oxygen are based on some estimated photosyn- thetic quotient (moles O 2 liberated/moles CO 2 incorporated). For the photosynthesis of carbohydrates the ratio is unity. For the synthesis of an algal cell, however, the expected ratio is higher, and presumably varies with the physiological state of the algae and the nutrients available. Oxygen methods in general have rather poor sensitiv- ity and are of no use if the gross incorporation of inorganic carbon during the test period is less than about 20 mg of carbon per cubic meter. Several days may be required in many of the less productive aquatic environments for this much photosynthesis to occur and bacteria may develop on the insides of the container during this time, invalidating the results. Photosynthetic rates can be measured in light and dark bottles also by determining the amount of carbon fixed in particulate form after a short incubation. This can be done by inoculating the bottles with radioactive carbon (Na 2 14 CO 3 ). Sensitivities with this method are much greater than the standard method and much shorter periods of incubation are possible. It is possible to obtain easily measurable amounts of 14 C in particulate form after only two hours by adjusting the specific activity of the inoculums. However, unlike the oxygen method, the dark bottle results do not provide an estimate of community respiration thus giving the ecologist less information with which to work. The 14 C method has been widely used because it is sensi- tive and rapid. One outcome of its popularity is that a great deal of scrutiny has been devoted to the method itself. After 18 years of use, however, it is still not clear whether the 14 C is measuring gross productivity, net productivity, or some- thing in between. The results probably most closely estimate net productivity, but it may be that this method applies only to a particular set of experimental conditions. Already mentioned is the evidence that some of the 14 C that is fixed during incubation may seep out of the algal cells in the form of water-soluble organic compounds. This material is presumably utilized by bacteria rather than passed on directly to the next higher trophic level as is the remainder of the con- sumed primary productivity. The amount of primary production liberated extracellularly is large enough to be measured with precision and a number of workers are now routinely including quantitative studies of extracellular products of photosynthesis as part of the measurements of primary productivity. Calibration of radioactive sources and instruments for measuring radioactivity pose a serious technical problem for the 14 C method. In order to calculate productivity in terms of carbon uptake it is necessary to know accurately the amount of 14 C added in microcuries and the number of microcuries recovered in particulate form by filtering the sample through a membrane filter. Further it has been found that phytoplankton cells may become damaged during filtration and calculations based on these conditions will show lower productivity rates than are actually the case. A point deserving emphasis is that those of us measuring primary productivity are still attempting to determine more precisely what is being measured, and generalizations about the transfer of energy through aquatic food-webs should be made continuously. Neither this nor any other practical tech- nique adequately measures the change in oxidation state of the carbon that is fixed. The subsequent ecological role of newly fixed carbon is even more difficult to measure because of the various ways the photosynthate may be used. USE OF PRIMARY PRODUCTIVITY MEASUREMENTS IN AQUATIC ECOSYSTEMS Lindeman (1942) developed a trophic-dynamic model of an aquatic ecosystem and introduced the concept of “energy flow,” or the efficiency of energy transfer from one trophic level to the next, to describe its operation. A certain value derived from the measured primary productivity represented the input of energy into the next grazing level, and so forth up the food chain. It was consistent with Lindeman’s purpose to express his data as energy units (calories). Subsequent workers have continued to probe the concept of energy flow. However, advances in biochemistry, physiology, and © 2006 by Taylor & Francis Group, LLC AQUATIC PRIMARY PRODUCTION 115 ecology require such a complex model of energy flow that it is difficult to relate it to the natural world. In an imaginary world or model of a system in which the function units are discrete trophic levels, it is not only possible but stimulating to describe the flow of energy through an ecosystem. But when the functional units of the system being investigated are conceived of as macromolecules it is difficult to translate biomass accumulation into energy units. Besides requiring a portion of their autotrophic produc- tion for respiration, phytoplankton communities must also reserve a portion for the maintenance of community struc- ture. In terms of information theory, energy expended for community maintenance is referred to as “ information .” Energy information cost has never been measured directly but there is indirect evidence that it must be paid. For exam- ple, when an aquatic ecosystem is altered artificially with the aim of increasing the production of fish, zooplankton and fish may increase in greater proportion than the phy- toplankton (McConnell, 1965; Goldman, 1968). Perhaps a large amount of primary production remains with the phy- toplankton as information necessary for the maintenance or development of community structure. Grazers then have access only to the production in excess of this threshold level. If the magnitude of the information cost is high rela- tive to primary production, then a small increase in the rate of growth of the primary producers will provide a relatively larger increase in the food supply of grazers and in turn the fish that consume them. There are difficulties that must be met in the course of fitting measurements of primary productivity to the trophic- dynamic model. A highly variable yet often significant portion of primary production, as measured by 14 C light- and-dark bottle experiments, is not retained by the produc- ers but instead moves into the environment in soluble form. It is difficult to measure the absolute magnitude of such excretion by a community of natural plankton because the excreta can rapidly serve as a substrate for bacterial growth and thus find its way back to particulate or inorganic form during the incubation period. Although this excrement is part of the primary productivity and eventually serves as an energy source for organisms at the higher trophic levels, the pathway along which this energy flows does not follow the usual linear sequence modeled for the transfer of energy from phytoplankton to herbivorous zooplankton. There is evidence that the amount of energy involved may some- times be of the same order of magnitude as that recovered in particulate form in routine 14 C productivity studies. The role of allochthonous material (material brought in from outside the system) in supporting the energy require- ments of consumer organisms must also be considered in studies of energy flow. No natural aquatic ecosystem is entirely closed. Potential energy enters in the form of organic solutes and debris. Organic solutes undergo conversion to particulate matter through bacterial action. Sorokin (1965) in Russia found this type of production of particulate matter to be the most important in producing food for crustacean filter- feeders. Particulate and dissolved organic matter may also arise in the aquatic environment through chemosynthesis. This is a form of primary production not usually considered and therefore not usually measured. Although its magnitude may not be great in many systems, Sorokin found it to be very important in the Rybinsk reservoir and in the Black Sea. PRIMARY PRODUCTION AND EUTROPHICATION The process of increasing productivity of a body of water is known as eutrophication and in the idealized succession of lakes, a lake would start as oligotrophic (low productivity), becoming mesotrophic (medium productivity) eventually eutrophic (highly productive) and finally dystrophic, a bog stage in which the lake has almost been filled in by weeds and the productivity has been greatly decreased. The concept of eutrophic and oligotrophic lake types is not a new one. It was used by Naumann (1919) to indicate the difference between the more productive lakes of the cultivated lowlands and the less productive mountain lakes. The trophic state of five dif- ferent aquatic environments will be discussed below. The general progression from an oligotrophic to an eutro- phic and finally to a dystrophic lake (lake succession) is as much a result of the original basin shape, climate, and such edaphic factors as soil, as it is of geologic age. It is unlikely that some shallow lakes ever passed through a stage that could be considered oligotrophic, and it is just as unlikely that the first lake to be considered here, Lake Vanda, will ever become eutrophic. It is also possible that the “progres- sion” may be halted or reversed. Lake Vanda, located in “dry” Wright Valley near McMurdo Sound in Antarctica, is one of the least productive lakes in the world. The lake is permanently sealed under 3 to 4 meters of very clear ice which transmits 14 to 20% of the incident radiation to the water below. This provides enough light to power the photosynthesis of a sparse phytoplankton population to a depth of 60 meters (Goldman et al. , 1967). Lake Vanda can be classified as ultraoligotrophic, since its mean productivity is only about 1 mg C·m Ϫ2 ·hr Ϫ1 . Lake Tahoe in the Sierra Nevada of California and Nevada is an alpine lake long esteemed for its remarkable clarity. Although it is more productive than Lake Vanda, it is still oligotrophic. The lake is characterized by a deep eupho- tic (lighted) zone, with photosynthesis occurring in the phy- toplankton and attached plants to a depth of about 100 m. Although the production under a unit of surface area is not small, the intensity of productivity per unit of volume is extremely low. Lake Tahoe’s low fertility (as inferred from its productivity per unit volume) is the result of a restricted watershed, whose granitic rocks provide a minimum of nutrient salts. This situation is rapidly being altered by human activity in the Tahoe Basin. The cultural eutrophica- tion of the lake is accelerated by sewage disposal in the basin and by the exposure of mineral soils through road build- ing and other construction activities. Since Lake Tahoe’s water is saturated with oxygen all the way down the water column, the decomposition of dead plankton sinking slowly towards the bottom is essentially complete. This means that nutrients are returned to the system and because of a water © 2006 by Taylor & Francis Group, LLC 116 AQUATIC PRIMARY PRODUCTION retention time of over 600 years the increase in fertility will be cumulative. Castle Lake, located at an elevation of 5600 feet in the Klamath Mountains of northern California, shows some of the characteristics of Lake Tahoe as well as those of more productive environments. It, therefore, is best classified as mesotrophic. Although it has a mean productivity of about 70 mg C·m Ϫ2 ·hr Ϫ1 during the growing season, it shows a depletion in oxygen in its deep water during summer stratifi- cation and also under ice cover during late winter. Clear lake is an extremely eutrophic shallow lake with periodic blooms of such bluegreen algae as Aphanizomenon and Microcystis and inorganic turbidity greatly reducing the transparency of the water. The photosynthetic zone is thus limited to the upper four meters with a high intensity of productivity per unit volume yielding an average of about 300 mg C·m Ϫ2 ·hr Ϫ1 during the growing season. Because Clear Lake is shallow, it does not stratify for more than a few hours at a time during the summer, and the phytoplankton which sink below the light zone are continuously returned to it by mixing. Cedar Lake lies near Castle Lake in the Klamath Mountains. Its shallow basin is nearly filled with sediment as it nears the end of its existence as a lake. Numerous scars of similar lakes to be found in the area are prophetic of Cedar Lake’s future. Terrestrial plants are already invading the lake, and higher aquatic plants reach the surface in many places. The photosynthesis beneath a unit of surface area amounts to only about 6.0 mg C·m Ϫ2 ·hr Ϫ1 during the growing season as the lake is now only about four meters in depth and may be considered a dystrophic lake. Some lakes of this type pass to a bog condition before extinction; in others, their shallow basins may go completely dry during summer and their flora and fauna become those of vernal ponds. In examining some aspects of the productivity of these five lakes, the variation in both the intensity of photosyn- thesis and the depth to which it occurs is evident. The great importance of the total available light can scarcely be over- emphasized. This was first made apparent to the author during studies of primary productivity and limiting factors in three oligotrophic lakes of the Alaskan Peninsula, where weather conditions imposed severe light limitations on the phytoplankton productivity. The average photosynthesis on both a cloudy and a bright day was within 10% of being proportional to the available light energy. Nutrient limiting factors have been reviewed by Lund (1965) and examined by the author in a number of lakes. In Brooks Lake, Alaska a sequence of the most limiting factors ranged from magnesium in the spring through nitrogen in the summer to phosphorous in the fall (Goldman, 1960). In Castle Lake potassium, sulfur, and the trace element molybdenum were found to be the most limiting. In Lake Tahoe iron and nitrogen gave greatest photosynthetic response with nitrogen of particular importance. Trace elements, either singly or in combination, have been found to stimulate photosynthesis in quite a variety of lakes. In general, some component of the phytoplankton population will respond positively to almost any nutrient addition, but the community as a whole will tend to share some common deficiencies. Justus von Liebig did not intend to apply his law of the minimum as rigidly as some have interpreted it, and we can best envision nutrient limitation from the standpoint of the balance and interac- tions of the whole nutrient medium with the community of organisms present at any given time. Much about the nutri- ent requirements of phytoplankton can be gleaned from the excellent treatise of Hutchinson (1967). It must be borne in mind that the primary productivity of a given lake may vary greatly from place to place, and measurements made at any one location may not provide a very good estimate for the lake as a whole. Variability in productivity beneath a unit of surface area is particularly evident in Lake Tahoe, where attached algae are already becoming a nuisance in the shallow water and trans- parency is often markedly reduced near streams which drain disturbed watersheds. In July, 1962, the productivity of Lake Tahoe showed great increase near areas of high nutrient inflow (Goldman and Carter, 1965). This condition was even more evident in the summer of 1967 when Crystal Bay at the north end of the lake and the southern end of the lake showed differ- ent periods of high productivity. This variability in productivity may be influenced by sewage discharge and land disturbance. Were it not for the great volume of the lake (155 km 3 ), it would already be showing more severe signs of eutrophication. In the foregoing paper I have attempted to sketch my impressions of aquatic primary productivity treating the sub- ject both as a research task and as a body of information to be interpreted. I believe that biological productivity can no longer be considered a matter of simple academic interest, but of unquestioned importance for survival. The productivity and harvest of most of the world’s terrestrial and aquatic environ- ments must be increased if the world population is to have any real hope of having enough to eat. This increase is not possible unless we gain a much better understanding of both aquatic and terrestrial productivity. Only with a more sound understanding of the processes which control productivity at the level of the primary producers can we have any real hope of understanding the intricate pathways that energy moves and biomass accumu- lates in various links of the food chain. With this information in hand the productivity of aquatic environments can be increased or decreased for the benefit of mankind. REFERENCES Atkins, W. R. G. (1922), Hydrogen ion concentration of sea water in its biological relation, J. Mar. Biol. Assoc. UK , 12, 717–771. Atkins, W. R. G. (1923), Phosphate content of waters in relationship to growth of algal plankton, J. Mar. Biol. Assoc. UK , 13, 119–150. Fernando, C. H. (1984), Reservoirs and lakes of Southeast Asia, in Lakes and Reservoirs , F. B. Taub, Ed., Elsevier, Amsterdam. Goldman, C. R. (1960), Primary productivity and limiting factors in three lakes of the Alaska Peninsula, Ecol. Monogr. , 30, 207–230. Goldman, C. R. (1968), Absolute activity of 14 C for eliminating serious errors in the measurement of primary productivity, J. du Conseil , 32, 172–179. Goldman, C. R. and R. C. Carter (1965), An investigation by rapid carbon-14 bioassay of factors affecting the cultural eutrophication of Lake Tahoe, California–Nevada, J. Water Pollution Control Fed. , 37, 1044–1059. Goldman, C. R., D. T. Mason and J. E. Hobbie (1967), Two Antarctic desert lakes, Limnol. Oceanogr. , 12, 295–310. © 2006 by Taylor & Francis Group, LLC AQUATIC PRIMARY PRODUCTION 117 Guerrero, R. D. (1983), Talapia farming the Philipines; Practices, problems and prospects. Presented at PCARRD-ICLARM Workshop, Los Baños, Philipines. Hutchinson, G. E. (1967), A Treatise on Limnology , Vol. II. Introduction to lake biology and the limnoplankton, John Wiley and Sons, New York. Junghran, V. G. (1983), Fish and fisheries of India, Hindustan Pub. Co. Kuo, C M. (1984), The development of tilapa culture in Taiwan, ICLARM Newsletter, 5(1). Lindeman, R. L. (1942), The trophic-dynamic aspect of ecology, Ecology , 23, 399–418. Lohman, H. (1908), Untersuchungen zur Feststellung des vollständigen Gehaltes des Meeres an Plankton, Wiss. Meeresunters, NF Abt. Kiel , 10, 131–370. Lund, J. W. G. (1965), The ecology of the freshwater phytoplankton, Biol. Rev. , 40, 231–293. McConnell, W. J. (1965), Relationship of herbivore growth to rate of gross photosynthesis in microcosms, Limnol. Oceanogr. , 10, 539–543. Naumann, E. (1919), Några synpunkter angående planktons ökologi, Med särskild hänsyn till fytoplankton. Svensk bot. Tidskr. , 13, 129–158. Petr, J. and J. M. Kapetsky (1990), Tropical reservoir fisheries, Resource Management and Optimization , 7, 3. Sorokin, Y. A. (1965), On the trophic role of chemosynthesis and bacte- rial biosynthesis in water bodies, pp. 187–205. In C. R. Goldman (ed.), Primary productivity in aquatic environments , University of California Press, Berkeley. Steele, J. H. (1956), Plant production on the Falden Ground. J. Mar. Biol. Ass. UK , 35, 1–33. CHARLES R. GOLDMAN University of California, Davis ATMOSPHERIC: see also AIR—various titles © 2006 by Taylor & Francis Group, LLC . reservoir and in the Black Sea. PRIMARY PRODUCTION AND EUTROPHICATION The process of increasing productivity of a body of water is known as eutrophication and in the idealized succession of lakes,. is the remainder of the con- sumed primary productivity. The amount of primary production liberated extracellularly is large enough to be measured with precision and a number of workers are now. production in excess of this threshold level. If the magnitude of the information cost is high rela- tive to primary production, then a small increase in the rate of growth of the primary producers