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.. Plant
Trang 1Primary 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
Trang 2An 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
Trang 3ecology 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 respiraproduc-tion, 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 dystroeutro-phic 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·m2·hr1
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
Trang 4retention 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·m2·hr1 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·m2·hr1 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·m2·hr1 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 requiremnutri-ents 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
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CHARLES R GOLDMAN
University of California, Davis
ATMOSPHERIC: see also AIR—various titles