Download chapter 1 - School of Ocean and Earth Science and Technology

yes no Was this document useful for you?
   Thank you for your participation!

* Your assessment is very important for improving the work of artificial intelligence, which forms the content of this project

Document related concepts

Marine pollution wikipedia, lookup

Marine debris wikipedia, lookup

Ecosystem of the North Pacific Subtropical Gyre wikipedia, lookup

Sustainable fishery wikipedia, lookup

For it is a universal law that the sea and its use is common to all . . . For everyone admits that if a
great many persons hunt on the land or fish in a river the forest is easily exhausted of wild
animals and the river of fish, but such a contingency is impossible in the case of the sea.
Hugo Grotius
Mare Liberum
Men have been catching fish from the lakes, rivers, and oceans of the world for millennia.
Until fairly recently there was a consensus that the fish resources of the oceans were
inexhaustible (Grotius, 1609), but that impression has changed in recent years. Perhaps the first
clear indication of the finite size of the resource was the decimation of certain species of whales
in the North Atlantic by the whaling industry in the 17th and 18th centuries. The subsequent
decline of the great whale populations in all the ocean basins has been accompanied by even
more precipitous collapses of other important fisheries such as the Norwegian herring, Japanese
sardine, Peruvian anchovy, and Canadian North Atlantic cod. The ability of mankind to overfish
these enormous resources reflects major improvements in fishing vessels, the ability of the
fishermen to locate the fish, and the methods used to catch the fish. There is a clear realization
now that our ability to harvest the fish of the sea vastly exceeds in many cases the ability of the
resource to renew itself. This realization has been instrumental in determining some of the most
important provisos of the 1982 United Nations Convention on the Law of the Sea (UNCLOS).
For example, the establishment of 200-mile exclusive economic zones (EEZ’s) within which
coastal states have sovereign rights over the exploitation of living and nonliving resources
directly reflects the realization that the major fishing nations of the world have the ability to
decimate almost all coastal fish populations within a few years’ time and that unless control over
the management of these fisheries clearly resides within a single nation, the tragedy of the
commons (Hardin, 1968) may well result. The tragedy of the commons is the fate of any
resource held in common ownership, when the collective ability of the owners to consume the
resource exceeds the capacity of the resource to renew itself. Each owner then perceives that his
own interests are best served by consuming as much of the resource as possible before it
disappears. Under such conditions the resource will surely vanish unless the owners agree
among themselves to constrain their use of the resource or control over the resource is
transferred to a single authority. The creation of EEZ’s amounts to adopting the latter strategy.
There is now general agreement that mankind should be managing the oceans’ renewable
resources so as to maximize the long-term benefit derived from their use. However, before
considering the issue of management, we should ask ourselves why we care, what benefits we
expect to derive from harvesting the fish in the sea, and what has been and will be the cost of
mismanagement. With respect to these questions it is appropriate to examine the present catch
and to try to understand the causes and consequences of the historical trends and fluctuations in
the catch statistics. Finally it is appropriate to ask in what way and by how much the catch might
be increased in future years.
Why do we care?
Present Catch
The total world catch of all aquatic organisms amounts to about 133 million tones per
year (Mt y-1) and has been increasing at a rate of about 2 Mt y-1 for the last 50 years (Fig. 1.1).
However, virtually all of the increase in the recent years has been due to aquaculture production,
which grew from 15 to 40 Mt y-1 between 1992 and 2002 (Fig. 1.2). Capture fisheries (as
opposed to aquaculture) currently account for about 93 Mt y-1, and of that total about 70 Mt y-1 is
contributed by marine finfish. Much of the remainder of the capture fishery is divided between
freshwater species (6.8 Mt y-1) and marine crustaceans and mollusks (12.6 Mt y-1). The
economic value of the catch is estimated to be $132 billion, with capture fisheries accounting for
$78.3 billion and aquaculture the remainder.
The disposition of the catch is summarized in Table 1.1. About 76% of the catch is
presently being used for human consumption. This percentage has been very slowly increasing
from a low of about 65% during the period 1967-1971, when the Peruvian anchovy catch
averaged more than 11 Mt and accounted for about 17% of the world fish catch. Virtually all of
Figure 1.1 Global annual fish catch from capture fisheries and aquaculture combined.
the Peruvian anchovy catch has been used for reduction purposes. Reduction refers to the
production of fish meal and oil. The fish meal is used primarily as a component of feed for
livestock, notably chickens, pigs, and more recently, freshwater fish such as trout. In most
countries fish oil is hydrogenated to form a solid compound and incorporated in this form into
products such as margarine and shortening. Fish marketed for reduction purposes are worth far
less than fish sold for human consumption. Although reduction accounts for 19% of the world
fish catch by weight, it contributes only 2% of the economic value of the catch.
A major issue in the disposition of the fish catch is its real and potential
contribution to human nutrition. Direct consumption of fish accounts for about 1% of human
calorie consumption and about 4.4% of protein consumption (Holt and Vanderbilt, 1980). These
figures increase a bit when one takes into account indirect pathways such as the consumption of
chickens or pigs that have been fed a ration containing fish meal. When such indirect pathways
Figure 1.2 Trends in capture fisheries and aquaculture production since 1992. Source:
Table 1.1 Disposition of the total aquatic catch for 2002
% of total catch by weight
Human consumption
are considered, fish and seafood are found to contribute about 3% of human calorie consumption
and 5-6% of protein consumption.
These figures are not very impressive. In fact, animals, both terrestrial and aquatic,
account for only about 18% of human caloric intake and 35% of human protein consumption
(Holt and Vanderbilt, 1980). Thus most of mankind’s supplies of calories and protein are
derived from plants, and these are largely of terrestrial origin. Given the fact that the oceans
cover about 71% of the surface of the Earth, a question naturally arises as to whether seafood
could not make a substantially greater contribution to human nutrition.
Before addressing this question, it is appropriate to review some important facts about
human nutrition. First, it is noteworthy that, “Food production on a global scale would meet the
requirements for the present population if it were distributed equitably” (Holt and Vanderbilt,
1980, p. 26). On a global average the daily per capita requirements for calories and protein are
about 2.4 kcal and 30 g protein, respectively. Actual consumption rates average 2.6 kcal and 70
g protein. Thus if calories and protein were equitably distributed, there would be about 10-15%
more calories and more than twice as much protein as the daily requirements of the human
population. The problem is that the food supply is not equitably distributed. The supply of
calories in Asia and Africa is 5-10% below the minimum per capita requirements for those
regions. However, a more meaningful statistic than the average caloric intake for a region is the
percentage of persons whose diets are calorie deficient. Some relevant data are shown in Table
1.2. In Latin America, for example, the average caloric intake exceeds the minimum
requirement by 4%, but the diets of over half the population are calorie deficient. It is apparent
from Table 1.2 that when the average caloric intake for a region drops more than a few
percentage points below the minimum requirement, one can anticipate that the great majority of
the population is undernourished. According to Reutlinger and Selowsky (1976) almost a billion
persons in developing countries with market economies have diets that provide less than 90% of
their daily calorie requirements.
Table 1.2 Percentage of persons whose diets are calorie deficient and average caloric supplies as
a percent of minimum requirements.
% of population with calorie-deficient
Average caloric supplies as %
of minimum requirement
Asia and Far East
Middle East
Latin America
Source: Holt and Vanderbilt (1980)
Average protein supplies are more than 60% above minimum requirements in even the
most undernourished regions of the world, and on the basis of this fact one might surmise that
protein deficiency is not a serious problem. Unfortunately this conclusion is false for several
reasons. When a diet is deficient in calories, the body will catabolize protein in order to make up
for the deficiency in calories. As a result the incidence of diseases such as marasmus and
kwashiorkor, which are associated with protein deficiency, is highly correlated with the degree
of caloric deficiency in the diet of persons in a region, even though almost all persons receive a
diet that is nominally protein sufficient. The conclusion is that protein deficiency is largely the
indirect result of caloric deficiencies. In fact, “It has been affirmed that a diet in which 5 percent
of the calories come from good-quality protein would practically always satisfy the individual’s
protein needs, whether he be a young child or an adult, provided that his total energy intake
meets requirements” (Holt and Vanderbilt, 1980, p. 22).
The words “good-quality protein” in the previous sentence are an important issue in the
context of fish consumption. Proteins are assembled from amino acids, nine of which are
essential in the diet of humans. For the body to make efficient use of proteins, the amino acid
composition of the protein in the food one eats must be similar to the average amino acid
composition of the protein in one’s body. For many foodstuffs, this condition is not satisfied.
Table 1.3 lists a variety of plant and animal protein sources and the approximate protein
utilization efficiency resulting from the imperfect match between the amino acid composition of
the foodstuff and the requirements of the human body. The amino acids in the foodstuffs that are
primarily responsible for limiting the protein utilization efficiency are noted in the table.
Table 1.3 Utilization efficiencies of protein from various food stuffs. Source: FAO (1970)
Efficiency (%)
Amino acids that limit utilization efficiency1
cow’s milk
cottage cheese
swiss cheese
trp, lys, met, cys
trp, lys
green peas
trp, lys
met, cys
met, cys
met, cys
met, cys
lys, met, cys
met, cys
brown rice
wheat germ
wheat grain
polished rice
trp, thr
lys, thr
lys, met, cys
lima beans
kidney beans
met, cys, val
met, cys
trp, met, cys
trp, met, cys
lys, trp
trp, lys
sunflower seeds
sesame seeds
lys, met, cys, thr
trp, met, cys
trp, lys
cereals and grains
trp, met, cys
Nuts and seeds
The essential amino acids are cysteine (cys), isoleucine (ile), leucine (leu), lysine (lys), methionine (met),
phenylalanine (phe), threonine (thr), tryptophan (trp), and valine (val)
It is apparent from an examination of this table that eggs are the best source of protein
from the standpoint of protein utilization efficiency. However, eggs also have a high cholesterol
content. Cow’s milk and fish are second to eggs as a source of protein, each with a protein
utilization efficiency of about 82-83%. The protein utilization efficiencies of the remaining
foodstuffs are at least ten percentage points lower. Vegetables, grains and cereals, legumes, and
nuts and seeds are in general poorer sources of protein than meat and dairy products because
protein from the former foodstuffs is often deficient in lysine and the sulfur-containing amino
acids cysteine and methionine. This point is particularly noteworthy, because in developing
countries animal protein accounts for only about 20% of total protein consumption. The
corresponding figure in developed countries is 55-60% (Holt and Vanderbilt, 1980). The
implication is that persons in developing countries must consume more total protein than person
in developed countries to avoid health problems associated with protein deficiency. This
realization combined with the fact that per capita caloric intake in Africa, for example, averages
10% below the minimum requirement makes it clear why diseases associates with protein
deficiency are common in that part of the world. An improvement in the quality of protein
available to persons in developing countries would undoubtedly help to alleviate protein
deficiency problems. Incorporation of more fish and/or fish products into the diet could
obviously serve that purpose.
An additional issue related to the consumption of fish is the composition of the
polyunsaturated fatty acids (PFA’s) in fish fat and oils. It is now generally recognized that a
proper balance of so-called -3 and -6 PFA’s is needed for good health. Here the designations
-3 and -6 refer to the fact that the last double bond occurs three cabon atoms and six carbon
atoms, respectively, from the end of the carbon chain in the PFA. An improper balance of -3
and -6 PFA’s in the diet can lead to the overproduction of hormone-like compounds called
eicosanoids, and this condition can in turn lead to the development of atherosclerosis (thickening
of blood vessel walls due to deposition of fat and cholesterol), heart attacks, and possibly other
health problems (Lands, 1986). Many commonly used fats and oils contain little or no -3
PFA’s. the only large scale sources of -3 PFA’s are linseed, soybean, rapeseed, and fish oil.
Fish oil and linseed oil contain by far the highest amounts of -3 PFA’s relative to -6 PFA’s
(Table 1.4). The -3 PFA in linseed oil is primarily linolenate acid, an 18-carbon PFA. In fish
oil the PFA’s are primarily 20- and 22-carbon fatty acids, the former consisting primarily of
Table 1.4 World production of fats and oils and the -3 and -6 PFA content of those oils.
Weight percent of total lipids
Production (Mt y-1)
Rape seeds
Source of oil
Source: Applewhite (1980) and Young (1982)
eicosapentaenoic acid (EPA). In recent years a substantial increase in the consumption of fish
and health food products containing fish oil has occurred in the United States, in part because of
public awareness of the need for a better balance of -3 and -6 PFA’s in the diet.
A case can therefore be made that many persons would benefit nutritionally if a higher
percentage of their food consisted of fish. In the case of developing countries partial substitution
of fish protein for protein obtained from vegetables, grains, and cereals would undoubtedly
increase protein utilization efficiency and hence reduce the incidence of diseases such as
marasmus and kwashiorkor. In developed countries partial substitution of fish for other meats
could greatly improve the ratio of -3 to -6 PFA’s in th diet and hence reduce the incidence of
atherosclerosis and heart attacks. Unfortunately most assessments of the potential fish resources
of the oceans indicate that a significant increase in the consumption of fish by the human
population is unlikely to occur. This conclusion is based on both empirical observations and
theoretical calculations.
What Limits Production?
Empirically there is no question that many once important commercial fisheries have
collapsed as a result of intensive fishing pressure. Although many such collapses have been
phenomena of the 20th century and reflect the use of highly sophisticated modern techniques for
location and catching fish, the record of collapsed fish populations goes back to the 17th and 18th
centuries when some North Atlantic whale populations were reduced almost to extinction by a
whaling fleet using techniques far less sophisticated than those employed to hunt, capture, and
process whales during the first half of the 20th century. The collapse of certain whale
populations during the early years of the North Atlantic whaling industry was one of the first
indications that Hugo Grotius’ (1609) characterization of the fish resources of the seas as without
bound was overly optimistic. Within the last 100 years numerous fish populations such as the
California sardine and Peruvian anchovy have collapsed while subjected to an intense and
selective fishery. Chapter 5 includes a documentation of the collapse of certain of these fish
populations. While some of these declines can be blamed in part on the vagaries of currents and
climate, there is no doubt that overfishing has been a major factor in virtually every case. The
overall picture that develops from an examination of these cases is that many conventional
fishing grounds cannot sustain much additional fishing effort and indeed may be overexploited at
the present time. The implication is that the yield of fish from the sea cannot significantly
increase unless the fishing nations of the world begin to (1) make more efficient use of the catch
and/or (2) exploit nonconventional stocks and/or underutilized fishing grounds.
Theoretical calculations provide one means by which the potential yield of both
conventional and nonconventional fish stocks can be assessed. The procedure is to estimate the
amount of organic mater produced by plants in the ocean and to follow that production up the
food chain to commercially useful fish. Since much of the food consumed by a predator may be
respired, excreted, or in some cases shed as molts or lost in the process of reproduction, the
efficiency with which organic matter is transferred from one trophic level to the next in n aquatic
food chain is generally assumed to be rather low. The estimates of potential fish yields from
such food chain models are therefore highly sensitive to the assumed transfer efficiencies and to
the number of trophic levels between plants and commercially useful fish.
Theoretical estimates of potential commercial fish catch date back to the 1960’s
[(Chapman, 1965; Graham and Edwards, 1962; Kasahara, 1966; Ryther, 1969; Schaefer, 1965;
Schmitt, 1965)]. Our understanding of marine food chains has undergone some important
revisions since that time, and it is therefore appropriate to update those earlier models based on
the most recent information.
We begin by dividing the oceans into three distinct areas: open ocean, coastal areas, and
upwelling areas. In the open ocean photosynthetic rates are limited by lack of light over 97-98%
of the water column. Light sufficient to support photosynthesis rarely penetrates to a depth
greater than 150 m, even in the clearest ocean water. As a rule of thumb the compensation
depth1 occurs where the visible light intensity is about 0.05 mole quanta m-2 d-1 (Bienfang and
Gundersen, 1977; Geider, et al., 1986; Laws, et al., 1989). This figure translates into about 0.1%
of the visible light incident on the surface of the ocean at the equator on a clear day (Kimball,
1928). The compensation depth is typically 100-150 meters at tropical latitudes in the open
ocean but is virtually zero at high latitudes during the winter months (Parsons, et al., 1966).
The portion of the water column above the compensation depth is traditionally referred to
as the euphotic zone. In the open ocean photosynthetic rates within the euphotic zone are
frequently limited by lack of nutrients. The reason for this limitation is illustrated in Fig. 1.3.
Essential nutrients such as nitrogen, phosphorus, and iron are assimilated by microscopic plants
called phytoplankton and incorporated into organic matter. The phytoplankton are grazed by
herbivores, which in turn are eaten by primary carnivores, and so forth up the food chain. At
each step in the food chain a large percentage of the organic matter is either respired to provide
energy or excreted as waste material. Nutrients that are released as the result of respiration are
available in dissolved inorganic form and may be directly assimilated by phytoplankton or
bacteria. Hence such recycled nutrients tend to remain within the euphotic zone. Nutrients that
are excreted while still bound to organic matter may be released in either dissolved or particulate
Depth where the net photosynthetic rate equals zero
Sea surface
death, and
and turbulent
Permanent pycnocline
Nutrients in
Figure 1.3 Nutrient and organic matter cycling in the upper water column of the open ocean.
Dashed lines represent recycling of dissolved nutrients via excretion and respiration. Sinking of
detritus removes nutrients from the surface waters. This loss is approximately balanced by
upward movement of nutrients via processes such as upwelling and turbulent diffusion.
form. Dissolved organic nutrients (DON) obviously do not sink and hence like the dissolved
inorganic nutrients (DIN) tend to remain within the euphotic zone. However, nutrients that are
excreted in particles will tend to sink. Once these particles have sunk below the depth of winter
mixing, there is no effective mechanism for returning them. Such nutrients may remain in the
dark portion of the water column2 for periods of time on the order of years to centuries or may
even become buried in the sediments at the bottom of the ocean.
The tendency of photosynthetic rates in the euphotic zone of the open ocean to be limite
by the supply of nutrients therefore reflects the tendency of particulate organic nutrients (PON)
to sink below the depth of winter mixing. Studies of photosynthetic rates and nutrient cycling
aphotic zone
within the euphotic zone of the open ocean suggest that 80% or more of primary production in
the open ocean is supported by nutrient recycling within the euphotic zone (Laws, et al., 2000).
The implication is that much of the PON produced by phytoplankton is in fact recycled within
the mixed layer as DIN or DON. However, the minor fraction of the PON that sinks below the
permanent pycnocline is not trivial, and this loss ultimately limits the photosynthetic rates that
can be sustained in the euphotic zone. Indeed, if there were no mechanism for offsetting this
loss, photosynthetic rates in the open ocean would eventually drop to zero.
Over the continental shelves, where the water column is usually less than 180 meters
deep (Gross, 1982), PON that sinks below the euphotic zone is likely to be returned as DON or
DON much more efficiently than is the case in the open ocean. The reason is that the winter
mixed layer depth can easily extend to 180 meters in temperate and polar latitudes. Hence unlike
the open ocean nutrients do not remain in the aphotic zone for hundreds of years, but are returned
to the euphotic zone on an annual basis, and over shallower portions of the continental shelf even
more frequently. The result is that the biomass and production of phytoplankton over the
continental shelves are much higher than in the open ocean, and only about 50% of the annual
primary production is supported by recycling of nutrients within the euphotic zone (Eppley and
Peterson, 1979).
Phytoplankton biomass and photosynthetic rates are also much higher in upwelling areas
than in the open ocean, but the physical mechanisms responsible for the high productivity of
continental shelves and upwelling areas are quite different. In upwelling areas water is advected
from below the nutricline toward the surface at rates as high as 1-3 meters per day. The
upwelled water does not come from great depths, but rather from depths of approximately 50100 meters. To be effective in stimulating production, upwelling must obviously occur at
locations where the top of the nutricline is shallower than 50-100 meters. The latitudinal
variation of the Coriolis force causes current gyres to be displaced toward the west, and the
resultant displacement of surface water causes the pycnocline as well as the nutricline to be
deeper on the western side of ocean basins. This behavior is illustrated dramatically in Figs. 1.41.5, which show the distribution of temperature and phosphate concentration across the Pacific
Ocean at approximately 27oN latitude from Mexico to 144oE longitude and then northwest across
the Kuroshio Current to Japan. The tilting of the isotherms and phosphate contours across the
ocean basin is obvious in these figures. The shoaling of both the isotherms and phosphate
Figure 1.4. Temperature isotherms along a transect from Baja, California, along approximately
27oN to 144oE and then north northeast across the Kuroshio Current to Tokyo. Redrawn from
Reid (1965)
Figure 1.5. Inorganic phosphate concentrations (M) along a transect from Baja, California,
along approximately 27oN to 144oE and then north northeast across the Kuroshio Current to
Tokyo. Redrawn from Reid (1965)
contours in the Kuroshio is a characteristic of western boundary currents. However, despite this
localized western boundary current effect, high nutrient concentrations are consistently found at
shallower depths along the eastern side of the ocean basin. For example, in Fig. 1.4 phosphate
concentrations of 2 micromolar (M) appear a depth of about 80 meters off the coast of Mexico
but are found only at depths exceeding 300-500 meters off the coast of Japan. The result of this
longitudinal asymmetry in nutrient concentrations across the ocean basins is that almost all
biologically significant upwelling areas are found in the eastern half of the ocean basins.
There are basically two types of upwelling systems, open-ocean and coastal. The most
important open-ocean upwelling occurs near the equator and is apparent in both the Atlantic and
Pacific Oceans. Figure 1.6 illustrates the processes responsible for the upwelling. Between
roughly 25oS and 5oN latitude the Southeast Trade Winds push the South Equatorial Current
from east to west. Ekman transport (i.e., Coriolis forces) diverts some of this water northward in
the northern hemisphere and southward in the southern hemisphere. The result is a depression of
the sea surface and shoaling of the thermocline at the equator (Fig. 1.6). The resultant upwelling
stimulates primary production near the equator in both the eastern Atlantic and Pacific Oceans.
There is also an upwelling associated with the Antarctic Divergence at about 65oS latitude where
Ekman transport moves surface water in the eastward flowing Antarctic Circumpolar Current
and westward flowing East Wind Drift to the north and south, respectively. However, the impact
of this upwelling on productivity in the Southern Ocean is much less significant than the effect of
equatorial upwelling on productivity in the tropics. Finally, there is a divergence of surface
water and upwelling near 10oN due to the tendency of Ekman transport to move surface water in
the eastward flowing Equatorial Countercurrent and westward flowing North Equatorial Current
to the south and north, respectively. However, the impact of the upwelling on production is less
at 10oN than at the equator because the upwelled water has a lower nutrient concentration at
10oN (Wyrtki and Kilonsky, 1984).
Coastal upwelling is associated with some of the most productive fisheries in the world
and is caused by a combination of both favorable current and wind regimes. The major coastal
upwelling areas of the world are shown in Figs. 1.7-1.8. In the northern hemisphere the
Northeast Trade Winds blow steadily between about 10o and 40oN latitude. Associated with
these winds are the eastern boundary currents off the coasts of North America and Africa, the
California Current and Canary Current, respectively. In the southern hemisphere the Southeast
Figure 1.6. Oceanographic conditions in the central equatorial Pacific between 150 and 160oW,
showing winds, surface currents, dynamic height, thermal structure, and meridional circulation.
SEC, ECC, and NEC refer to South Equatorial Current, Equatorial Countercurrent, and North
Equatorial Current, respectively. Redrawn from Wyrtki and Kilonsky (1984).
Figure 1.7 Surface winds systems (arrows) and major coastal upwelling areas (hatched) in the
northern hemisphere during the winter. Source: K. Wyrtki (pers. comm.)
Trade Winds are associated with similar coastal current systems, the Peru Current off the coast of
South America and the Benguela Current off the coast of southern Africa. A combination of
Coriolis forces and sometimes offshore winds tend to drive the surface water in these currents
toward the west, as indicated in Fig. 1.9. As this surface water is advected offshore, it is
replaced by water from depths of about 50-100 meters. This upwelling has a major impact on
primary production along these coastlines because the upwelled water is rich in nutrients.
The upwelling systems off the west coasts of the Americas and Africa stimulate
production more-or-less throughout the year, but two upwelling systems in the Indian Ocean are
strictly seasonal. During summer in the northern hemisphere the Southeast Trade Winds and
South Equatorial Current are fully developed in the southern Indian Ocean, while the Monsoon
Winds, blowing out of the southwest, create an anticyclonic circulation pattern in the northern
Indian Ocean. The Southwest Trades create an upwelling system off the coast of Java, while the
Monsoon Winds cause upwelling along the coasts of Somalia and the Arabian peninsula (Fig.
1.7). However, during winter in the northern hemisphere the Monsoon Winds blow off the Asian
Figure 1.8 Surface winds systems (arrows) and major coastal upwelling areas (hatched) in the
southern hemisphere and Indian Ocean in February and August. Source: K. Wyrtki (pers.
continent. Both the wind and current systems off the Arabian peninsula, the northeast coast of
Africa, and the southern coast of Java reverse direction, and the upwelling is destroyed. Thus the
upwelling in these areas is confined to the northern hemisphere summer months.
Current estimates of marine net primary production are derived from satellite-based
estimates of surface water chlorophyll concentrations and temperature. This information
becomes input to empirical algorithms that are used to calculate vertically integrated water
column primary production. The numbers so calculated differ somewhat depending on the
algorithms used to relate chlorophyll and temperature to primary production, the range of
Figure 1.9 Wind and current systems and inorganic phosphate concentrations (M) along the
California coast during upwelling conditions. Source: K. Wyrtki (pers. comm.)
estimated global marine primary production being roughly 45 to 57 petagrams (Pg)3 of carbon
per year (Falkowski, et al., 2003). Table 1.5 lists estimates of marine primary production in open
ocean, coastal, and upwelling areas based on calculations of Martin et al. (1987). In this case the
total primary production is estimated to be 51.5 Pg C y-1, about the midpoint of the range of
recent estimates. A striking feature of this summary is that upwelling areas contribute very little
to the total of marine primary production, even though upwelling areas are the most productive
per unit area. The explanation of this discrepancy is the fact that upwelling areas account for
A petagram is 1015 grams.
only about 0.1% of the ocean’s surface area. The open ocean on the other hand, despite ranking
last among the three provinces in terms of production per unit area, accounts for more than 80%
of marine primary production, because it accounts for 90% of the ocean’s surface area.
Table 1.5 Estimates of marine primary production from Martin et al. (1987)
% of primary
% of ocean
(1012 m2)
(gC m-2 y-1)
(Pg C y-1)
Open ocean
Coastal zone
If commercial fish catches were directly proportional to primary production rates, the
open ocean would clearly account for most of the commercial fish catch, and the coastal zone
would account for over 40 times the commercial fish catch of upwelling areas. In fact the coastal
zone and upwelling areas contribute almost equally to the world fish catch and are far more
important in that respect than the open ocean.
The explanation for this paradox lies in the very different nature of the primary producers
and the food chains leading to commercially useful fish in the three oceanic provinces. Both
phytoplankton biomass and photosynthetic rates in the open ocean are dominated by algal
picoplankton, tiny unicellular phytoplankton with a diameter between 0.2 and 2.0 microns (m)
(Sieburth, et al., 1978). Such organisms typically account for 50-90% of the chlorophyll a (chl
a) and primary production in the open ocean (Fogg, 1986; Stockner and Antia, 1986). These tiny
cells are too small to be grazed by the typical crustacean zooplankton, most of whom feed
preferentially on organisms in the microplankton (20-200 m diameter) size range (Parsons, et
al., 1967). Our understanding now indicates that the algal picoplankton and nanoplankton
(diameter 2-20 m), which together account for 98-99% of the algal biomass and production in
the open ocean (Takahashi and Bienfang, 1983) are grazed primarily by phagotrophic protozoan
flagellates, which in turn are grazed by ciliates such as tintinnids. The open-ocean ciliates are
large enough to be grazed by crustacean zooplankton such as copepods, ostracods, amphipods,
decapods, and euphausids, which are then consumed by even larger zooplankton such as
chaetognaths or by micronekton (small fish). The food chain leading from this trophic level to
commercially useful open ocean fish such as tuna, salmon, squid, billfish, and sharks involves
probably 1-2 additional trophic levels. Small tuna and squids may feed directly on micronekton.
However, large tuna such as yellowfin feed primarily on small tuna, squid, and forage fish such
as mackerels, jacks, sauries, and flying fish (Mann, 1984). The reason is that tuna and other
similar fish feed primarily during the day when the vertical migrators are absent from the
epipelagic. Based on figures given by Mann (1984) only about 1/3 of crustacean zooplankton
production is transferred up the epipelagic food chain to commercially useful fish. The
remaining 2/3 goes to the mesopelagic.
Figure 1.10 summarizes the open ocean food chain leading to commercially useful fish.
A critical assumption in constructing such a model is the efficiency with which organic carbon is
transferred from one trophic level to the next. It is known that maximum growth efficiencies are
typically about 30% in young, actively growing animals (Gerking, 1952). However, growth
efficiencies invariably decline and become zero in mature adults. Second, in animals at least
there is a basal metabolic requirement that must be satisfied to maintain the animal even in the
absence of growth. A proportionally higher percentage of an organism’s assimilated food is used
to support basal metabolism the slower the animal is growing. In the case of nekton it can be
argued that considerable energy is spent searching for food due to the low abundance of prey in
the open ocean and that growth efficiency under such conditions must be considerably less than
the empirical maximum of 30%. Finally, when considering trophic level production efficiencies
rather than growth efficiencies of individual organisms, additional losses must be taken into
account. For example, death by any mechanism other than predation leads to a reduction in
ecological efficiency but is ignored in the calculation of growth efficiencies of individual
Large tuna, sharks, billfish (0.51)
Small tuna, salmon, squid (3.39)
Chaetognaths, micronekton (22.6)
Mesopelagic vertical migrators (45.2)
Crustacean zooplankton (339)
Ciliates (1,695)
Flagellates (8,476)
Algal picoplankton and
nanoplankton (42,380)
Figure 1.10 The food chain leading to commercial fish production in the open ocean. Values in
parentheses are production rates in Mt carbon per year.
Based on these considerations as well as the work of Slobodkin (1961) and Schaefer
(1965), Ryther (1969) concluded that trophic level production efficiencies in marine food chains
probably varied between 10% and 20%. He reasoned that efficiencies in open ocean food
chains were probably close to 10% because evidence at the time indicated that phytoplankton
populations in the open ocean were growing very slowly due to the low concentration of
inorganic nutrients (e.g., Sharp, et al., 1980) and it seemed reasonable to assume that most
protozoans and zooplankton were likewise growing slowly due to the low concentration of prey
organisms. However, the implications of subsequent laboratory studies with chemostats
(Goldman, 1980; McCarthy and Goldman, 1979) and direct field measurements (Laws, et al.,
1987; Marra and Heinemann, 1987) suggested that phytoplankton in the open ocean were not
severely nutrient limited and might be growing at rates of 1-2 doublings per day. Protozoan
growth rates estimated in conjunction with such studies likewise yielded growth rates of
approximately 1.0 doubling d-1 (Heinbokel, 1988). Hence there is a strong suggestion that in the
open ocean the plankton at least are not growing as slowly as was once believed and by
implication that the ecological efficiencies at the lower trophic levels may be close to 20%.
Figure 1.10 assumes a trophic level production efficiency of 20% between the first and
fifth trophic levels and an efficiency of 15% between the fifth and seventh trophic levels. The
assumption of a 20% transfer efficiency for the lower trophic levels is consistent with Mann’s
(1984) estimate that mesopelagic fish production amounts to about 0.9-1.8 kcal m-2 y-1. Using
the conversion 1.0 g C = 11.4 kcal (Platt and Irwin, 1973), Mann’s estimate translates into 0.080.16 g C m-2 y-1 or 26-51 Mt C y-1 for the open ocean, a result that agrees reasonably well with
the estimate in Fig. 1.10 of 45.2 Mt C y-1 calculated with trophic level production efficiencies of
20% for trophic levels 1-5.
The rationale for assuming ecological efficiencies of 15% at the higher trophic levels is
that the larger predators are highly motile and undoubtedly consume a great deal of energy in
swimming. The migrations of tuna, for example, take them back and forth across the width of
the Pacific Ocean (Bardach and Ridings, 1985; Blackburn, 1965). It therefore seems reasonable
to assume that ecological efficiencies between the two highest trophic levels are less than 20%,
although it is unclear by how much. Choosing the ecological efficiencies between the fifth and
seventh trophic levels to be the average of the two extremes postulated by Ryther (1969) seems a
reasonable compromise and leads to a production estimate at the seventh trophic level that is
roughly consistent with calculations made by Mann (1984), who estimated top carnivore
production in the open ocean to be about 0.02-0.03 kcal m-2 y-1 = 0.57-0.86 Mt C y-1.
Food chains leading to commercially useful fish in the coastal zone are radically different
from open ocean food chains for several reasons. First, the size distribution of phytoplankton
cells is different. Whereas algal microplankton account for only 1-2% of the primary production
in the open ocean, studies by McCarthy et al. (1974), Malone (1971a), Hallegraeff (1981), and
Malone et al. (1983) indicate that algal microplankton probably contribute about 1/3 of the
primary production in the coastal zone. Cells in the microplankton size range can easily be
grazed by crustacean zooplankton such as copepods and euphausids. Furthermore, in many
important temperate and polar coastal fishing areas a very significant portion of the annual
primary production is contributed by the spring bloom, which is dominated by algal
microplankton. For example, studies by Malone et al. (1983) indicate that 35% of annual
primary production in the New York bight is contributed by the February-April diatom bloom.
Because of their large size algal microplankton tend to sink rapidly, and studies by Laws et al.
(1988) indicate that about 40% of the organic matter produced during the spring bloom may sink
out of the euphotic zone in the form of viable cells. This flux of cells constitutes an important
source of nutrition for the benthos. Second, commercial finfish in the coastal zone include both
pelagic species such as the clupeids (e.g., herring, sardines, anchovies, and menhaden) and
demersal fish such as gadoids (e.g., cod, haddock, hake, pollock). In addition the coastal zone
catch includes mollusks such as clams and oysters and crustaceans such as crabs, lobsters, and
shrimp. Many of the commercially important coastal zone pelagic finfish feed on herbivorous
zooplankton or invertebrate carnivores such as chaetognaths. Thus they are much lower on the
food chain than are the open ocean top level carnivores. The food chain leading to the demersal
fish is more complex. Some demersal fish such as cod and whiting feed to a significant degree
on pelagic fish (Steele, 1974); while others, such as haddock, derive much of their nutrition from
a detritus food chain, with several intermediate steps between the detritus and demersal fish.
Thus from a food chain standpoint the demersal fish are further removed from the primary
producers than are the coastal zone pelagic species.
Figure 1.11 summarizes the coastal zone food chains leading to commercially useful fish.
The structure of the food web is similar to that postulated by Steele (1974), but quantitatively the
fluxes have been modified to allow for the most recent information on coastal zone primary
production rates (Table 1.5) and the size distribution of the phytoplankton. All ecological
efficiencies are assumed to be 20%, since the abundance of nutrients and food in the coastal zone
suggests that organisms are growing rapidly and do not expend a great deal of energy searching
for food. For the lower trophic levels this assumption is consistent with Steele’s conclusion,
based on different arguments that, “Transfer efficiencies around 20 percent appear to be required
of the pelagic herbivores and also possibly of the benthic infauna that feed on fecal material”
(Steele, 1974, p. 25).
Of the annual primary production of 9,000 Mt of carbon, 1/3 or 3,000 Mt are attributed to
algal microplankton. About 60% or 1,800 Mt of this production is assumed to be grazed by
crustacean zooplankton. The other 40% or 1,200 Mt sinks directly to the bottom as
phytodetritus. Algal picoplankton and nanoplankton are assumed to account for 2/3 or 6,000 Mt
of the total primary production. Their production must be routed through intermediate protozoan
trophic levels before reaching the crustacean zooplankton. Reeve (1970, p. 187) has argued that,
“The majority of energy converted into animal material by copepods must be distributed to
higher levels via chaetognaths”. Figure 1.11 assumes that invertebrates such as chaetognaths and
ctenophores consume about 75% of the crustacean zooplankton production, with the remainder
being eaten by pelagic finfish, which also consume the invertebrate carnivores.
natural mortality
and fishing
carnivores (61)
pelagic fish (32.6)
macrobenthos (49)
flagellates (1,200)
demersal fish (10)
zooplankton (408)
ciliates (240)
large demersal
fish (0.4)
epifauna (4)
bacteria (322)
meiobenthos (19)
phytoplankton (9,000)
Figure 1.11 Food chains leading to commercial fish production in the coastal zone. Values in
parentheses are production rates in Mt of carbon per year.
The crustacean zooplankton are assumed to assimilate about 80% of the food they ingest
and to excrete the other 20% as fecal material, an assumption consistent with zooplankton
metabolic studies summarized by Corner and Davies (1971). This fecal material combined with
the fallout of micronekton phytodetritus is assumed to provide the organic input to the benthic
detritus food chain. Following Steele (1974), this detritus is assumed to be converted entirely
into bacterial biomass before being consumed by benthic infauna. The benthic infauna are
assumed to consist of macrobenthos such as annelid worms, echinoderms, and mollusks and
microbenthos such as nematodes and copepods. The macrobenthos is assumed to graze as well
on the meiobenthos, and production of the former is assumed to be 2.5 times the production of
the latter. About 60% of the macrobenthos production is assumed to go to demersal fish and
40% to benthic epifauna. The latter are in turn grazed by the former. Finally some of the older
and larger demersal fish (e.g., adult cod) are known to feed on younger stages of demersal
species, and this natural mortality is assumed to remove about 20% of the total production of
demersal fish.
The implications of the model are that pelagic fish production in the coastal zone should
amount to about 32.6 Mt of carbon per year and demersal fish production about 10.4 Mt of
carbon. Assuming a wet weight to carbon ratio of about 10 for finfish (Ryther, 1969), these
estimates translate into annual yields of 9.1 and 2.9 grams of wet weight per square meter for
pelagic and demersal species, respectively, in the coastal zone. These yields are remarkably
similar to Steele’s (1974) total yield estimates of 8.0 and 2.6 grams of wet weight per square
meter for pelagic and demersal species, respectively, in the North Sea, an area whose ecology
and fisheries have been extensively studied.
Food chains leading to commercially useful fish are shortest in upwelling areas. Almost
all commercially important fish in upwelling areas are planktivorous clupeids such as sardines
and anchovies. Although the juveniles of these species may feed largely on zooplankton, the gill
rakers of the adults are finely spaced enough to filter out many algae in the microplankton
category. During upwelling events as much as 80-90% of the primary production may be
accounted for by algal microplankton (Malone, 1971b). This condition arises in part because the
individual phytoplankton cells that proliferate during upwelling events are large but also reflects
the fact that many of the species form colonial gelatinous masses or long filaments (Ryther,
1969). Hence much of the organic matter produced during upwelling events can be cropped by
herbivorous clupeids.
Upwelling, however, is not a continuous process either temporally or spatially. The
reason is that the wind conditions required to produce upwelling are themselves not constant
temporally or spatially. As a result masses of upwelled water with horizontal dimensions on the
order of kilometers to tens of kilometers may appear at the surface from time to time and persist
over periods of days to weeks, but not indefinitely. Between upwelling events production drops
dramatically, and the composition of the phytoplankton shifts toward organisms in the
picoplankton and nanoplankton size range.
Malone’s (1971b) study of productivity and phytoplankton composition in the California
Current system from October 1969 to February 1971 dramatically illustrates this behavior.
During intense upwelling events photosynthetic rates were 5-10 times higher than during oceanic
(non-upwelling) conditions. The photosynthetic rates of the algal picoplankton and
nanoplankton were relatively constant throughout the year, with a coefficient of variation (CV)4
of 42%. Algal microplankton productivity on the other hand underwent large fluctuations (CV =
138%) and increased dramatically during upwelling events. During intense upwelling algal
microplankton accounted for about 83% of the primary production but for only 28% at other
times. Over the course of the 16-month study the algal microplankton contributed about 57% of
the total primary production.
Figure 1.12 summarizes the food chain leading to commercially useful fish in upwelling
areas based on this information. As in the coastal areas, all ecological efficiencies are assumed
carnivores (1.4)
pelagic fish (9.3)
ciliates (2.6)
natural mortality
and fishing
zooplankton (9.1)
flagellates (12.9)
phytoplankton (150)
Figure 1.12 Food chains leading to commercial fish production in upwelling areas. Values in
parentheses are production rates in Mt of carbon per year.
The coefficient of variation is the standard deviation divided by the mean value.
to be 20%. Of the annual primary production of 150 Mt of carbon, 57% or 85.5 Mt is attributed
to algal microplankton, and the remaining 64.5 Mt to picoplankton and nanoplankton. The
sinking loss of algal microplankton cells is assumed to be negligible due to the fact that the cells
are being advected upward at speeds of 1-3 m d-1 during upwelling events, when most of the
microplankton production occurs. With few exceptions viable phytoplankton cells sink at rates
less than or equal to approximately 1.0-1.5 m d-1 (Bienfang, 1981; Laws, et al., 1988).
Following Ryther (1969), we assume about half the algal microplankton production to be grazed
directly by the commercially important fish, with the remainder consumed by crustacean
zooplankton. The algal picoplankton and nanoplankton production is routed through a flagellateciliate food chain. The crustacean zooplankton are assumed to graze on ciliates and algal
microplankton and are themselves eaten by pelagic fish and invertebrate carnivores. As was the
case in the coastal province, we assume 75% of the crustacean zooplankton production to be
routed through the invertebrate carnivores and the remainder to the pelagic fish. Although the
pelagic fish are assumed to feed n algal microplankton, crustacean zooplankton, and invertebrate
carnivores, it is clear from the numbers in Fig. 1.12 that almost all the food eaten by the pelagic
fish is algae.
Table 1.6 summarizes the estimates of commercially useful fish production based on the
models in Figs. 1.10-1.12. These estimates may be compared to the present harvest of marine
finfish of about 70 Mt fresh weight. The total estimated production exceeds the harvest by about
a factor of 8, but how sensitive is the estimated production to the assumptions in the models, and
how realistic is it to compare total production to sustainable harvest?
Table 1.6 Estimates of annual production of commercially useful fish based on the models in
Figs. 1.10-1.12. The ratio of fresh weight to carbon in the fish is assumed to be 10.
Carbon (Mt)
Open ocean
Fresh weight (Mt)
Coastal zone
Certainly the models are sensitive to the percentage of primary production attributed to
the microplankton, because routing the primary production through the flagellate-ciliate food
chain reduces the input to the crustacean zooplankton by a factor of 25 if the ecological
efficiency is 20%. In the case of the open ocean food web (Fig. 1.10), the production of
crustacean zooplankton would almost double if only 4% of the primary production were assumed
to be grazed by crustacean zooplankton, i.e., if 4% of the primary production were attributed to
algal microplankton. As did Ryther (1969), we assumed that no open ocean phytoplankton were
grazed directly by crustacean zooplankton, an assumption that must certainly be regarded as
conservative. Data reported by Takahashi and Bienfang (1983) for Hawaiian waters indicate that
microplankton account for 1.2% of primary production in the open ocean, but Malone’s (1971a)
work in the eastern Pacific and Caribbean would put the microplankton contribution closer to
10%. Had we assumed an algal microplankton contribution of 10%, the production of crustacean
zooplankton in the open ocean food web model would have increased by a factor of 3.4, and
similar increases would be expected at higher trophic levels.
That the implications of the open ocean model are roughly consistent with independent
estimates of open ocean fish production (e.g., Mann, 1984) should not be too reassuring. The
model could easily be right for the wrong reasons. For example, assuming that crustacean
zooplankton directly graze 5% of the open ocean primary production and that ecological
efficiencies between all trophic levels are 15% gives production estimates at trophic levels 5-7
that are virtually identical to those of Fig. 1.10. Given the information that has accumulated over
the last 35 years, it seems fair to say that primary production rates in the open ocean are
substantially higher than Ryther’s (1969) assumed figure of 50 g C m-2 y-1 (see Table 1.5).
Nevertheless, the conclusion is still that the open ocean can account for only a small percentage
of the traditional commercially important fish catch.
The coastal zone food web (Fig. 1.11) is much more complex han the postulated linear
open ocean food chain. There is good agreement between the estimated pelagic and demersal
fish production and Steele’s (1974) independently derived estimates of fish production in the
North Sea, but again the agreement could be fortuitous. It is noteworthy that Ryther’s (1969)
estimate of fish production in the coastal zone is only about 30% of the value estimated from the
present model. The discrepancy can be traced largely to the fact that Ryther’s assumed primary
production rate is 40% of the value assumed in Fig. 1.11.
Our estimate of commercial fish production in upwelling areas is reasonably close to the
value calculated by Ryther (1969), but the agreement is somewhat deceptive. Our assumed
primary production rate is 1.4 times the figure used by Ryther, but we also assumed that only
57% of primary production was accounted for by microplankton (Ryther assumed 100%). By
the time the remaining 43% of the primary production is routed through the flagellate-ciliate
food chain, its contribution to the food chain leading to commercial fish is almost zero. If the
remainder of our model is basically consistent with Ryther’s (1969) assumptions, our calculated
fish production should be (1.4)(57%) = 80% of the value estimated by Ryther, which is very
close to the actual ratio of 78%. In food chain and food web models, two rather different sets of
assumptions can lead to essentially the same conclusion regarding production at the highest
trophic levels.
In our models we have ignored the role of dissolved organic matter and hence implicitly
assumed that excretion of dissolved organic carbon (DOC) represents as much of a loss to the
system as does respiration. Strictly speaking, this assumption is false. DOC can be assimilated
by bacteria, which are then consumed primarily by protozoa flagellates (Azam, et al., 1983;
Ducklow, 1983; Fenchel, 1982). In this way the DOC released by both animals and algae is
recycled back into the food chain. The importance of this “microbial loop” was emphasized in
seminal papers by Pomeroy (1974) and Azam et al. (Azam, et al., 1983). A major question in
recent years has been whether the microbial loop functions primarily as a remineralizer of
organic carbon or whether it supplies a significant input of particulate organic carbon (POC) to
the food chain. Experimental studies have tended to show that the microbial loop is not a
significant source of POC. For example, Smith et al. (1977, p. 35) concluded that,
“Bacterioplankton production has a minor role in the particulate carbon budget of upwelling
regions”; Joint and Williams (1985, p. 297) found that, “The data do not appear to support the
idea of a significant flow of energy through the ‘microbial loop’ in the Celtic Sea in August”;
Azam et al. (1983, p. 260) concluded, “Energy released as DOM [dissolved organic matter] by
phytoplankton is rather inefficiently returned to the main food chain via a microbial loop of
bacteria-flagellate-microzooplankton”; and Ducklow et al. (1986, p. 865) stated, “Secondary
(and, by implication, primary) production by organisms smaller than 1 micrometer may not be an
important food source of marine food chains”.
From a theoretical standpoint it is not hard to rationalize why the microbial loop
contributes little to POC production. In the coastal zone and upwelling areas primary production
by algal microplankton is far more important than picoplankton and nanoplankton production as
a source of food for the crustacean zooplankton because any carbon routed through the
flagellate-ciliate food chain is reduced by a factor of 1/(0.2)2 = 25 before it reaches the
crustacean zooplankton. DOC must travel through a bacteria-flagellate-ciliate food chain before
reaching the crustacean zooplankton and hence would be reduced by more than a factor of 25
before reaching the crustacean zooplankton. Obviously the flux of DOC would have to be
enormous to compete with algal microplankton production as a source of POC for crustacean
The province where the microbial loop would most likely be significant is the open
ocean, where algal microplankton production accounts for very little of the photosynthesis.
Figure 1.13 is a representation of the open ocean food web analogous to Fig. 1.10 but with a
microbial loop included. We have assumed following Williams (1981) that 30% of
phytoplankton production is excreted as DOC by the phytoplankton, so that the previously
estimated figure of 42,380 Mt of carbon per year for the primary production rate in the open
ocean represents only 70% of the true annual production rate of 60, 543 Mt of carbon. Also
consistent with Williams’ (1981) model is our assumption that organisms excrete as DOC about
20% of the carbon they ingest. The mesopelagic vertical migrators are assumed to excrete in the
mesopelagic rather than the epipelagic, although it makes little quantitative difference whether
their excretion is included in the microbial loop or not. Following Ducklow (1983) and Goldman
et al. (1987), we assume that pelagic bacteria convert DOC into bacterial biomass with an
efficiency of about 50%.
The implication of Fig. 1.13 is that recycling of organic carbon through the microbial
loop can increase production at higher trophic levels by almost 40% (compare to Fig. 1.10) in a
system in which all production is routed through protozoan flagellates and ciliates. However, if
only 5% of algal primary production is assumed to be grazed directly by crustacean zooplankton,
assumptions otherwise identical to those employed in Fig. 1.13 lead to the conclusion that
recycling of organic carbon through the microbial loop can increase higher trophic level
production by only 17-18%. Evidently the impact of the microbial loop on commercial fish
production will be significant only in systems where no more than a few percent of
photosynthetic production is grazed by crustacean zooplankton. This condition may (Takahashi
and Bienfang, 1983) or may not (Malone, 1971a) apply to the open ocean.
In 1969 Ryther estimated the production of commercially useful fish in the open ocean to
be about 1.6 Mt per year. Regardless of the impact of the microbial loop on open ocean
production, several pieces of evidence suggest that Ryther’s estimate was much too low. First of
all, the present commercial catch of tunas, bonita, and billfish amounts to about 6.0 Mt per year,
large tuna, sharks, billfish (0.7)
small tuna, salmon, squid (4.65)
chaetognaths, micronekton (31)
mesopelagic vertical migrators (63)
crustacean zooplankton (470)
ciliates (2,351)
flagellates (11,754)
bacteria (16,388)
algal picoplankton and
nanoplankton (60,543)
Figure 1.13 Food chain leading to commercial fish production in the open ocean with the
microbial loop included. Values in parentheses are production rates in Mt of carbon per year.
and the catch of these species has exceeded 2.0 Mt since 1974. Obviously the open ocean is
producing substantially more than 1.6 Mt of these and other high level carnivores, but is the true
figure close to the 39 Mt estimated with the present model? Relevant to this question is the
estimation of Clarke (1977) that the present population of sperm whales eats more than 110 Mt
of cephalopods per year. Obviously this figure exceeds by about a factor of three our estimated
production of all high level (trophic levels 6 and 7) carnivores in the open ocean but is not
implausible if many of the cephalopods consumed by sperm whales are denizens of the
mesopelagic and feed on vertical migrators. In fact lantern fish are known to be a major source
of food for many oceanic squid (R. Young, personal communication). Assuming Clarke (1977)
is right, production at trophic level 5 in the open ocean must be comparable to or even greater
than the estimates given in Fig. 1.10. The implication is that fish production at trophic level 6
and 7 must be at least an order of magnitude higher than Ryther’s (1969) estimate.
Table 1.6 suggests that the commercial fish catch from the open ocean might be about
40% of the commercial catch from upwelling areas, but an examination of catch statistics
indicates that the open ocean probably accounts for less than 20% of the commercial catch
recorded in upwelling areas. The reason for this discrepancy may be severalfold. First, the
surface area of the open ocean is about 900 times that of upwelling regions. Commercial fish
production per unit area is over 2,000 times greater in upwelling systems than in the open ocean.
Consequently it s in general much more costly to find and catch fish in the open ocean than it is
in upwelling areas. To be worth catching, an open ocean fish must bring a high price to the
marketplace. The same condition does not constrain fishing activities in upwelling areas. In
short, economic considerations may have tended to limit our exploitation of open ocean fisheries
because the resource is so widely dispersed, while fisheries in upwelling areas have been
exploited to the maximum extend possible. Second, the sustainable catch may be a smaller
percentage of gross production in the open ocean than in upwelling areas. Certainly the
population dynamics of the important open ocean species appear to be very different from the
population dynamics of the important upwelling species, and the implications of this difference
with respect to sustainable yields can be profound. We will examine this point in much more
detail in Chapter 4.
Up to this point our estimates of commercial fish production have ignored the
contribution of bivalve mollusks and decapod crustaceans. Strictly speaking these organisms are
not fish, but they are a good source of protein, and the catch of mollusks and crustaceans is
routinely reported in commercial fish catch summaries. Shrimp and prawns account for about
half the total decapod catch and crabs about 25%. Clams and oysters account for about a third of
the total marine bivalve catch, and mussels and scallops about 10-15%.
Together bivalve mollusks and decapod crustaceans account for 10-15% of the total
marine fish catch based on fresh weight. This statistic is somewhat misleading, because the
percentage of organic matter in some of these organisms is rather low compared to finfish. For
example, the shell of some oysters may account for 70% of the oyster’s fresh weight (J. Bardach,
personal communication). Nevertheless, it seems fair to say that bivalves and decapods are
among the more important contributors to the marine fish catch. More intriguing is the position
some of these organisms occupy in the marine food web. Bivalves are generally considered to
be herbivores. Hence these organisms are low on the food chain, and if they harvest a significant
percentage of the primary production in coastal and upwelling areas, their potential production is
enormous. Decapods of commercial importance are found primarily in coastal areas, where as a
group they are probably best classified as omnivores.
Several different factors limit the contribution of bivalves to the marine fish catch. First,
bivalves require a suitable substrate for settlement. Clams require a soft bottom; oysters need a
hard substrate. The abundance of these organisms is therefore controlled to a large extent by the
availability of substrates and the ability of the bivalves to compete with other organisms (e.g.,
corals) for those substrates. Second, because bivalves are sessile organisms, they depend on
currents to bring them food. Obviously they can consume only those phytoplankton cells that are
advected to them by favorable currents. They are not in a good position to compete with
protozoans and zooplankton for phytoplankton cells in other than very shallow areas. Third,
coastal pollution has seriously reduced the yields of many once-productive shellfish beds, either
because the growth of the shellfish has been seriously reduced, the shellfish have been killed
outright, or the shellfish are contaminated and unfit for human consumption (Bardach, et al.,
1972; Ryther and Dunstan, 1971). As long ago as 1964 about 12% of the shellfish grounds in the
United States were closed to harvesting for health reasons and, “In New York state, a principal
producer of oysters but also a highly populous and industrialized state, oyster production over a
50-year period declined by 99% . . . The town of Malebon, once the chief oyster port of the
Philippines, has been virtually eliminated from the industry by pollution” (Bardach, et al., 1972,
p. 676).
At the present time production of bivalve mollusks is dominated by the aquaculture
industry, with an annual production of about 11 Mt. That figure has doubled during the last 10
years. During the same time period, the wild catch of oysters, mussels, scallops, and clams has
dropped from 2.0 to 1.5 Mt. To a fair degree the growth of the bivalve aquaculture industry
reflects the utilization of suitable coastal habitat by the industry, i.e., a transition from harvesting
wild stocks to systematic farming and husbandry. Competition with other uses of the coastal
zone, including recreation and waste disposal, will ultimately limit the size of the industry.
The potential catch of decapod crustaceans is substantially less than the potential catch of
bivalve mollusks because of the higher position of the former on the food chain. In coastal areas,
where most of the harvest of decapods occurs, the decapods are probably best considered to be a
component of the epifauna. If Fig. 1.11 is not misleading, the potential decapod harvest should
therefore be small compared to demersal fish production. Gulland (1971) estimated the potential
decapod catch at 2.3 Mt, but his estimate is undoubtedly too low. The total decapod yield has
exceeded Gulland’s estimate every year since 1980, and the wild catch currently averages more
than 4 Mt y-1. Aquaculture production provides another 1.5 Mt y-1. Like the bivalves, decapods
have been adversely affected by pollution and human use and development of coastal areas. For
example, along coastal Louisiana the shrimp catch has shifted from about 95% white shrimp to
about a 50:50 mixture of white and brown shrimp. This shift in composition has apparently been
caused by destruction of the white shrimp’s brackish water nursery grounds due to construction
activities associated with laying of oil pipelines and erection of drilling rigs (NAS, 1975, p. 89).
The Sustainable Catch
With the production estimates in Table 1.6, it is possible to make an estimate of the
sustainable catch that mankind might expect to take from the oceans if we rely on the traditional
species of fish. By sustainable catch we mean the catch one could expect to achieve year after
year. Obviously one could take an enormous harvest in any one year by catching every fish in
the sea, but the catch in subsequent years would be zero, and hence the very large single-year
harvest would not represent a sustainable yield. A sustainable harvest is achieved when each
year’s losses to fishing and natural mortality are offset by increases resulting from reproduction
and growth. In other words
Where F is the annual sustainable fish catch, M is the loss from the fish population due to natural
mortality, and G is the gross population increase due to growth and reproduction. The
production figures in Tables 1.6 are estimates of G.
It is thought-provoking to realize that in the absence of a fishery (F = 0) G and M must on
the average balance each other. Otherwise the population would disappear (M > G) or,
alternatively, we would be up to our ears in fish (G > M). In the early years of a fishery it is
reasonable to assume that G and M will still be nearly equal and therefore population losses (F +
M) will exceed gains (G). The population will therefore decline. However, if all goes well the
dynamics of the fish population will eventually change in response to the fishery, and G will
exceed M. This condition might develop, for example, because with a smaller population there
are more resources available to the remaining individuals. Hence the fish that remain grow
faster, are better able to avoid predators, produce more offspring, and so forth. The population
size stabilizes when the difference between G and M equals F (i.e., Eq. 1 is satisfied).
Figure 1.14A illustrates how G and M might be expected to vary as a function of
population size. As the population is reduced from its virgin (unfished) size, a gap develops
between G and M. This gap represents the sustainable fishery yield corresponding to the given
population size. In other words, the sustainable catch F equals the vertical distance between the
G and M curves, as illustrated in Fig. 1.14B. Obviously F equals zero for the virgin population,
but F increases as the population size is reduced and eventually reaches a maximum, which is the
length of the dashed line in Fig. 1.14A and Fig. 1.14B. Further reductions in the population size
reduce the sustainable catch.
Figure 1.14 (A) Hypothetical relationship between a fish stock and gross production (G) and
natural mortality (M). The dashed line represents the maximum sustainable yield in a steady
state system. (B) The sustainable fish catch (G – M) as a function of stock size on the same scale
as gross production and natural mortality in panel A.
An important question in fisheries management is the size of the maximum sustainable
yield (MSY) relative to gross production for the virgin population. As Fig. 1.14 is drawn, the
MSY is 25% of the gross production of the virgin stock. Most fisheries biologists agree that the
MSY is unlikely to be more than 50% of the gross production of the virgin stock (Gulland,
1971), and for various reasons to be discussed in this text, the percentage may be substantially
less. As a working hypothesis, let us assume that the MSY is 25% of the gross production of the
virgin stock.
Let us now return to the food chain/web models in Figs. 1.10-1.12. The MSY estimate
for the upwelling areas is straightforward because we harvest from only one of the boxes in the
model. The MSY is therefore estimated to be about (0.25)(93) = 23 Mt fresh weight per year. In
the case of the open ocean we can harvest at both trophic levels 6 and 7, but any harvest at
trophic level 6 will presumably diminish production at trophic level 7. In this case the MSY is
obviously achieved by taking as much as possible from trophic level 6 and accepting a
diminished harvest at trophic level 7. If we harvest 25% of the production at trophic level 6, it
seems reasonable as a first approximation to assume that production at trophic level 7 will be
reduced by 25%. Hence the MSY is (0.25)[33.9 + (0.75)(5.1)] = 9.4 Mt fresh weight per year.
The coastal zone food web is even more complex. We harvest from three boxes in the
model, but the catch of large demersal fish will be negligible compared to the catch of pelagic
and small demersal species. It makes sense to take as much of the pelagic fish production as
possible and accept a somewhat reduced harvest of demersal species. If we assume that
harvesting 25% of the pelagic production reduces by 25% the consumption of pelagic fish by
demersal fish, the production of demersal fish becomes (0.2)[(0.75)(16.3) + 29 + 4] = 9.0 Mt of
carbon per year. The coastal zone MSY is therefore estimated to be (0.25)(32.6) = 8.2 Mt of
carbon or 82 Mt of fresh weight of pelagic fish and (0.25)(9.0) = 2.3 Mt of carbon or 23 Mt fresh
weight of demersal fish per year. These figures translate into areal harvest rates of 2.3 and 0.64
tonnes fresh weight per square meter per year for pelagic and demersal species, respectively,
values that are rather close to the average yields of the respective categories of fish in the North
Sea during the period 1910-1960 (Steele, 1974). Based on these calculations, the MSY for the
entire ocean is 23 (upwelling) + 9.4 (open ocean) + 105 (coastal zone) = 137 Mt fresh weight per
This figure is in the range of other estimates, most of which put the potential finfish catch
in the range 100-200 Mt per year (Graham and Edwards, 1962; Gulland, 1971; Ryther, 1969;
Schaefer, 1965). However, the agreement of the estimates is somewhat deceptive, because the
assumptions that underlie the estimates sometimes differ greatly, as do the details of the catch
breakdown. Ryther (1969), for example, concluded that the potential yield in upwelling and
coastal areas was about the same and equal to 60 Mt, whereas our model predicts the yield from
coastal areas to be 4.6 times the yield from upwelling areas.
Of perhaps greater concern is the fact that the present finfish catch of 70 Mt y-1 is
apparently about all the fishing pressure the ocean can sustain (Pauly, et al., 1998; Pauly, et al.,
2003). If the MSY is roughly 140 Mt, why are fisheries in trouble when the catch is only half
that value? We will have a chance to examine this question in detail in Chapter 4. For now
suffice it to say that there are two rather fundamental problems with trying to achieve the MSY.
First, it is straightforward to show that the MSY is not a stable equilibrium point. Although G =
F + M at the MSY, a perturbation to this balance can lead to a disastrous collapse of the fishery.
Many important fish populations naturally experience large interannual fluctuations in
reproduction. A few years in a row of poor reproduction can have disastrous consequences when
a stock is being fished at the MSY. Secondly, from a strictly financial standpoint, it is very
likely that fishing at the MSY makes no financial sense. Except for the highest priced fish, the
financial return per unit effort is often much greater when the stock is fished at a rate well below
the MSY. The conclusion is that there are significant biological and financial barriers to fishing
a stock at the traditional MSY. Is the present finfish catch of 70 Mt y-1 about all we can expect
from the ocean?
Nonconventional Fishery Resources
Up to this point we have considered only conventional marine fisheries, the traditional
finfish and shellfish that account for almost all of the present fish catch. However, there remain
considerable underexploited nonconventional resources such Antarctic krill, midwater fish, and
squid. Can these resources be harvested economically, and would exploitation of these
nonconventional fish likely improve the nutritional status of persons in underdeveloped
Just prior to the breakup of the former Soviet Union, the nonconventional species that
contributed the most to the marine fish catch was the Antarctic krill. However, in 2002 the
harvest of Antarctic krill amounted to only 0.13 Mt. This figure is only a fraction of what most
experts consider to be the potential yield. El-Sayed and McWhinnie (1979) have estimated that
natural predators of Antarctic krill consume about 400 Mt of krill per year, with crabeater seals
the single most important predator, consuming nearly 100 Mt. Based on an assessment of the
quantity of rill consumed by baleen whales, seals, birds, cephalopods, and fish in the Antarctic,
Lubimova and Shust (1980) have estimated that a krill harvest of 60 Mt y-1 could be sustained
without producing a serious impact on the krill population or the natural predators of kill.
Gulland (1971) similarly estimated the potential Antarctic krill yield at 50 or more Mt y-1. These
figures are comparable to the present catch of all marine finfish!
If Antarctic krill were exploited at the rate of 50-60 Mt y-1, the Antarctic krill fishery
would be more than seven times larger than any other single species fishery in the world. The
enormous potential krill catch reflects the fact that while Antarctic kill have some carnivorous,
detritivorous, and cannibalistic habits (El-Sayed and McWhinnie, 1979), they function largely as
herbivores and hence occupy a very low position on the food chain. Therefore from the
standpoint of their tropic position they are comparable to some of the pelagic fish found in
upwelling areas. However, it is problematic whether a catch of 50-60 Mt of Antarctic krill will
ever be realized and even more questionable whether any significant amount of the catch will
find its way to the mouths of undernourished persons. The experience of Russia and Japan, the
only nations to seriously consider exploiting the Antarctic krill fishery, has been that the krill
vary greatly in abundance and location from year to year. The krill are easily bruised, and once
brought on board ship they spoil so rapidly that almost immediate processing and conversion to a
stable product is necessary if any use is to be made of the catch. Furthermore, a noted by
Bardach (1989, p. 2-8), “Their gut must be removed before processing because the algae they
contain tend to cause digestive upset in mammals.” Finally, the Antarctic fishery lies virtually at
the end of the Earth; fishing is impossible during the winter; and the weather is less than ideal
during the summer. In short, the Antarctic krill fishery is one in which economic and
technological considerations limit participation to only the most advanced fishing nations.
Processed krill products designed for human consumption include krill butter and krill
cheese. Krill have also been incorporated into sausage-type products by the Japanese and
Germans (El-Sayed and McWhinnie, 1979). Less sophisticated techniques are required to
produce krill meal suitable as a component of livestock feed, and it would not be surprising if
much of the krill catch were ultimately used for that purpose. Hence for several different reasons
exploitation of the Antarctic krill fishery is unlikely to have much impact on the nutrition of
persons in third world countries.
The open ocean could conceivably contribute much more to commercial fisheries if it
became practical to harvest lower on the food chain. Relevant to this point is Mann’s (1984)
assessment that fish production in the open ocean is dominated by migratory mesopelagic fish, of
which the myctophids or lantern fish are undoubtedly the most important. As Fig. 1.10 indicates,
gross production of these vertical migrators may approach 45.2 Mt of carbon per year or 452 Mt
per year of wet weight. If we take the MSY to be 25% of the latter figure, the potential catch is
about 113 Mt y-1, which is consistent with Gulland’s (1971) independently derived estimate of
100+ Mt per year. This figure is comparable to the present wild catch of all aquatic organisms,
both freshwater and marine!
Given this remarkable potential, it is thought-provoking to discover that the annual
harvest of lantern fish has never exceeded 85,000 tonnes and has averaged less than 2,000 tonnes
since 1993. Russia, Iran, and the Ukraine have been the only nations involved in the fishery in
recent years, and the entire catch is taken in the South Atlantic and Indian oceans. Why is the
actual catch four orders of magnitude smaller than the estimated MSY?
The answer is that lantern fish are widely dispersed horizontally, and while they do
undertake predictable vertical migrations, their concentration at any given depth is too low to
make harvesting economically practical in most parts of the ocean with the exception of some
upwelling areas (Gulland, 1971). I once participated in a research cruise concerned with the
distribution of mesopelagic fish near the Hawaiian Islands. After a midwater trawl lasting
several hours, the two graduate students on board waited eagerly as the net was pulled in. They
had caught less than a dozen small fish. A harvest thousands of times that size would be
required to justify several hours of ship time on a modern fishing vessel. In short, unless there is
some major technological breakthrough in the methodology of catching small mesopelagic fish,
it is doubtful that the annual catch will ever be more than a tiny fraction of the MSY.
Furthermore, even if such a technological breakthrough were made, it would most likely be the
technologically advanced fishing nations rather than third world countries that would be in the
best position to take advantage of the new technology.
The annual catch of cephalopods (squid, cuttlefish, and octopuses) has exceeded 1.0 Mt
since 1972 and has averaged 3.3 Mt since 1996. Various squid species account for the majority
of the catch. If we accept Clarke’s (1977) estimate that sperm whales alone consume about 100
Mt of squid per year, the MSY of cephalopods must greatly exceed the present catch. If we
assume that sperm whales are the dominant consumers of squid and that the MSY equals 25% of
production by the virgin stock, then the MSY of squid is approximately 25 Mt per year. Gulland
(1971) set the potential squid yield at somewhere between 10 and 100 Mt y-1. Is it possible that
the squid harvest could be increased by a factor of 5-10, and if so would much of the catch
benefit persons in third world countries?
While an emphatic yes cannot be given to either of these questions, the probability that
both questions will someday be answered affirmatively is much greater than is the case for the
Antarctic krill and myctophid fisheries. First of all, squid are most abundant in the tropics and
subtropics, a latitudinal zone in which many third world countries are found. Because coastal
states now have sovereign rights over the exploitation of living resources within 200 nautical
miles of their coastlines (Jagota, 1985), many of the potentially important squid fisheries are now
under the control of a subset of these same third world countries. Second, methods exist for
catching squid that do not require a technologically advanced infrastructure. For example, it is
well known that squid are attracted to lights at night. Hawaiian fishermen make use of this fact
by hanging a small light just under the surface of the water at night and catching the squid that
are attracted to the light on jigs or with gaffs (DLNR, 1979). This is not high-tech fishing, but it
works. A third point about the squid fishery is that in some parts of the world there are no
market incentives to encourage development of the fishery. As noted by Gulland (1971, p. 252),
“Squids are heavily exploited round Japan and southern Europe, where they fetch several
hundred dollars a ton as a favored food, but are only lightly fished off Newfoundland, where they
are used mainly as bait at a tenth or less of the price.” With respect to this point it is noteworthy
that the once low-valued Alaska Pollock is now one of the largest fisheries in the world, in part
because a combination of chemical and mechanical methods have been devised to transform its
flesh into ersatz crab and lobster claw meat. Hence given the right market incentives, the squid
fishery may expand dramatically. In summary, of the major nonconventional resources, the
squid fishery appears the most likely to expand on a large scale and at the same time to benefit
third world nations both economically and nutritionally.
Applewhite, T. H., 1980. Fats and fatty oils. Kirk-Othmer Encyclopedia of Chemical Technology
(3rd ed., Vol. 9, pp. 759-831), John Wiley, New York.
Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., Thingstad, F., 1983. The
ecological role of water-column microbes in the sea. Marine Ecology-Progress Series 10, 257263.
Bardach, J. E., 1989. Living marine resources, technology and the extended economic zone.
Paper presented at the EEZ Resources: Technology Assessment Conference, Honolulu.
Bardach, J. E., Ridings, P. J., 1985. Pacific tuna: biology, economics, and politics. In: Borgese,
E. M. and Ginsburg, N. (Eds.), Ocean Yearbook (Vol. 5, pp. 29-57), University of Chicago
Press, Chicago.
Bardach, J. E., Ryther, J. H., McLarney, W. O., 1972. Aquaculture: The Farming and Husbandry
of Freshwater and Marine Organisms. Wiley-Interscience, New York.
Bienfang, P., Gundersen, K., 1977. Light effects on nutrient-limited, oceanic primary production.
Mar. Biol. 43 (3), 187-199.
Bienfang, P. K., 1981. Sinking rates of heterogeneous, temperate phytoplankton populations. J.
Plankton Res. 3 (2), 235-253.
Blackburn, M., 1965. Oceanography and the ecology of tunas. Oceanography and Marine
Biology Annual Reviews 3, 299-322.
Chapman, W. M., 1965. Potential resources of the ocean (Serial publication 89-21, 89th
Congress, first session), U. S. Government Printing Office, Washington, D.C.
Clarke, M. R., 1977. Beaks, nets and numbers. Symposium of the Zoological Society of London
38, 89-126.
Corner, E. D. S., Davies, A. G., 1971. Plankton as a factor in the nitrogen and phosphorus cycles
in the sea. Advances in Marine Biology 9, 101-204.
DLNR, 1979. Hawaii Fisheries Development Plan. Department of Land and Natural Resources,
Ducklow, H. W., 1983. Production and fate of bacteria in the oceans. Bioscience 33, 494-501.
Ducklow, H. W., Purdie, D. A., Williams, P. J. L., Davies, J. M., 1986. Bacterioplankton: a sink
for carbon in a coastal plankton community. Science (NY) 232, 865-867.
El-Sayed, S. Z., McWhinnie, M. A., 1979. Antarctic krill: protein of the last frontier. Oceanus 22
(1), 13-20.
Eppley, R. W., Peterson, B. J., 1979. Particulate organic matter flux and planktonic new
production in the deep ocean. Nature 282 (5740), 677-680.
Falkowski, P. G., Laws, E. A., Barber, R. T., Murray, J., 2003. Phytoplankton and their role in
primary, new, and export production. In: Fasham, M. J. R. (Ed.), Ocean Biogeochemistry: The
Role of the Ocean Carbon Cycle in Global Change (pp. 99-121), Springer, Berlin.
FAO, 1970. Lives in peril. Protein and the child., Food and Agriculture Organization of the
United Nations, Rome.
Fenchel, T., 1982. Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and
importance as bacterial consumers. Marine Ecology Progress Series 9, 35-42.
Fogg, G. E., 1986. Picoplankton. Proceedings of the Royal Society of London Series B 288, 130.
Geider, R. J., Osborne, B. A., Raven, J. A., 1986. Growth, photosynthesis and maintenance
metabolic cost in the diatom Phaeodactylum tricornutum at very low light levels. Journal of
Phycology 22 (1), 39-48.
Gerking, S. D., 1952. The protein metabolism of sunfishes of different ages. Physiological
Zoology 25, 358-372.
Goldman, J. C., 1980. Physiological processes, nutrient availability, and the concept of relative
growth rate in marine phytoplankton ecology, pages 179-194. In: Falkowski, P. G. (Ed.), Primary
Productivity in the Sea, Plenum, New York.
Goldman, J. C., Caron, D. A., Dennett, M. R., 1987. Regulation of gross growth efficiency and
ammonium regeneration in bacteria by substrae C:N ratio. Limnology and Oceanography 32,
Graham, H. W., Edwards, R. L., 1962. The world biomass of marine fishes. In: Heen, E. and
Kreuzer, R. (Eds.), Fish in Nutrition (pp. 3-8), Fishing News (Books), Ltd., London.
Gross, M. G., 1982. Oceanaography, 3rd ed. Prentice-Hall, New York.
Grotius, H., 1609. Mare Liberum. Oxford University Press, Oxford, U.K.
Gulland, J. A., 1971. The Fish Resources of the Ocean. Food and Agriculture Organization of the
United Nations, Rome.
Hallegraeff, G. M., 1981. Seasonal study of phytoplankton pigments and species at a coastal
station off Sydney: importance of diatoms and the nanoplankton. Marine Biology 61, 107-118.
Hardin, G., 1968. The tragedy of the commons. Science (NY) 162, 1243-1248.
Heinbokel, J. F., 1988. Reproductive rates and periodicities of oceanic tintinnine ciliates. Marine
Ecology Progress Series 47, 239-248.
Holt, S. J., Vanderbilt, C., 1980. Marine Fisheries. In: Borgese, E. M. and Ginsburg, N. (Eds.),
Ocean Yearbook II (pp. 9-56).
Jagota, S. P., 1985. The United Nations convention on the law of the sea. Ocean Yearbook 5, 1028.
Joint, I. R., Williams, R., 1985. Demands of the herbivore community on phytoplankton
production in the Celtic Sea in August. Marine Biology 87, 297-306.
Kasahara, H., 1966. Prospect of fish production from the sea. Proceedings 7th International
Congress of Nutrition (Vol. 4. Problems of World Nutrition, pp. 958-964), Pergamon Press, New
Kimball, H. H., 1928. Amount of solar radiation that reaches the surface of the earth on the land
and on the sea, and methods by which it is measured. Monthly Weather Review 56, 393-398.
Lands, W. E. M., 1986. Fish and Human Health. Academic Press, New York.
Laws, E. A., DiTullio, G. R., Redalje, D. G., 1987. High phytoplankton growth and production
rates in the North Pacific subtropical gyre. Limnology and Oceanography (4), 905-918.
Laws, E. A., Bienfang, P. K., Ziemann, D. A., Conquest, L. D., 1988. Phytoplankton population
dynamics and the fate of production during the spring bloom in Auke Bay, Alaska. Limnology
and Oceanography 33 (1), 57-65.
Laws, E. A., DiTullio, G. R., Betzer, P. R., Karl, D. M., Carder, K. L., 1989. Autotrophic
production and elemental fluxes at 26 degree N, 155 degree W in the North Pacific subtropical
gyre. Deep-Sea Research 36 (1A), 103-120.
Laws, E. A., Falkowski, P. G., Smith, W. O., Ducklow, H., McCarthy, J. J., 2000. Temperature
effects on export production in the open ocean. Global Biogeochemical Cycles 14, 1231-1246.
Lubimova, T. G., Shust, K. V., 1980. Quantitative stuidy of the Antarctic krill consumed by
principal groups of species. In: Lubimova, T. G., Gershanovich, D. E., Popov, L. A., Bogdanov,
A. S. and Neyman, A. A. (Eds.), Biological Resources of the Antarctic Krill (pp. 203-224), AllUnion Research Institute of Marine Fisheries and Oceanography, Moscow.
Malone, T. C., 1971a. The relative importance of nanoplankton and netplankton as primary
producers in tropical oceanic and neritic phytoplankton communities. Limnology and
Oceanography 16, 633-639.
Malone, T. C., 1971b. The relative importance of nanoplankton and netplankton as primary
producers in the California current system. Fishery Bulletin 69, 799-820.
Malone, T. C., Hopkins, T. S., Falkowski, P. G., Whitledge, T. E., 1983. Production and
transport of phytoplankton biomass over the continental shelf of the New York Bight.
Continental shelf research. Oxford, New York NY 1 (4), 305-337.
Mann, K. H., 1984. Fish production in open ocean ecosystems. In: Fasham, M. J. R. (Ed.), Flows
of Energy and Materials in Marine Ecosystems (pp. 435-458), Plenum Press, New York.
Marra, J., Heinemann, K. R., 1987. Primary production in the North Pacific central gyre: some
new measurements based on 14C. Deep-Sea Research Part I 34, 1821-1829.
Martin, J. H., Knauer, G. A., Karl, D. M., Broenkow, W. W., 1987. VERTEX: Carbon cycling in
the Northeast Pacific. Deep-Sea Research 34, 267-285.
McCarthy, J. J., Goldman, J. C., 1979. Nitrogenous nutrition of marine phytoplankton in
nutrient-depleted waters. Science (Wash.) 203 (4381), 670-672.
McCarthy, J. J., Taylor, W. R., Loftus, M. E., 1974. Significance of nanoplankton in the
Chesapeaka Bay estuary and problems associated with the measurement of nanoplankton
productivity. Marine Biology 24, 7-16.
NAS, 1975. Petroleum in the Marine Environment. National Academy of Sciences, Washington,
Parsons, T. R., Giovando, L. F., LeBrasseur, R. J., 1966. The advent of the spring bloom in the
eastern subarctic Pacific Ocean. Journal of the Fisheries Research Board of Canada 23, 539-546.
Parsons, T. R., LeBrasseur, R. J., Fulton, J. D., 1967. Some observtions on the dependence of
zooplankton grazing on the cell size and concentration of phytoplankton blooms. Journal of the
Oceanographical Society of Japan 23, 10-17.
Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., Torres, F., Jr., 1998. Fishing down marine
food webs. Science (Washington) 279 (5352), 860-863.
Pauly, D., Alder, J., Bennett, E., Christensen, V., Tyedmers, P., Watson, R., 2003. The Future for
Fisheries. Science (Washington) 302 (5649), 1359-1361.
Platt, T., Irwin, B. D., 1973. Caloric content of phytoplankton. Limnology and Oceanography 18,
Pomeroy, L. R., 1974. The ocean's food webs: a changing paradigm. BioScience 24, 409-504.
Reeve, M. R., 1970. The biology of chaetognatha. I. Quantitative aspects of growth and
reproduction in Sagitta hispida. In: Steele, J. H. (Ed.), Maarine Food Chains (pp. 168-192),
Oliver and Boyd, New York.
Reid, J. L., Jr., 1965. Intermediate Waters of the Pacific Ocean. John Hopkins Press, Baltimore.
Reutlinger, S., Selowsky, M., 1976. Malnutrition and poverty: Magnitude and policy options,
World Bank Staff, Washington, D.C.
Ryther, J. H., 1969. Photosynthesis and fish production in the sea. Science (Washington) 166
(3901), 72-76.
Ryther, J. H., Dunstan, M. M., 1971. Nitrogen, phosphorus, and eutrophication in the coastal
marine environment. Science (NY) 171, 1008-1013.
Schaefer, M. B., 1965. The potential harvest of the sea. Transactions of the American Fisheries
Society 94, 123-128.
Schmitt, W. K., 1965. The planetary food potential. Annals of the New York Academy of
Sciences 118, 645-718.
Sharp, J. H., Perry, M. J., Renger, E. H., Eppley, R. W., 1980. Phytoplankton rate processes in
the oligotrophic waters of the central North Pacific Ocean. J. Plankton Res. 2 (4), 335-353.
Sieburth, J. M., Smetacek, V., Lenz, J., 1978. Pelagic ecosystem structure: heterotrophic
compartments of the plankton size fractions. Limnology and Oceanography 23, 1256-1263.
Slobodkin, L. G., 1961. Growth and regulation of animal populations. Holt, Rinehart, and
Winston, New York.
Smith, W. O., Barber, R. T., Huntsman, S. A., 1977. Primary production off the coast of
northwest Africa: excretion of dissolved organic matter and its heterotrophic uptake. Deep-Sea
Research Part I 24, 35-47.
Steele, J., 1974. The structure of marine ecosystems. Harvard University Press, Cambridge, MA.
Stockner, J. G., Antia, N. J., 1986. Algal picoplankton from marine and freshwater ecosystems: a
multidisciplinary perspective. Canadian Journal of Fisheries and Aquatic Sciences 43, 24722503.
Takahashi, M., Bienfang, P. K., 1983. Size structure of phytoplankton biomass and
photosynthesis in subtropical Hawaiian waters. Marine biology , Heidelberg 76 (2), 203-211.
Williams, P. J. L., 1981. Incorporation of microheterotrophic processes into the classical
paradigm of the planktonic food web. kieler meeresforschungen sonderheft 5, 1-28.
Wyrtki, K., Kilonsky, B., 1984. Mean water and current structure during the Hawaii-to-Tahiti
shuttle experiment. Journal of Physical Oceanography 14, 242-254.
Young, F. V. K., 1982. The production and use of fish oils. In: Barlow, S. M. and Stansby, M. E.
(Eds.), Nutritional Evaluation of Long-chain Fatty Acids in Fish Oil (pp. 1-23), Academic Press,
New York.