CHAPTER 1

LIMITATIONS OF THE MARINE FISH CATCH

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

1609

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

1

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

2

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

3

Figure 1.2 Trends in capture fisheries and aquaculture production since 1992. Source:

http://www.fao.org/fi/statist/statist.asp

Table 1.1 Disposition of the total aquatic catch for 2002

Use % of total catch by weight

Human consumption 75.8

Fresh 39.7

Frozen 20.0

Cured 7.3

Canned 8.7

Reduction 19.0

miscellaneous 5.3

4

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.

Malnutrition

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.

5

Table 1.2 Percentage of persons whose diets are calorie deficient and average caloric supplies as

a percent of minimum requirements.

Region

% of population with calorie-deficient

diets

Average caloric supplies as %

of minimum requirement

Asia and Far East 84-92 94

Middle East 66-71 96

Africa 75-84 90

Latin America 52-57 104

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.

6

Table 1.3 Utilization efficiencies of protein from various food stuffs. Source: FAO (1970)

7

Food Efficiency (%) Amino acids that limit utilization efficiency1

poor adequatedairy

eggs 94 trp, lys, met, cyscow’s milk 82 trp, lyscottage cheese 74 lysswiss cheese 72 lys

meatsfish 83 lysturkey 73 lyspork 67 lysbeef 67 lyschicken 64 lyslamb 64 lys

vegetablescorn 73 trp, lysasparagus 72 met, cysbroccoli 60 met, cyscauliflower 60 met, cys trp, lyspotato 60 met, cys trpkale 53 lys, met, cysgreen peas 51 met, cys lys

cereals and grainsbrown rice 68 lyswheat germ 67 trp lysoatmeal 66 lyswheat grain 59 lysrye 57 trp, thr trppolished rice 57 lys, thr trpmillet 55 lys trp, met, cyspasta 48 lys, met, cys

legumessoybeans 60 met, cys, val lys, trplima beans 50 met, cys trp, lyskidney beans 37 trp, met, cys lyslentils 30 trp, met, cys lys

Nuts and seedssunflower seeds 57 lys trpsesame seeds 52 lys trp, met, cyspeanuts 43 lys, met, cys, thr

1The essential amino acids are cysteine (cys), isoleucine (ile), leucine (leu), lysine (lys), methionine (met),

phenylalanine (phe), threonine (thr), tryptophan (trp), and valine (val)

8

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

9

Table 1.4 World production of fats and oils and the -3 and -6 PFA content of those oils.

Weight percent of total lipids

Source of oil Production (Mt y-1) -3 -6

fish 1.02 13-35 1-4

Linseed 0.96 26-58 5-23

Soybean 14.57 2-10 49-52

Rape seeds 3.54 1-10 10-22

Sunflower 5.43 44-68

Cottonseed 3.29 50

Peanut 3.49 13-34

Olive 1.37 4-15

coconut 3.28 1-3

palm 4.30 6-12

butter 5.10 3

lard 3.80 4-9

tallow 5.87 1-3

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.

10

What Limits Production?

Observations

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.

Theory

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

11

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

1 Depth where the net photosynthetic rate equals zero

12

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

2 aphotic zone

Permanent pycnocline

Sea surface

sinking

Excretion, death, and

sinking

grazing

Upwelling and turbulent diffusion

regeneration

phytoplankton

herbivores

carnivores

Winter mixed layer

dissolved nutrients

Nutrients in detritus

dissolved nutrients

grazing

13

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 50-

100 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. 1.4-

1.5, 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

14

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)

15

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)

16

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

17

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).

18

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

19

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.

comm.)

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

20

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

3 A petagram is 1015 grams.

21

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)

Province % of ocean

Area

(1012 m2)

Mean

production

(gC m-2 y-1)

Global

production

(Pg C y-1)

% of primary

production

Open ocean 90.0 326 130 42.38 82

Coastal zone 9.9 36 250 9.00 18

upwelling 0.1 0.36 420 0.15 0.4

total 100 362 142 51.53 100

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

22

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

organisms.

23

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

113 226

Algal picoplankton and nanoplankton (42,380)

Flagellates (8,476)

Ciliates (1,695)

Crustacean zooplankton (339)

Mesopelagic vertical migrators (45.2)Chaetognaths, micronekton (22.6)

Small tuna, salmon, squid (3.39)

Large tuna, sharks, billfish (0.51)

Trophic level

1

2

3

4

5

6

7

24

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 0.08-

0.16 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

25

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

26

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.

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

2816.316.3

102306

29

20

97

225408

1,800

6,0001,200

phytoplankton (9,000)

flagellates (1,200)

ciliates (240)

crustacean zooplankton (408)

invertebrate carnivores (61)

bacteria (322) meiobenthos (19)

macrobenthos (49) epifauna (4)

pelagic fish (32.6) demersal fish (10)

large demersal fish (0.4)

natural mortalityand fishing

27

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

28

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

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.

4 The coefficient of variation is the standard deviation divided by the mean value.

2.36.8

64.5

42.75

phytoplankton (150)

flagellates (12.9)

ciliates (2.6)crustacean

zooplankton (9.1)

invertebrate carnivores (1.4) pelagic fish (9.3)

natural mortality and fishing

42.75

29

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 flagellate-ciliate 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) Fresh weight (Mt)

Open ocean 3.9 39

Coastal zone

Pelagic 32.6 326

Demersal 10.4 104

Upwelling 9.3 93

30

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.

31

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”.

32

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

zooplankton.

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

33

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,

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

18,163

31

6.21

0.9

4.65

31

470

2,351

11,754

157 313

2,351

11,754

42,380algal picoplankton and nanoplankton (60,543)

flagellates (11,754)

ciliates (2,351)

crustacean zooplankton (470)

mesopelagic vertical migrators (63)chaetognaths, micronekton (31)

small tuna, salmon, squid (4.65)

large tuna, sharks, billfish (0.7)

bacteria (16,388)

DOC (32,776)

34

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%.

35

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

36

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

F = G – M (1)

37

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.

38

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

39

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

year.

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

40

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

countries?

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.

41

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,

42

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

43

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.

44

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