Download Pomeroy, L. R., 1974. The ocean`s food web, a changing paradigm

The Ocean's Food Web, A Changing Paradigm
Author(s): Lawrence R. Pomeroy
Source: BioScience, Vol. 24, No. 9 (Sep., 1974), pp. 499-504
Published by: University of California Press on behalf of the American Institute of Biological Sciences
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The
Ocean's
Food
Web,
A
Changing Paradigm
Lawrence R. Pomeroy
Few of us may ever live on the sea or
under it, but all of us are making
increasing use of it either as a source of
food and other materials, or as a dump.
As our demands upon the ocean increase, so does our need to understand
the ocean as an ecosystem. Basic to the
understanding of any ecosystem is
knowledge of its food web, through
which energy and materials flow. Flux
of both energy and essential elements
shapes or limits ecosystems, but only
energy and organic compounds are considered here. The related problems of
limiting supplies of essential elements
(N, P, Si, Fe) will be considered elsewhere (Pomeroy').
Although the ocean's food web has
been studied for more than a century,
several recent discoveries lead us to
believe that the classical textbook description of a chain from diatoms
through copepods and krill to fishes and
whales may in fact be only a small part
of the flow of energy. Recent studies of
microorganisms, dissolved organic matter, and nonliving organic particles in
the sea suggest the presence of other
pathways through which a major part of
the available energy may be flowing.
Marine scientists have been approaching
this view of the food web cautiously for
decades, and caution is to be expected
whenever an established paradigm is
questioned (Kuhn 1962). Now there are
many lines of evidence which suggest
that a new paradigm of the ocean's food
web is indeed emerging.
Ryther (1969) recognizes three regions
of differing productivity. The open
ocean, with 90% of the total area and
the lowest mean rate of photosynthesis,
accounts for 81.5% of primary production. Coastal waters over the continental
shelves, with 9.9% of the total area and
twice the rate of photosynthesis of the
open ocean, account for 18% of primary
production. The major upwellings, with
0.1% of the total area and a rate of
photosynthesis nearly 10 times that of
the open ocean, account for 0.5% of
primary production. The real accuracy
of these estimates is not as good as the
three digit numbers suggest. The usual
methods of estimating the photosynthetic rate of phytoplankton do not
measure all organic matter produced,
and there is rarely enough replication to
give us confidence limits for the values.
The most obvious plants in the sea
are the seaweeds, but they probably are
not the most significant primary producers. Ryther (1963) estimates that
seaweeds account for 10% of the primary production of the ocean. Recent
data on photosynthetic rates of kelp
and other large seaweeds (Mann 1973)
make that estimate seem high, although
it is still difficult to make a good
estimate on a planetary scale. Certainly,
seaweeds and sea grasses are of major
importance in the coastal zone.
On a planetary scale phytoplankton
are the major producers. Phytoplankton
have been divided into two size groups,
net plankton and nannoplankton. The
separation is arbitrary, based on the
THE ROLESOF MICROORGANISMS aperture of what was once the finest
bolting cloth for making plankton nets.
Net plankton (>60 pm) have received
Photosynthesis
considerable attention and form the
basis of the established paradigm of the
Photosynthesis is the best understood biological process in the ocean.
food web, but nannoplankton (<60 pm)
have proven more difficult to study and
Many thousands of measurements of
until recently they have been neglected.
photosynthesis have been made, fairly
well distributed over the World Ocean.
The author is with the Departmentof Zoology, University of Georgia, Athens, GA
30602.
September 1974
IPomeroy,
L. R. Mineral cycling in marine
ecosystems. In F. G Howell, ed. Mineral Cycling in Southeastern Ecosystems. USAEC
Conf. In press.
Like net plankton, they are so sparsely
distributed in the water that it is necessary to concentrate them in some
fashion to see them at all. Because many
of them cannot be preserved well, they
must be studied at sea while alive. Only
recently has high magnification, oilimmersion microscopy at sea permitted
the study of living nannoplankton
aboard ships.
Efforts to understand the relative
importance of net and nannoplankton
have been made by several investigators,
using the 14C technique (SteemanNielsen 1952), by counting separately
the radioactivity retained on discs of
bolting cloth and on fine membrane
filters. This was a crude separation.
Some organisms larger than the aperture
of the bolting cloth would be forced
through it in fragments, and if a sufficiently thick layer of plankton accumulated on the bolting cloth, nannoplankton would be retained by it. In
spite of these shortcomings, at least a
dozen studies produced consistent results showing that the large diatoms and
other net plankton, although highly
visible and beautiful, account for a small
fraction of total primary production. In
a majority of cases nannoplankton account for more than 90% of total
photosynthesis (Table 1). This is true
not only in the central gyres of the
ocean, but in upwellings, coastal waters,
and estuaries. No one seems to have
made the separation in polar regions.
However, Digby (1953) found that in
Scoresby Sound, Greenland, nannoplankton chlorophyll was always equal
to and sometimes three times as abundant as net plankton chlorophyll.
English (1961) found proportionately
greater amounts of nannoplankton
chlorophyll than net plankton chlorophyll at drift station Alpha in the arctic.
Some remaining doubts about the
validity of the results of physical separation of net plankton from nannoplankton have been dispelled by Watt (1971)
who measured the rates of photosynthesis of individual phytoplankters
499
most of the energy made available by
primary production.
The numerical abundance of various
size classes of heterotrophs has been
examined by Beers, using a plankton
Photosynthesis
Reference
Location
net/nanno
pump which brings water aboard ship
where it passes through a series of fine
meshes (Beers et al. 1967, Beers and
Malone1971
Pacific
Neritic
0.5
Mexico,
Stewart 1969), concentrating organisms
Malone1971
PeruCurrent(Equador)
0.09
Malone1971
E. tropicalPacific
0.12
in several size classes. This work focuses
Malone1971
CaribbeanSea
0.10
on the abundance and description of the
Watt1971
Atlanticslope, May
0.6
smaller heterotrophs, but the results
Watt1971
GrandBanks,August
0.4
imply that the smaller plankton, espeWatt1971
Gulf Stream,400N, August
0.05
cially the microorganisms, should be
Anderson1965
0.04
Washingtonshelf
significant consumers of energy. MicroAnderson1965
0.03
Washingtonslope
organisms as they are discussed in this
Anderson1965
N. Pacific
0.03
paper include all Protista and not
Yentsch& Ryther 1959
Sound
0.02
Vineyard
bacteria alone. Only when bacteria are
Teixeiraet al 1967
0.6
Mangroveestuary
considered specifically will they be so
Ocean
Central
Indian
0.04
1964
Saijo
0.07
E. IndianOcean
called.
Saijo& Takesue1965
0.01
Gilmartin1964
Canadianfjord
New techniques for measuring in situ
0.11
Teixeira1963
TropicalAtlantic
rates of respiration through biochemical
0.4
Holmes& Anderson1963
FridayHarbor,Wash.
techniques offer perhaps the greatest
0.01
Holmes1958
E. tropicalPacific
hope for measuring and understanding
the metabolic processes of microorganisms in the sea. Two of these now
Respiration
by '4C autoradiography. He found that
in use are the measurement of the
in most cases the large diatoms and
of
Weknowmuchlessaboutrespiration electron transport system (ETS)
dinoflagellates showed little photomeathe
and
in the oceanthanaboutphotosynthesis. plankton (Packard 1969)
synthetic activity while nannoplankton
Consumersin the ocean covera much surement of adenosine triphosphate
showed much activity. In the Sargasso
(ATP) content of plankton (Holmbroader spectrum of sizes than proSea one nannoplankton species, CocHansen and Booth 1966). Both methods
ducers do. Even if we dismiss as insignifcolithus huxleyi, appears to be responof organisms on a
icantthe respirationof all marinemam- require concentration
sible for most of the photosynthesis
do not necessarily give any
and
filter
mals (cf. Holdgate 1967), it is still
during most of the year. Far from being
indication of the size or identity of the
net
of
the
the grasses
plankton
sea,
impossible to collect all sizes of organorganisms. Sensitivity is
isms in a single measurementof respira- respiring with
appear to be the Sequoias of the sea,
achieved
enzyme assays. In its
while the major part of photosynthesis
tory rate. Moreover, total respiratory
ETS method measures
the
form
present
is done by C. huxleyi and other nannorate is so low that it is necessary to
in the presence of
activity
potential
concentrate the organisms from a large
plankton.
a rather arbitrary
and
excess
substrates,
volume of water in order to achieve
The relative importance of nannoactual electron
estimate
to
used
is
factor
enough sensitivity to measure changes in
plankton is also suggested by recent
observed
the
from
potential
transport
dissolved oxygen or any other paramstudies of numerical abundance. ConThis introduces an error of unknown
time.
short
a
in
of
of
eter
ventional methods
respiration
studying phytomagnitude. The ATP method was origiAny concentration process has ineviplankton populations from preserved
proposed as a measure of micronally
table uncertainties and difficulties.
samples often result in descriptions of
bial
biomass, but it also shows promise
Despite these difficulties, several in4ominance by a succession of large
as
a
parameter of respiration (Hobbie et
diatom and dinoflagellate species. In
vestigators have made physical separaal.
1972).
tions of two or more size classes of
reality there is usually a constant
All of these approaches to measuring
numerical dominance of nannoplankton
plankton and have measured various
each
size.
biochemical, microscopic,
of
respiration,
of
often
respiration
which are less well preserved and
parameters
collected
suggest that microand
respirometric,
Johannes
and
Semina
(1966)
Pomeroy
1972,
ignored (Bernard 1967,
organisms are major consumers of enorganisms with a No. 2 net (366 pm) and
Steidinger 1973). There is some eviergy in the sea. In the central oceanic
concentrated the smaller organisms (indence that within the nannoplankton
reverse-flow
gyres a significant component of this
is
by
cluding phytoplankton)
(<60 gm) much of the photosynthesis
of
the
may be the respiration of the phytojim
30
respiration
than
smaller
comparing
filtration,
by organisms
plankton. In the gyres growth of phytonet
plankton and microorganisms.
(Holmes and Anderson 1963, Saijo
plankton is limited by the supply of
Several similar studies have since been
1964). However, these separations,
essential elements, and the ratio of
World
of
the
various
in
made
filters
membrane
parts
with
made
which were
photosynthesis to respiration is low.
Ocean (Pomeroy and Johannes 1968,
of different porosities, have been critiIn
Turner
A different approach to the question
1974).
Hobbie et al. 1972,
cized because of the possibility of fragmicroof
the relative significance of net plankof
cases
all
respiration
virtually
mentation of fragile nannoplankton.
ton and microorganisms is that of ShelVerification of the results by microorganisms exceeds that of net plankton
don et al. (1972) who used a particle
and is usually 10 times as great, suggestscopic methods such as Watt's autoare
counter
together with existing data on
consuming
ing that microorganisms
radiography is needed.
TABLE1. Estimates of the relativeimportanceof net phytoplanktonand nannoplanktonin
photosynthesis.Mostof the valuesare mediansof sets of observations.
500
BioScience Vol. 24 No. 9
large organisms to suggest that the
biomass of all size classes of organisms
in the sea, from bacteria to whales, is
about the same. There are problems to
be resolved in discriminating living from
dead particles counted. Some verification of the findings of Sheldon et al. by
an independent method is needed. One
such independent verification within the
size range of net plankton and microorganisms seems to have been provided
by Beers and Stewart (1969), albeit at a
different time in a different part of the
ocean. If the concept of uniform biomass distribution among size classes of
organisms in the ocean is even approximately correct, the inverse relation between size and metabolic rate (Zeuthen
1947) makes the smallest organisms the
largest consumers of energy.
If microorganisms are major consumers in the sea, we need to know
what kinds are the metabolically important ones and how they fit into the
food web. At present we do not even
know the relative abundance of the
various kinds of protists. Few investigators have examined freshly collected
populations of living microorganisms at
sea. Each investigator has used his own
distinctive method with little collaboration or intercomparison. What evidence
we have is filled with contradictions.
Large numbers of small palmelloid
algae, or something of that general
description, have been reported, even at
considerable depth (Bernard 1967).
Other investigators report large populations of bacteria (Kriss 1963, Seki
1972). Still other investigators have
rarely found substantial populations of
these or other recognizable microorganisms (Wiebe and Pomeroy 1972).
Further studies of the systematics,
abundance, and metabolic activity of
the communities of microorganisms of
the open sea are needed to resolve these
conflicting reports.
(Riley 1970, Gordon 1970a and 1970b,
Wiebe and Pomeroy 1972). Several
mechanisms of aggregate formation have
been proposed (Nishizawa 1969, Riley
1970). Recent work suggests that some
aggregates form as the result of the
adherence of soluble organic molecules
to the surface film of bubbles (Wheeler
1972). Other naturally occurring particles are flocculent and may be fecal or
the remains of mucous nets. The proportion of particulate organic matter in
the ocean which consists of authigenic
aggregates, rather than fecal products or
other materials, is not known, but most
particulate organic matter represents
secondary production of one sort or
another. The fate of aggregates and
other particles is uncertain, although
aggregates produced in the laboratory
from natural sea water can support the
growth of zooplankton. It is not known
whether bacteria or other protists can
utilize them, but bacteria rarely are
found attached to them in freshly collected samples of sea water (Wiebe and
Pomeroy 1972).
HeterotrophicConsumptionof
DissolvedOrganicMaterial
The dissolved organic matter in the
World Ocean is one of the largest
reserves of organic carbon on the planet.
Most of it is refractory, with a residence
time of thousands of years (Williams et
al. 1969). Yet we know that perhaps
one-fourth of the organic matter synthesized by marine phytoplankton is lost as
dissolved
material (Anderson and
Zeutschel 1970, Thomas 1971). Most of
this material probably consists of early
products of photosynthesis, such as
glucose or glycolic acid. There is also a
substantial release of dissolved organic
material during digestion, defecation,
and excretion all along the food web
(Webb and Johannes 1967, Corner and
Davies 1971). Some of this probably is
material or its precursors, but
refractory
INDIRECTAND ABIOTICPATHWAYS
most of it is readily assimilable amino
acids and larger protein fragments,
Other Sources of Particulate
and carbohydrates. The imlipids,
OrganicMatter
portance of the production of assimilable dissolved organic material has been
The paradigm of the ocean's food
suggested repeatedly (Khailov 1952,
web is also being changed through recStrickland 1971). In a recent series of
ognition of the potential importance of
papers P.J. leB. Williams and his colmatter
nonliving particulate organic
leagues have shown that these assimiwhich does not come directly from
lable compounds, which may be released
primary production. Nonliving particles
by either plants or animals, are removed
than
more
abundant
are
of several types
from sea water rapidly and efficiently.
living organisms in the sea. Some reWilliams (1970) suggests that the microsemble
aggregates produced from
gram amounts of glucose and amino
natural sea water in the laboratory
September 1974
acids that we find in the sea are the
concentrations below which microorganisms can no longer remove them
efficiently. As soon as photosynthetic
or digestive activities of plankton increase the concentration of any assimilable organic compound, the microorganisms take it up, quickly bringing
the concentration of the assimilable
materials back to the basal concentration. According to Andrews and Williams (1971) direct consumption of
dissolved organic matter may account
for half of the total degradation of
organic matter in the ocean. They estimate that the consumption of glucose
and amino acids by microorganisms
amounted to 35% of total annual
primary production. When glycolate
and other carbohydrates are included,
the total could indeed be 50%. This
is beginning to look like a much
more significant pathway than we had
suspected.
The identity of the microorganisms
which may consume such a major share
of available energy is uncertain, but the
evidence points to bacteria or very small
flagellates. Williams (1970) found that
80% of the microorganisms responsible
for the utilization of soluble organic
compounds would pass through an 8 iim
membrane filter and 50% would pass a
1 pm filter. Here again there are questions about the validity of using membrane filters in this way which should be
answered by autoradiography or electron microscopy.
The production of soluble organic
compounds and utilization of them by
microorganisms occurs in all parts of the
ocean. The percentage of photosynthate
that is lost by phytoplankton in dissolved form varies with their nutritional
state. In the central gyres, where the
supply of essential elements limits
growth, as much as 40% of fixed carbon
is lost as soluble organic compounds,
while in nutrient-rich coastal waters and
upwellings only 10% is lost (Thomas
1971). Although it may seem paradoxical, the largest rate of production of
soluble organic compounds by phytoplankton is in the coastal waters and
upwellings, because 10% of the photosynthesis in upwellings is greater than
40% of the photosynthesis in the central
gyres. It is also in the highly productive
regions of the ocean that respiration is
highest (Pomeroy and Johannes 1966,
1968).
If small Protista are important both
as primary producers and as primary
consumers, this may have implications
501
PARTICULATE
ORGANIC MATTER
ZFECES
AND
D
tEXCRETA
DISSOLVED
NET
ORGANIC
MATTER
ZOOPLANKTON
PHYTOPLANTO N
FISHES
NANNOPL ANKTON
TOP
MUCUS
BACTERIA
NET
CARNIVORES
POMAKERS
PROTOZOA
Fig. 1. The classical paradigm of the ocean's food web in simplified form is
enclosed within the circle. More recently conceived pathways are outside the circle.
The possible relative magnitude of the pathways is discussed in the text.
for the remainder of the food web,
including fisheries. Actively growing
bacteria have high assimilation efficiency. Payne (1970) found assimilation of individual substrates by bacteria
to be around 60% in laboratory cultures
(compared to 10-20% for many larger
organisms). Andrews and Williams
(1971) and others before them found
that the assimilation efficiency for glucose in the sea is as much as 65%, and
the efficiency for assimilation of individual amino acids is nearly 80%. This
strongly suggests that the primary consumers are active bacteria, and that they
are converting a substantial fraction of
primary photosynthate, and secondarily
produced dissolved organic materials as
well, into microbial protoplasm. This
could channel into higher trophic levels
at least 30% more energy than we now
estimate. However, if there are long
periods when no substrates are available,
microorganisms may ultimately respire
all they have assimilated. In this case
there would be a major shunt of high
grade organic energy to heat.
The widely dispersed condition of
bacteria and other small protists presents another problem. They can be
consumed directly by other microorganisms, by mucus-net feeders such as
salps or certain pteropods (Gilmer
1972), and according to laboratory ex502
periments, by some copepods. However,
the highly dispersed condition of the
protists may provide an effective refuge
for them from filter feeders, particularly
for those under 5 gm and in the open sea
where their absolute abundance is lowest. We have quite limited information
on the mean residence time of Protista
in the open sea. If it is very short
(hours), then Protista probably are an
active link in a major pathway in the
food web. If it is long (days or weeks),
the Protista may be consuming most of
the energy they capture. In this case
they will be a major energy sink. Jannasch's (1969) chemostat experiments
with bacteria in natural sea water indicate a generation time for bacteria of
several days. If something like half of
the ocean's total primary production is
really moving through this pathway, we
need to find out whether it is going to
consumers or is lost as CO2.
A NEW PARADIGM
The Web of Consumers
In the classical paradigm of the
ocean's food web (Fig. 1) the primary
consumers are thought to be net zooplankton, such as copepods, mysids, and
euphausiids. The secondary and tertiary
consumers are nekton, including fishes,
cephalopods, and cetaceans. Microorganisms are assigned the role of decomposers (Strickland 1965, p. 585).
Now there is increasing evidence that
net zooplankton are not metabolically
dominant. Microorganisms (whose biomass is approximately equal to that of
the net plankton) are greater movers of
energy and materials because of their
higher metabolic rate per unit mass. The
relative impact of microorganisms and
macroorganisms on the flux of energy in
the sea is still debated. Recent estimates
of the microbial component of respiration vary from 50% (Riley 1972) to
over 90% (Pomeroy and Johannes
1966). Both Strickland (1971) and Raymont (1971)
suggest that microorganisms are a major metabolic component of the oceanic ecosystem, but
they do not attempt to quantify their
importance. Williams (1970) believes
that the most active component has a
size of less than 1 pm while Sheldon et al.
(1973) present evidence that the most
actively growing component has a size
of around 4
/m.
Unseen Strands in the Food Web
The new paradigm of the ocean's
food web that is developing, as a result
of recent studies of protistan activities
and alternative pathways of organic
matter, may contain many unseen
strands. We are not certain how the long
recognized food web of diatoms and
copepods fits into the expanded web
which is gradually appearing. Quantitatively, large diatoms seem to be minor
contributors to production, and net
plankton seem to be a minor component of respiration; but if this is not
the major link of photosynthesis to
nekton, what is? Are the communities
of upwellings really more efficient producers of nekton, and is the food web
really different in them? These questions are important not only to the
basic ecologist but to the fisheries scientist. The flow of useful information
from basic ecology to fisheries research
has been sparse. Fisheries scientists can
predict optimal yields and fish population dynamics with good success, but
relating fish production to processes at
lower trophic levels has been less successful. Strickland (1969) said, "I doubt
if much has been learned [about marine
productivity] of direct help to fishermen that could not have been deduced
equally well from oceanographic data
on currents, convergences, upwellings,
and mixing."
BioScience Vol. 24 No. 9
While this may be an overly pessimistic view of the situation, one must
admit that it is difficult to relate the
production of tertiary consumers to
unidentified primary consumers and
controversial primary producers.
Better strategies for utilizing the productivity of the sea might be devised if
we understood in more detail the pathways of energy transfer and whether
they really differ in the productive and
unprodfuctive regions of the ocean.
Hunting and catching methods for harvesting the wild populations of the sea
have been perfected to the point where
overfishing is possible, and less desirable
populations will have to be exploited to
expand or even sustain fishery yields.
Nothing comparable to terrestrial agriculture has been developed in the sea,
and there is little reason to believe that
it is the best model on which to base
new developments. Harvesting plants,
other than coastal seaweeds, is out of
the question. Monospecies animal cultures comparable to herds and flocks
really do not exist, and only in circumstances where a species segregates itself
(salmon, anchovies) is there immediate
hope of intensive management. Only in
salmon has there been significant progress in developing genetically defined
populations.
Management of existing wild populations now consists at best of controlling
fishing pressure to optimize yield, where
legal and political considerations permit.
Greater yields would be possible if we
could harvest the lower trophic levels,
such as the larger zooplankton. This is
technologically possible, but at existing
population densities it is probably a
poor trade for the energy required to do
it. Enhancement of productivity by
creating artificial upwellings has been
discussed for many years. The technology for accomplishing this still seems
to be marginal and costly, and little
consideration has been given to the
problem of managing the resulting successional changes in natural communities. Our understanding of the
marine food web and the basic principles of stability and diversity of
natural ecosystems is not yet sufficient
for such tasks (cf. Pomeroy2).
At the same time that we are approaching maximal yields from fisheries,
we are forced to cope with increasing
threats to the sea from pollution on a
regional or even global scale. This
creates a tendency to concentrate on
2See footnote 1, p. 499.
September 1974
expensive technological solutions to immediate problems while providing little
support for a better understanding of
how the system works. In the long run,
more satisfactory and probably less
costly solutions can be achieved through
knowledge
gained
through basic
research.
ACKNOWLEDGMENTS
The viewpoint presented in this
paper has developed over several years
of research and discussion with colleagues, particularly Dirk Frankenberg,
Robert E. Johannes, and William J.
Wiebe. They also provided helpful criticism of the manuscript. Research contributing toward the development of
this paper was supported by grants from
the National Science Foundation.
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